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Fungal Biology

Ram Prasad Editor

Mycoremediation and Environmental Sustainability Volume 1

Fungal Biology

Series Editors Vijai Kumar Gupta Department of Chemistry and Biotechnology Tallinn University of Technology Tallinn, Estonia Maria G. Tuohy School of Natural Sciences National University of Ireland Galway Galway, Ireland

About the Series Fungal biology has an integral role to play in the development of the biotechnology and biomedical sectors. It has become a subject of increasing importance as new fungi and their associated biomolecules are identified. The interaction between fungi and their environment is central to many natural processes that occur in the biosphere. The hosts and habitats of these eukaryotic microorganisms are very diverse; fungi are present in every ecosystem on Earth. The fungal kingdom is equally diverse, consisting of seven different known phyla. Yet detailed knowledge is limited to relatively few species. The relationship between fungi and humans has been characterized by the juxtaposed viewpoints of fungi as infectious agents of much dread and their exploitation as highly versatile systems for a range of economically important biotechnological applications. Understanding the biology of different fungi in diverse ecosystems as well as their interactions with living and non-living is essential to underpin effective and innovative technological developments. This series will provide a detailed compendium of methods and information used to investigate different aspects of mycology, including fungal biology and biochemistry, genetics, phylo genetics, genomics, proteomics, molecular enzymology, and biotechnological applications in a manner that reflects the many recent developments of relevance to researchers and scientists investigating the Kingdom Fungi. Rapid screening techniques based on screening specific regions in the DNA of fungi have been used in species comparison and identification, and are now being extended across fungal phyla. The majorities of fungi are multicellular eukaryotic systems and therefore may be excellent model systems by which to answer fundamental biological questions. A greater understanding of the cell biology of these versatile eukaryotes will underpin efforts to engineer certain fungal species to provide novel cell factories for production of proteins for pharmaceutical applications. Renewed interest in all aspects of the biology and biotechnology of fungi may also enable the development of “one pot” microbial cell factories to meet consumer energy needs in the 21st century. To realize this potential and to truly understand the diversity and biology of these eukaryotes, continued development of scientific tools and techniques is essential. As a professional reference, this series will be very helpful to all people who work with fungi and should be useful both to academic institutions and research teams, as well as to teachers, and graduate and postgraduate students with its information on the continuous developments in fungal biology with the publication of each volume. More information about this series at http://www.springer.com/series/11224

Ram Prasad Editor

Mycoremediation and Environmental Sustainability Volume 1

Editor Ram Prasad Amity Institute of Microbial Technology Amity University Noida, UP, India

ISSN 2198-7777 ISSN 2198-7785 (electronic) Fungal Biology ISBN 978-3-319-68956-2 ISBN 978-3-319-68957-9 (eBook) https://doi.org/10.1007/978-3-319-68957-9 Library of Congress Control Number: 2017962335 © Springer International Publishing AG 2017 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

The buildup of toxic chemicals and heavy metals in the environment is an ever- increasing and serious problem. These toxins threaten humans, animals, and the present ecosystem. Fungi feature among nature’s most vital agents for the decomposition of waste matter and are crucial components of the soil food web, providing nourishment for the supplementary biota that live in the soil environment. The degree of sustainability of the physical environment is an index of the survival and well-being of all-inclusive components in it. Additionally, it is not sufficient to try disposing toxic/deleterious substances with any known method. The best method of sustaining the environment is such that returns back all the components (wastes) in a recyclable way so that the waste becomes useful and helps the biotic and abiotic relationship to maintain an aesthetic and healthy equilibrium that characterizes an ideal environment. Researchers have been able to tailor fungal strains to neutralize toxic weapons and waste. Research is being done to use mycoremediation in the field of national defense against chemical and biological warfare and used to help mend war-torn environments. Mycoremediation practices involve mixing mycelium (the vegetative part of a fungus) into contaminated soil, placing mycelial mats over toxic sites, or a combination of these techniques in one or more treatments. Toxins in our food chain (including heavy metals, PCBs, and dioxins) become more concentrated at each step, with those at the top being contaminated by ingesting toxins consumed by those lower on the food chain. Fungal mycelia can destroy these toxins in the soil before they enter our food supply. This book should be enormously advantageous for botanists, researchers, technocrats, policy makers, and scientists of fungal biology and those who are interested in environmental suitability. I am honored that the leading scientists who have extensive, in-depth understanding and expertise in fungal biology and environmental concern took the time and effort to develop these outstanding chapters. Each chapter is written by internationally recognized academicians so the reader is given an up-to-date and detailed account of our knowledge of the fungal system and innumerable applications of fungi.

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Preface

We are indebted to the many people who helped to bring this book to light. I wish to thank series editors Dr. Vijai Kumar Gupta and Dr. Maria G. Tuohy and Eric Stannard, senior editor of Botany, Springer, for generous assistance, constant support, and patience in initializing the volume. Special thanks go to my exquisite wife Dr. Avita Maurya for her continuous support and inspirations in putting everything together. Dr. Prasad in particular is very thankful to Professor Ajit Varma, Amity University, for the kind support and constant encouragement. Special thanks are due to my esteemed friend and well-wisher Mr. Manjit Kumar, kith and kin, and all faculty colleagues of AIMT, Amity University. Noida, Uttar Pradesh, India

Ram Prasad

Contents

1 Fungal Bioremediation as a Tool for Polluted Agricultural Soils�� 1 Sandra Pérez Álvarez, Marco Antonio Magallanes Tapia, Bernardo Nayar Debora Duarte, and María Esther González Vega 2 Marine-Derived Fungi: Prospective Candidates for Bioremediation �� 17 Anjana K. Vala and Bharti P. Dave 3 Biofilm: A Next-Generation Biofertilizer�� 39 Talat Parween, Pinki Bhandari, Zahid Hameed Siddiqui, Sumira Jan, Tasneem Fatma, and P.K. Patanjali 4 Fungi: A Remedy to Eliminate Environmental Pollutants�� 53 Sunita J. Varjani and Rajal K. Patel 5 Mycoremediation: Decolourization Potential of Fungal Ligninolytic Enzymes�� 69 Hesham A. El Enshasy, Siti Zulaiha Hanapi, Soad A. Abdelgalil, Roslinda Abd Malek, and Avnish Pareek 6 Long-Time Corrosion of Metals and Profiles of Fungi on Their Surface in Outdoor Environments in Lithuania �� 105 Elena Binkauskienė, Dalia Bučinskienė, and Albinas Lugauskas 7 Mycoremediation: An Eco-friendly Approach for Degradation of Pesticides�� 119 Geeta Bhandari 8 Mycoremediation of Heavy Metal and Hydrocarbon Pollutants by Endophytic Fungi �� 133 Rashmi Mishra and V. Venkateswara Sarma 9 Fungal-Mediated Solid Waste Management: A Review �� 153 Abhinav Jain, Shreya Yadav, Vinod Kumar Nigam, and Shubha Rani Sharma vii

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Contents

10 Mycoremediation: A Step Toward Cleaner Environment�� 171 Vankayalapati Vijaya Kumar 11 Arbuscular Mycorrhizal Fungi Provide Complementary Characteristics that Improve Plant Tolerance to Drought and Salinity: Date Palm as Model�� 189 Ahmed Qaddoury 12 Applications of Haloalkaliphilic Fungi in Mycoremediation of Saline-Alkali Soil�� 217 Shi-Hong Zhang and Yi Wei Index�� 235

Contributors

Soad A. Abdelgalil Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia City of Scientific Research and Technological Applications, Alexandria, Egypt Sandra Pérez Álvarez Instituto Politécnico Nacional, CIIDIR-IPN, Unidad Sinaloa, Departamento de Biotecnología Agrícola, Guasave, Sinaloa, México Geeta Bhandari Sardar Bhagwan Singh Post Graduate Institute of Biomedical Sciences and Research Balawala, Dehradun, Uttarakhand, India Pinki Bhandari Institute of Pesticide Formulation Technology, Gurgaon, India Elena Binkauskienė State Research Institute Center for Physical Sciences and Technology, Vilnius, Lithuania Dalia Bučinskienė State Research Institute Center for Physical Sciences and Technology, Vilnius, Lithuania Bharti P. Dave Department of Life Sciences, Maharaja Krishnakumarsinhji Bhavnagar University, Bhavnagar, India Bernardo Nayar Debora Duarte Instituto Politécnico Nacional, CIIDIR-IPN, Unidad Sinaloa, Departamento de Biotecnología Agrícola, Guasave, Sinaloa, México Hesham A. El Enshasy Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia Faculty of Chemical Engineering and Energy, Universiti Teknologi Malaysia, Johor Bahru, Malaysia City of Scientific Research and Technological Applications, Alexandria, Egypt Tasneem Fatma Department of Bioscience, Jamia Millia Islamia, New Delhi, India Siti Zulaiha Hanapi Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia ix

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Contributors

Abhinav Jain Department of Bio-Engineering, Birla Institute of Technology, Mesra, Ranchi, India Sumira Jan ICAR-Central Institute of Temperate Horticulture, Srinagar, India Vankayalapati Vijaya Kumar Core Green Sugar and Fuels Private Limited, Tumkur Village, Shahapur Taluk, Yadgir District, Karnataka, India Albinas Lugauskas State Research Institute Center for Physical Sciences and Technology, Vilnius, Lithuania Roslinda Abd Malek Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia Rashmi Mishra Department of Biotechnology, Pondicherry University, Pondicherry, India Vinod Kumar Nigam Department of Bio-Engineering, Birla Institute of Technology, Mesra, Ranchi, India Avnish Pareek Department of Applied Biotechnology, College of Applied Sciences, Ministry of Higher Education, Sur, Sultanate of Oman Talat Parween Institute of Pesticide Formulation Technology, Gurgaon, India P.K. Patanjali Institute of Pesticide Formulation Technology, Gurgaon, India Rajal K. Patel Gujarat Ecological Education and Research, Foundation, Indroda Nature Park, Gandhinagar, Gujarat, India Ahmed Qaddoury Plant Biotechnology & Agrophysiology of Symbiosis, Department of Biology, FST, University Cadi Ayyad, Marrakesh, Morocco Shubha Rani Sharma Department of Bio-Engineering, Birla Institute of Technology, Mesra, Ranchi, India Zahid Hameed Siddiqui Department of Biology, University of Tabuk, Tabuk, Kingdom of Saudi Arabia Marco Antonio Magallanes Tapia Instituto Politécnico Nacional, CIIDIR-IPN, Unidad Sinaloa, Departamento de Biotecnología Agrícola, Guasave, Sinaloa, Mexico Anjana K. Vala Department of Life Sciences, Maharaja Krishnakumarsinhji Bhavnagar University, Bhavnagar, India Sunita J. Varjani School of Biological Sciences and Biotechnology, Indian Institute of Advanced Research, Gandhinagar, Gujarat, India María Esther González Vega Instituto Nacional de Ciencias Agrícolas (INCA), San José de las Lajas, Mayabeque, Cuba V. Venkateswara Sarma Department of Biotechnology, Pondicherry University, Pondicherry, India

Contributors

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Yi Wei College of Plant Sciences, Jilin University, Changchun, China Shreya Yadav Department of Bio-Engineering, Birla Institute of Technology, Mesra, Ranchi, India Shi-Hong Zhang College of Plant Sciences, Jilin University, Changchun, China

About the Editor

Ram Prasad, Ph.D. is assistant professor at the Amity Institute of Microbial Technology, Amity University, Uttar Pradesh, India. His research interest includes plant-microbe interactions, fungal biology, sustainable agriculture, and microbial nanobiotechnology. Dr. Prasad has more than hundred publications to his credit, including research papers and book chapters and five patents issued or pending, and has edited or authored several books. Dr. Prasad has 12 years of teaching experience, and he has been awarded the Young Scientist Award (2007) and Prof. J. S. Datta Munshi Gold Medal (2009) by the International Society for Ecological Communications, the FSAB fellowship (2010) by the Society for Applied Biotechnology, the Outstanding Scientist Award (2015) in the field of microbiology by Venus International Foundation, UICC Fellows (USA, 2015), and the American Cancer Society UICC International Fellowship for Beginning Investigators (USA, 2014). In 2014–2015, Dr. Prasad served as visiting assistant professor in the Department of Mechanical Engineering at Johns Hopkins University, USA.

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Chapter 1

Fungal Bioremediation as a Tool for Polluted Agricultural Soils Sandra Pérez Álvarez, Marco Antonio Magallanes Tapia, Bernardo Nayar Debora Duarte, and María Esther González Vega

1.1 Introduction Agriculture means cultivation of plants and fungi for food, medicine, fiber, biodiesel, and other products used to sustain human life, drive the economy of the countries, and be a source of life for majority of people living in developing nations; also, it embellishes the landscape of the region where it is practiced. This activity uses almost two thirds of the water for human use and the greater proportion of land use on our planet (ILO 2011; Arias-Estévez et al. 2008; FAO 2009). World population continues to increase, and therefore the demand for agricultural products will continue to grow, so it is estimated that there could be a decrease in the world food production in the future (Bayoumi and Patkó 2010; FAO 2009).

1.2 The Effect of Agriculture in the Environment Agriculture has a direct impact on biodiversity loss and the degradation of land and water. As agricultural production increases due to the demand for agricultural products and its derivatives, problems are generated to the environment to erroneous using of chemicals, irrigation, and plant hormone applications, among others. Likewise, agriculture is the main source of water pollution by phosphates, nitrites, and pesticides; the latter has increased in the last 35 years. Also it affects the basis of its own future through land degradation, salinization, over-abstraction of water, S.P. Álvarez (*) • M.A.M. Tapia • B.N.D. Duarte Instituto Politécnico Nacional, CIIDIR-IPN, Unidad Sinaloa, Departamento de Biotecnología Agrícola, Guasave, Sinaloa, México e-mail: [email protected] M.E.G. Vega Instituto Nacional de Ciencias Agrícolas (INCA), San José de las Lajas, Mayabeque, Cuba © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_1

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reduction of agricultural genetic diversity, soil diversity, and organic matter in the world (EEA 2003; Walls 2006; Loebenstein and Thottappilly 2007; Arias-Estévez et al. 2008; Önder et al. 2011; FAO 2009).

1.2.1 Eutrophication of Waters Eutrophication can be defined (OECD 2012) as the increase in the rate of production and accumulation of organic carbon in excess of what an ecosystem is normally capable of processing. It is a product of complex interactions between temperature, nutrient loading, flow rate, and other biological and geochemical factors. Symptoms include: • Excessive phytoplankton and macro algal growth at the water surface which may reduce light penetration and cause decline of submerged aquatic vegetation • An imbalance in nutrient ratios that can lead to a shift in phytoplankton species composition, creating favorable conditions for toxic algal blooms • Changes in benthic species composition leading to reduced diversity and effects on the food web • Low dissolved oxygen and formation of hypoxic waters (dead zones) in coastal and marine settings Eutrophication according to agricultural practices is induced by phosphorus and nitrogen applied to land, accumulated in soil, and moved to an aquatic ecosystem (such as lakes and rivers) by direct runoff, erosion, and spray drift, where the population of algae and phytoplankton increases considerably as a result of the concentrations of these chemical nutrients which stimulate its growth (well-nourished or eutrophic). As the population of these organisms increases, the oxygen of the aquifer is consumed and thus the death of the benthic organisms by the anoxic conditions of the place (Vollenweider 1968; Edmondson 1995; Carpenter et al. 1998; Rial-Otero et al. 2003). Modification of eutrophication of inland waters in North America has focused on the reduction of phosphate loadings because it could be a limiting factor in spurring algal growth in fresh waters, partly due to the ability of some alga to synthesize nitrogen from the air, so after many years of debate about the primary factors of coastal eutrophication, the present consensus is that nitrogen is the major limiting factor controlling algal blooms (Howarth 2006). Nitrogen export to the Yellow Sea (China) and the North Sea (Europe) is 10–15 times on natural levels and on average 6 times natural loads to US coastal waters. Agriculture is now the main source of nitrogen in Europe and the USA as 90 and 66% of urban wastewater is treated. By contrast, sewage contributes 33% of riverine nitrogen in China, compared to only 12% in the USA (MA 2005).

1 Fungal Bioremediation as a Tool for Polluted Agricultural Soils

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Fig. 1.1 Global carbon dioxide emissions by region, 1990–2012 (WRI 2015)

1.2.2 Climate Change and Emissions of Greenhouse Gases Increasing emissions of greenhouse gases due to human activities worldwide have led to a substantial increase in atmospheric concentrations of long-lived and other greenhouse gases (see the Atmospheric Concentrations of Greenhouse Gases indicator). Every country around the world emits greenhouse gases into the atmosphere, meaning the root cause of climate change is truly global in scope. Some countries produce far more greenhouse gases than others, and several factors – such as economic activity (including the composition and efficiency of the economy), population, income level, land use, and climatic conditions – can influence a country’s emission levels. Tracking greenhouse gas emissions worldwide provides a global context for understanding the USA’s and other nations’ roles in climate change (EPA 2016). The carbon dioxide emissions from 1990 to 2012 for different regions of the world can be seen in Fig. 1.1. According to WRI (2015) these totals do not include emissions or sinks related to land-use change or forestry. Inclusion of land-use change and forestry would increase the apparent emissions from some regions while decreasing the emissions from others. As the climatic conditions affect agriculture, this activity influences the environment. The increase in temperature, droughts, storms, and floods caused by climate change adversely impacts agricultural production and its traditional systems in the world; however, a high percentage (25%) of greenhouse gases emissions is caused by the agriculture, derived from the digestion of the rumiant animals that emits methane gas (CH4) to the environment and the decomposition of manure and organic matter of the soil that produces nitrous oxide (N2O) and also fertilizer use and

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d eforestation. Also, forests collect a high percentage of the atmospheric carbon (C), and the destruction of the same ones for use of agricultural land implies that the majority of this gas is released toward the atmosphere (Olesen 2006; Walls 2006; Önder and Kahraman 2010; FAO 2009).

1.2.3 Pollution of Groundwater by Leaching of Nutrients Pollution of water is one of the principal environmental problems, and nitrate is among the most common and widespread pollutants in groundwater together with wastes and chemicals. Although the movement of groundwater through the aquifer can easily remove a lot of impurities from the water by filtering it through the porous rocks, many of those impurities are contaminants which are not easily degraded in the subsurface like nitrate which is impounded into the groundwater by agricultural activities (fertilizers, livestock manure, and so on). Since nitrate is soluble and negatively charged, it has high mobility and is thus easily leached from the unsaturated zone (Vinod et al. 2015). The most important physical process involved in possible nitrate contamination is leaching into groundwater by rain or irrigation water infiltrating through the soil down to the groundwater table, so the nitrate that is not used by the crops, immobilized by bacteria into soil organic matter or converted to atmospheric gases by denitrification, can leach from the root zone and possibly end up in groundwater leading to the pollution problems (Galloway et al. 2004). It is a fact that the contamination of groundwater quality deterioration by pesticides and nutrients (potassium, nitrate, magnesium, chloride, and calcium) is a serious threat to human health, aquatic fauna, and ecosystem in many countries due to their leaching and infiltration into soil and water. These chemicals will remain in the soil depending on their degradation time and environmental conditions at the time of its application (Hamilton and Shedlock 1992; Bayoumi and Patkó 2010; Aravinna et al. 2017).

1.2.4 Pollution and Soil Degradation Soil degradation has been defined as a change in the soil health status resulting in a diminished capacity of the ecosystem to provide goods and services for its beneficiaries, while land degradation encompasses all the negative changes in the capacity of the ecosystem to provide goods and services (FAO 2014). The indiscriminate use of pesticides and fertilizers in agricultural activity has a significant impact on the soil, resulting in salinization or acidification. In addition, agriculture generates soil degradation due to erosion, which affects all soil properties, loss of soil biodiversity, fertility, and organic matter (EEA 2003; Walls 2006; Loebenstein and Thottappilly 2007; Arias-Estévez et al. 2008).


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1.2.5 Polluted Agricultural Soil Scenario Soil resources represent a great importance not only for human health but also for the environmental, so at present the world is facing a global soil crisis (Zhu and Meharg 2015). Soils are a fundamental part of our planet because water resources go through soil, soil is a substrate for plants, and the flora and fauna of the planet are associated to it, so the biodiversity depends on this resource (Montanarella and Vargas 2012). Usually, 1 g of soil contains up to one billion bacterial cells and 200 m fungal hyphae (Roesch et al. 2007). In soil biota the turnover of organic matter occurs and also the transformation of nutrients, such as nitrogen and phosphorus, and these nutrients are an essential part of soil quality. The role of soil biota in plant growth and, hence, productivity is now well known (Wardle et al. 2004). Some authors suggest that change in the soil biota has the potential to improve or hinder the success of revegetation on retired agricultural land, but enrichment of soil by decomposition of nitrogen, for example, rich litter in these sites, requires longer than the 8–15 years since they were revegetated (Bourne et al. 2008). Exhaustive plant breeding of the last decade has made crops highly dependent of fertilizers and pesticides, while the diversity needed to accomplish nutrient-limiting soil conditions has been lost due to change of traditional crops, which were selected over millennia for use in ecosystems with low nutrient input (Gamuyao et al. 2012). At present many evidences are supporting the hypothesis that the productivity of terrestrial ecosystems and their multifunctionality are determined by soil biodiversity and biological community composition (van der Heijden et al. 2008; Wagg et al. 2014). These days industry development continues to increase and also release agrochemicals into the environment with the consequent accumulation of heavy metals in agricultural soils causing a growing public concern about food security worldwide (Wong et al. 2002). Heavy metals can pose long-term environmental and health implications because of their nonbiodegradability and persistence (Zhao et al. 2011). The physical process most important sources of heavy metals in the environment are the anthropogenic (human activities) such as industrial production, mining, smelting procedures, agriculture, steel and iron industry, and transportation chemical industry as well as domestic activities that release high amounts of heavy metals into surface and groundwater, into soils, and ultimately to the biosphere (Jantschi et al. 2008; Pantelica et al. 2008; Abbas et al. 2011). Some crops, like those that belong to the Solanaceae family (Shilev and Babrikov 2005), can accumulate great amounts of heavy metals, so this problem is of great concern due to the probability of food contamination through the soil root interface (Shilev and Babrikov 2005, Abbas et al. 2011). Heavy metals like cadmium (Cd), lead (Pb), chromium (Cr), nickel (Ni), silver (Ag), and copper (Cu) are not essential for plant growth, but they can be taken by them and accumulated in toxic forms, so the ingestion of these plants represents a possible risk to human health and wildlife. Numerous studies show that the use of waste water contaminated with heavy metals for irrigation over

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long period of time increases the heavy metal contents of soils above the permissible limit. Ultimately, increasing the heavy metal content in soil also increases the uptake of heavy metals by plants depending upon the soil type, plant growth stages, and plant species (Abbas et al. 2011). Remediation of natural resources contaminated with heavy metals like soil and water has become ineffective and costly; however, bioremediation is a cost-effective way. Bioremediation is efficient and an environmentally friendly method for decontamination (soil and water), and mycoremediation used fungi to degrade or sequester contaminants in the environment. Fungi are present in aquatic sediments, terrestrial habitats, and water surfaces and play a significant role in natural remediation of heavy metals (Dugal and Gangawane 2012).

1.3 A dvances, Challenges, and Potential of Fungal Bioremediation Microorganisms and plants could be used for remediation as a sustainable remediation technology to rectify and reestablish the natural condition of soil. However, the presence of heavy metals in agricultural soil causes considerable modification of the microbial community, regardless of their importance for the growth of microorganisms at relatively low concentrations (Doelman et al. 1994). Modification of the microbial community is mainly through an inhibitory action by blocking essential functional groups, displacement of essential metal ions, or modification of active conformations of biological molecules (Li and Tan 1994; Wood and Wang 1983). It is also important to know that the response of microbial communities to heavy metals depends on the concentration and availability of them and is a complex process that is controlled by several factors, such as the type of metal and the nature of the medium and microbial species (Goblenz et al. 1994). Bioremediation of heavy metal through microbial treatment has many advantages including being friendly with the environment, being specific, self-reproducibility, recycling of bioproducts, and so on. This method has some disadvantages; one is the slowness of the processes, and the other one is the difficulty in controlling it. Nevertheless, microbial processes represent the most logical, long-term solution for remediation. With the increase of heavy metal accumulation in many areas of the world, it is a great challenge to know better and deeply the existing microbial that can be used for bioremediation processes to a commercial level (Banik et al. 2014). Another disadvantage of bioremediation is that some microorganisms cannot break toxic metals into harmless metabolites, so these have inhibitory effects on microbial activity (Dixit et al. 2015). Undoubtedly, current crop production has contributed to environmental pollution mainly due to the indiscriminate use of agrochemicals and soil degradation, and in the next 30 years, these environmental problems will continue. This has caused a latent concern in the pollution that the agricultural activity generates to the


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e nvironment; therefore, recent studies have focused on soil bioremediation, where the potential of the fungi Trichoderma sp., Beauveria bassiana, and Paecilomyces lilacinus, has been documented. In this sense, it is extremely important to focus studies on the search for new species that present this ability to mitigate or eradicate environmental pollution, particularly on agricultural soils, where the impact has been on a larger scale (Tixier et al. 2001; Gupta et al. 2007; Tripathi et al. 2013; FAO 2009). Future research must be focused in improving in situ bioremediation strategies using genetically engineered microorganisms (GEM) and also study the application and adaptation of those microorganisms to extreme conditions (stress) with great quantities of heavy metals (Dixit et al. 2015).

1.4 Bioremediation of Soils by Fungi Microorganisms are known to immobilize heavy metal ions by linking them with their cell walls (Vankar and Bajpai 2008); also they can use those contaminants as a source of nutrients and energy and convert them into soluble substances (Kumar et al. 2008). The phytoremediation process can be intensified by the presence of microorganism enhancing phytostimulation or rhizodegradation (Kavamura and Esposito 2010). Fungi are useful for bioremediation of places contaminated with heavy metals because their biomass content has high percentage of cell wall materials which offers excellent metal-binding properties (Mann 1990; Muraleedharan et al. 1991). The cell walls of fungi can be a cation exchanger due to their negative charge (Fomina et al. 2007). Additionally the use of fungal biomasses as biosorption materials is very convenient because of their inexpensive production methods based on simple fermentation techniques (Maurya et al. 2006). Fungi are important in the natural environment due to their decomposition, transformation, and nutrient cycling (Archana and Jaitly 2015).

1.4.1 Trichoderma sp. The Trichoderma fungi are commonly found in all types of soils, and some of them have the ability to clean polluted environments, such as soils and water, so they can be effective fungi for bioremediation (Vankar and Bajpai 2008). Several studies have shown the role of Trichoderma for bioremediation. This fungus can remove and concentrate ions, such as Pb, Cd, Cu, Zn, and Ni, and the main mechanism recognized for the uptake was sorption (Yazdani et al. 2009; Srivastava et al. 2011). T. viride, for example, can be used to remove Cd and Pb from aqueous media (Asha Sahu et al. 2012). T. asperellum and T. viride can remove arsenic from liquid media through biovolatilization in laboratory conditions

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(Srivastava et al. 2011). Trichoderma asperellum, T. harzianum, and T. tomentosum were studied for removing Cd under different pH conditions, and authors found that the optimal removing was obtained 91.06% (10.95 mg/g based on fungus dry weight) for T. asperellum, 83.92% (9.85 mg/g based on fungus dry weight) for T. harzianum, and 82.63% (5.48 mg/g based on fungus dry weight) for T. tomentosum at the pH = 9; all the data represented decreasing of Cd in the experimental samples compared to control ones (Mohsenzadeh and Shahrokhi 2014). Some other Trichoderma species like Trichoderma atroviride are reported to influence uptake and translocation of Ni, Zn, and Cd in Brassica juncea, while T. harzianum was reported to promote growth of crack willow (Salix fragilis) in metal-contaminated soil (Adams et al. 2007). Tripathi et al. (2013) demonstrated that Trichoderma-inoculated chickpea plants were healthier than the uninoculated control during arsenic (As) exposure. Some mechanisms that Trichoderma can use to diminish metal stress in plants are recognized to enhanced root biomass production, hyperaccumulation of toxicants in plant, tissues protection against oxidative damage, and enhanced nutrient availability and efficiency (Mastouri et al. 2010).

1.4.2 Beauveria bassiana (Bals.) Vuill. Biosorption is the main principle for bioremediation that uses primarily amino, carboxyl, hydroxyl, and carbonyl groups of the cell wall for metal binding as elucidated by FTIR (Fourier transform infrared spectroscopy) analysis, and it is used by the fungus B. bassiana (Tomko et al. 2006). According to Kameo et al. (2000), B. bassiana accumulated Cu in the mycelia, and a Cu-metallothionein [MTs are low molecular weight, unique cysteine-rich metal-binding proteins (Nordberg et al. 1972; Kojima et al. 1976)] was induced. In the same experiment, B. bassiana accumulated Cd in the mycelia, and the elution profile showed very similar pattern to a Cu-binding protein and revealed the existence of a low molecular weight, Cd-binding protein; finally exposure to cadmium may cause to induce an MT (class II type of MT) which might be family 8 according to a new classification in the fungus B. bassiana (Kameo et al. 2000). B. bassiana, according to Tomko et al. (2006), is reported to efficiently adsorb Cd and Pb from aqueous metal solutions, and physicochemical factors such as pH and contact time at room temperature can affect the rate of metal biosorption for this fungus. Purchase et al. (2009) demonstrated that B. bassiana, isolated from constructed wetlands receiving urban runoff, accumulated up to 0.64% of available Zn (zinc) and 8.44% of Pb. They suggested, according to transmission electron microscopy and emission dispersion X-ray spectrophotometry, that the mechanism of resistance in B. bassiana may be associated with the precipitation of Pb (possibly in the form of oxalates). Besides biosorption, immobilization and precipitation could be used by fungal species for uptake of heavy metals. Other processes can be reductive


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metal precipitation such as synthesis of metallic nanoparticles. According to this B. bassiana has the ability of heavy-metal chelation using oxalates as organic chelators for iron directly sequestered on the fungal hyphae, copper with the formation of characteristic “Liesegang rings,” and silver with coprecipitation of copper and silver oxalates (Joseph et al. 2012). Gola et al. (2016) tested the growth kinetics and heavy metal removal ability of B. bassiana in individual and multi metals, and the specific growth rate varied from 0.025 h1 to 0.039 h−1, so FTIR analysis showed the connection of different surface functional groups in biosorption of several metals, while cellular changes in fungus were reflected by different microscopic analyses such as scanning electron microscopy, atomic force microscopy (showed increases in cell surface roughness in fungal cells exposed to heavy metals), and transmission electron microscopy (revealed removal of heavy metals via sorption and accumulation processes). This research is the first report of bioremediation’s mechanism of individual and mixture of heavy metals by entomopathogenic fungi. Researchers have proved that B. bassiana through biosorption can bioremediate some metals such as Pb, Cd, C, and Zn.

1.4.3 Paecilomyces lilacinus (Thom) Samson Paecilomyces lilacinus (Deuteromycotina/Hyphomycetes) is an entomopathogenic fungi presently receiving attention for its potential in biological control programs. P. lilacinus is usually isolated from soil, particularly in samples originating from warmer regions (Domsch and Gams 1980). Furthermore, this fungus has been found infecting a range of different hosts (Samson 1974) and is a mycoparasite of several species of fungi (Gupta et al. 1993). This fungus also has the potential to infect insects (Rombach et al. 1986) and the eggs and cysts of nematodes (Carneiro 1992). P. lilacinus also can be used for bioremediation purpose together with some other filamentous fungi, such as Rhizopus, Penicillium, Aspergillus, white rot fungi, Mucor, and Trichoderma (Zafar et al. 2007). Additionally, filamentous fungi are ubiquitous in nature and easily available in great quantities, which could be used as an economic and continuous supply of biosorbents (Wang et al. 2001). Studies of the biosorption mechanism, which is used by P. lilacinus for bioremediation, confirmed that the functional groups for the binding of metal ions are amide (−NH2), carboxylate (−COO), thiols (−SH), phosphate (PO43−), and hydroxide (−OH) (Wang and Chen 2009; Bozkurt et al. 2010; Xu et al. 2012). The stability of the adsorption process depended generally on the kind, amount, affinity, and distribution of those groups (Celekli and Bozkurt 2011). The biosorption mechanism of heavy metals by filamentous fungi can be used as a potential strategy for the remediation of Cd-contamination places. On the other hand, the use of fungal biomass in field-scale remediation still needs more research; this means that more fungal remediation agents need to be studied. It is extremely difficult to find organism growing in an environment contaminated with Cd because of the extreme toxicity of the metal, but microbes that

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s urvived on Cd pollution could have developed a Cd-resistant mechanism to tolerate this metal (Abou-Shanab et al. 2007). Since 2007, P. lilacinus has been developed into commercial products and used to control nematodes for years (Zou et al. 2007). Additionally, it has been studied in environment treatment as biphenyl-oxidizing organisms that can oxidize chlorinated biphenyl derivatives (Sietmann et al. 2006). A high Cd-resistant fungus was isolated from Zhuzhou Smelter Group and identified as M1 P. lilacinus by Zeng et al. (2010). During the growth in 100 mg L−1 Cd medium, the fungus received less toxicity and can adsorb this metal. Many mycorrhizal fungi have been reported possessing Cd-resistant ability (Blaudez et al. 2000). Some fungi such as, Aspergillus, Penicillium, Alternaria, Geotrichum, Fusarium, Rhizopus, Monilia, and Trichoderma have been reported to find resistance in Cd from 0.2 to 5 mg mL−1 (Zafar et al. 2007), so M1 showed higher Cd resistance (Baldrian and Gabriel, 2002; Tanous et al. 2006), and also it was found to be well resistant to some other metals such as Zn, Mn, Cu, Pb, and Co (Zeng et al. 2010). In another research P. lilacinus has been identified as XLA, and it was isolated from soil contaminated with Cd by Xia et al. (2015), and the minimum inhibitory concentrations (MICs) of Cd2+, Co2+, Cu2+, Zn2+, Cr3+, and Cr6+ in minimum mineral (MM) medium agar plates have been determined, and they were 29,786, 2945, 9425, 5080, 1785, and 204 mg L−1 for XLA.

1.5 Conclusions and Future Intensification of agriculture and manufacturing industry has resulted in increased release of a wide range of xenobiotic compounds to the environment. Bioremediation is a branch of biotechnology that is responsible for the use of biological agents, mainly microorganisms such as yeast, fungi, or bacteria to clean up contaminated soil and water (Strong and Burgess 2008), and its activity relies on promoting the growth of specific microflora that are native, or not, to the contaminated sites, and they are able to perform detoxification activities. In bioremediation processes, microorganisms use some contaminants as nutrient or energy sources (Hess et al. 1997; Agarwal 1998; Tang et al. 2007; Kumar et al. 2011). The biodegradation capacity of the different groups of fungi is essential to compensate for the depletion of microbial communities due to soil contamination, and, hence, it is a key aspect for the ecosystem recovery. Even more, the bioremediation potential of different groups of fungi from different ecosystems appears to be interconnected, creating communities that favor the survival of its members and enhancing the detoxification activities of the different ecosystems. The first study that reports the ability of the fungi to degrade anthropogenic compounds was realized by Wunch et al. in 1999. They reported the degradation of a polycyclic aromatic hydrocarbon (benzo[α] pyrene) by Marasmiellus troyanus in a liquid culture. Since this report, to date different authors and research groups have been given the task of finding more evidence to solve this problem (Anastasi et al. 2013; Rhodes 2014; Singh et al. 2015).


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This chapter showed that three genera of fungi (Trichoderma, Beauveria, and Paecilomyces) play a direct and important role in the degradation of complex compounds through a metabolic and enzymatic degradation and demonstrated the importance of developing multidisciplinary approaches to solve problems related to anthropogenic pollution and is now clearly appreciated by the scientific community. Nowadays, further efforts are needed to better understand how the agricultural soils work as a whole, and a better knowledge of the complexity of this heterogeneous environment, and the interactions between the different microorganisms, will make it possible to develop more effective bioremediation strategies.

References Abbas SAU, Khan MJ, Tariqjan M, Khan NU, Arif M, Parveen S (2011) The effect of using waste water on tomato. Pak J Bot 43:1 Abou-Shanab RAI, Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367 Adams P, De-Leij FAAM, Lynch JM (2007) Trichoderma harzianum Rifai 1295–22 mediates growth promotion of crack willow (Salix fragilis) saplings in both clean and metal-contaminated soil. Microb Ecol 54:306–313 Agarwal SK (1998) Environmental biotechnology. APH Publishing Corporation, New Delhi, pp 267–289 Anastasi A, Tigini V, Varese GC (2013) Fungi as bioremediators. In: The bioremediation potential of different Ecophysiological groups of fungi. Springer, Berlin, pp 29–49 Aravinna P, Priyantha N, Pitawala A, Yatigammana SK (2017) Use pattern of pesticides and their predicted mobility into shallow groundwater and surface water bodies of paddy lands in Mahaweli river basin in Sri Lanka. J Environ Sci Health B 52:37–47 Archana A, Jaitlty AK (2015) Mycoremediation: utilization of fungi for reclamation of heavy metals as their optimum remediation conditions. Biolife 3(1):77–106 Arias-Estévez M, López-Periago E, Martínez-Carballo E, Simal-Gándara J, Mejuto JC, García- Río L (2008) The mobility and degradation of pesticides in soils and the pollution of groundwater resources. Agric Ecosyst Environ 123(4):247–260 Baldrian P, Gabriel J (2002) Intraspecific variability in growth response to cadmium of the wood- rotting fungus Piptoporus betulinus. Mycologia 94:428–436 Banik S, Das KC, Islam MS, Salimullah M (2014) Recent advancements and challenges in microbial bioremediation of heavy metals contamination. JSM Biotechnol Bioeng 2(1):1035 Bayoumi HEAF, Patkó I (2010) Relationship between environmental impacts and modern agriculture. Environmental Protection Engineering Institute, Óbuda University, e-Bulletin 1,1 Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117 Bourne M, Nicotra AB, Colloff MJ, Cunningham SA (2008) Effect of soil biota on growth and allocation by Eucalyptus microcarpa. Plant Soil 305:145 Bozkurt H, Celekli A, Yavuzatmaca M (2010) An eco-friendly process: predictive modelling of copper adsorption from aqueous solution on Spirulina platensis. J Hazard Mater 173:123–129 Carneiro RMDG (1992) Princípios e tendências de controle biológico de nematóides com fungos nematófagos. Pesq Agrop Brasileira 27:113–121 Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharp-ley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568

12


Celekli A, Bozkurt H (2011) Biosorption of cadmium and nickel ions using Spirulina platensis: kinetic and equilibrium studies. Desalination 275:141–147 Dixit R, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212 Domsch KH, Gams W (1980) Compendium of soil fungi. Academic Press, New York, pp 529–532 Doelman P, Jansen E, Michels M, van Til M (1994) Effects of heavy metals in soil on microbial diversity and activity as shown by the sensitivity-resistance index, an ecologically relevant parameter. Bioi Fertil Soils 17:177–184 Dugal S, Gangawane M (2012) Metal tolerance and potential of Penicillium species for use in mycoremediation. J Chem Pharm Res 4:2362–2366 Edmondson WT (1995) Eutrophication. Encyclopedia of environmental biology, vol 1. Academic Press, New York, pp 697–703 EEA (European Environment Agency) (2003) Europe’s environment: the third assessment. State of Environment report No 1/2003. Copenhagen EPA, Environmental protection Agency (2016) Climate change indicators in the United States: global greenhouse gas emissions www.epa.gov/climate-indicators – Updated August 2016 FAO (2014) Soil degradation. Accessed on (19/11/2014) Available: www.fao.org/soils-portal/ soil-degradation-restoration/en FAO (Food and Agriculture Organization of the United Nations) (2009) How to feed the world in 2050. FAO, Rome. http://www.fao.org/fileadmin/templates/wsfs/docs/expert_paper/How_to_ Feed_the_World_in_2050.pdf Fomina M, Charnock J, Bowen AD, Gadd GM (2007) X-ray absorption spectroscopy (XAS) of toxic metal mineral transformations by fungi. Environ Microbiol 9:308–321 Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70(2):153–226 Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535–539 Goblenz A, Wolf K, Bauda P (1994) The role of glutathione biosynthesis in heavy metal resistance in the fission yeast Schizosaccharomyces pombe. FEMS Microbiol Rev 14:303–308 Gola D, Dey P, Bhattacharya A, Mishra A, Malik A, Namburath M, Ahammad SZ (2016) Multiple heavy metal removal using an entomopathogenic fungi Beauveria bassiana. Bioresour Technol 218:388–396 Gupta SC, Leathers TD, Wicklow DT (1993) Hydrolytic enzymes secreted by Paecilomyces lilacinus cultured on sclerotia of Aspergillus flavus. Appl Microbiol Biotechnol 39:99–103 Gupta RP, Kalia A, Kapoor S (2007) Bioinoculants: a step towards sustainable agriculture. New India Publishing Agency, New Delhi, p 306 Hamilton PA, Shedlock RJ (1992) Are fertilizers and pesticides in the ground water?; U.S. Geological Survey: Reston, VA; Circular 1080 van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310 Hess A, Zarda B, Hahn D, Hanner A, Stax D (1997) In situ analysis of denitrifying toluene and m-xylene degrading bacteria in a diesel fuel contaminated laboratory aquifer column. Appl Environ Microbiol 63:2136–2141 Howarth RW (2006) Atmospheric deposition and nitrogen pollution in coastal marine ecosystems. In: Visgilio GR, Whitelaw DM (eds) Acid in the environment: lessons learned and future prospects. Springer, NY, pp 97–116 ILO (International Labour Organization) (2011) Safety and health in agriculture, isbn: 978-92-2- 124971-9. Retrieved Dec 2016 Jantschi L, Suciu I, Cosma C, Todica M, Bolboaca SD (2008) Analysis of soil heavy metal pollution and pattern in central Transylvania. Int J Mol Sci 9:434


13

Joseph E, Cario S, Simon A, Wörle M, Mazzeo R, Junier P, Job D (2012) Protection of metal artifacts with the formation of metal–oxalates complexes by Beauveria bassiana. Front Microbiol 2:270 Kameo S, Iwahashi H, Kojima Y, Satoh H (2000) Induction of metallothioneins in the heavy metal resistant fungus Beauveria bassiana exposed to copper or cadmium. Analysis 28(5): 382–385 Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28(1):61–69 Kojima Y, Berger C, Vallee BL, Kägi JHR (1976) Amino-acid sequence of equine renal metallothionein-1B. Proc Nat Acad Sci USA 73:3413–3417 Kumar R, Bishnoi NR, Garima K (2008) Biosorption of chromium (VI) from aqueous solution and electroplating wastewater using fungal biomass. Chem Eng J 135:202–208 Kumar A, Bisht BS, Joshi VD, Dhewa T (2011) Review on bioremediation of polluted environment: a management tool. Int J Environ Sci 1(6):1079–1093 Li F, Tan TC (1994) Monitoring BOD in the presence of heavy metal ions using poly (4-vinylpyr-idine) coated microbial sensor. Biosens Bioelectron 9:445–455 Loebenstein G, Thottappilly G (2007) Agricultural research management. Springer, Dordrecht MA (Millennium Ecosystem Assessment) (2005) Ecosystem services and human well-being: wetlands and water synthesis. World Resources Institute, Washington D.C. 68 pp. Web site: http:// www.millenniumassessment.org/en/index.aspx) Mann H (1990) Removal and recovery of heavy metals by biosorption. In: Volesky B (ed) Biosorption of heavy metals. CRC Press, Raton, pp 93–137 Mastouri F, Bjorkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221 Maurya NS, Mittal AK, Peter C, Elmar R (2006) Biosorption of dyes using dead macro fungi: effect of dye structure, ionic strength and pH. Bioresour Technol 97:512–521 Mohsenzadeh F, Shahrokhi F (2014) Biological removing of cadmium from contaminated media by fungal biomass of Trichoderma species. J Environ Health Sci Eng 12:102–109 Montanarella L, Vargas R (2012) Global governance of soil resources as a necessary condition for sustainable development. Curr Opin Environ Sustain 4:559–564 Muraleedharan TR, Iyengar L, Venkobachar C (1991) Biosorption: an attractive alternative for metal removal and recovery. Curr Sci 61:379–385 Nordberg GF, Nordberg M, Piscator M, Vesterberg O (1972) Separation of two forms of rabbit metallothionein by isoelectric focusing. Biochem J 126(3):491–498 OECD (2012) Water quality and agriculture – meeting the policy challenge. OECD studies on water. OECD Publishing, Paris Olesen JE (2006) Climate change as a driver for European agriculture. SCAR – Foresight in the field of agricultural research in Europe. https://ec.europa.eu/research/agriculture/scar/pdf/ scar_foresight_climate_change_en.pdf Önder M, Kahraman A (2010) Global climate changes and their effects on field crops. In: 10th international multidisciplinary geoconference SGEM, Conference Proceedings, 20–26 June 2010, Bulgaria. 2010, vol. II, pp. 589–592 Önder M, Ceyhan E, Kahraman A (2011) Effects of agricultural practices on environmental. In: International Conference on Biology, Environment and Chemistry (ICBEC), vol. 24 © IACSIT Press, Singapore Pantelica A, Cercasov V, Steinnes E, Bode P, Wolterbeek B (2008) Investigation by INAA, XRF, ICPMSnand PIXE of Air Pollution Levels at Galati (Siderurgical Site), In: Book of abstracts, 4th Nat. Conf. of Applied Physics (NCAP4), Galati, Romania, September 2008 (A. Ene – Ed.) Galati University Press, Galati, Romania Purchase D, Scholes LNL, Revitt DM, Shutes RBE (2009) Effects of temperature on metal tolerance and the accumulation of Zn and Pb by metal-tolerant fungi isolated from urban runoff treatment wetlands. J Appl Microbiol 106:1163–1174

14


Rhodes CJ (2014) Mycoremediation (bioremediation with fungi)-growing mushrooms to clean the earth. Chem Speciat Bioavailab 26(3):196–198 Rial-Otero R, Cancho-Grande B, Arias-Estévez M, López-Periago E, Simal-Gándara J (2003) Procedure for the measurement of soil inputs of plant-protection agents washed off through vineyard canopy by rainfalls. J Agric Food Chem 51(17):5041–5046 Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290 Rombach MC, Aguda RM, Shepard BM, Roberts DW (1986) Infection of rice brown plant hopper, Nilaparvata lugens (Homoptera: Delphacidae), by field application of entomopathogenic hyphomycetes (Deuteromycotina). Environ Entomol 15:1070–1073 Sahu A, Manna MC, Mandal A, Subba Rao A, Thakur J (2012) Exploring bioaccumulation efficacy of Trichoderma viride: an alternative bioremediation of cadmium and lead. Natl Acad Sci Lett 35(4):299–302 Samson RA (1974) Paecilomyces and some allied hyphomycetes. In: Studies in mycology, vol 6. Centraal bureau voor Schimmelcultures, Baarn Shilev S, Babrikov T (2005) Heavy metal accumulation in Solanaceae-plants grown at contaminated area. In: Gruev B, Nikolova M Donev A (eds) Proceedings of the Balkan scientific conference of biology in Plovdiv (Bulgaria) from 19th till 21st of May 2005. pp. 452–460 Sietmann R, Gesell M, Hammer E, Schauer F (2006) Oxidative ring cleavage of low chlorinated biphenyl derivatives by fungi leads to the formation of chlorinated lactone derivatives. Chemosphere 64:672–685 Singh M, Srivastavar PK, Vermar PC, Kharwar RN, Singhi N, Tripathi RD (2015) Soil fungi Mycoremediation of arsenic pollution in agriculture soils. J Appl Microbiol 119:1278–1290 Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409(12):2430–2442 Strong PJ, Burgess JE (2008) Treatment methods for wine-related ad distillery wastewaters: a review. Biorem J 12:7087 Tang CY, Criddle QS, CS F, Leckie JO (2007) Effect of flux (transmembrane pressure) and membranes properties on fouling and rejection of reverse osmosis and nanofiltration membranes treating perfluorooctane sulfonate containing waste water. J Environ Sci Technol 41:2008–2014 Tanous C, Chambellon E, Bars DL, Delespaul G, Yvon M (2006) Glutamate dehydrogenase activity can be transmitted naturally to Lactococcus lactis strains to stimulate amino acid conversion to aroma compounds. Appl Environ Microbiol 72:1402–1409 Tixier C, Sancelme M, Bonnemoy F, Cuer A, Veschambre H (2001) Degradation products of a phenylurea herbicide, diuron: synthesis, ecotoxicity, and biotransformation. Environ Toxicol Chem 20(7):1381–1389 Tomko J, Backor M, Stofko M (2006) Biosorption of heavy metals by dry fungi biomass. Acta Metall Slovaca 12:447–451 Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD (2013) Trichoderma: a potential bioremediator for environmental clean-up. Clean Techn Environ Policy 15:541–550. https://doi.org/10.1007/s10098-012-0553-7 Vankar PS, Bajpai D (2008) Phyto-remediation of Chrome-VI of tannery effluent by Trichoderma species. Desalination 222:255–262 Vinod PN, Chandramouli PN, Koch M (2015) Estimation of nitrate leaching in groundwater in an agriculturally used area in the state Karnataka, India, using existing model and GIS. Aquat Procedia 4:1047–1053 Vollenweider RA (1968) Scientific fundamentals of lake and stream eutrophication, with particular reference to phosphorus and nitrogen as eutrophication factors. (Technical Report DAS/ DSI/68.27). OECD, Paris Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Nat Acad Sci USA 111:5266–5270


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Walls M (2006) Agriculture and environment. The Standing Committee on Agricultural Research (SCAR) Foresight Group. 22 strani. http://ec.europa.eu/research/agriculture/scar/pdf/scar_ foresight_environment_en.pdf Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226 Wang J, Zhan X, Ding D, Zhou D (2001) Bioadsorption of lead(II) from aqueous solution by fungal biomass of Aspergillus niger. J Biotechnol 87:273–277 Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633 Wong SC, Li XD, Zhang GQ, Min YS (2002) Heavy metals in agricultural soils of the Pearl River Delta, South China. Environ Pollut 119:33–44 Wood JM, Wang HK (1983) Microbial resistance to heavy metals. Environ Sci Technol 17:582–590 WRI (World Resources Institute) 2015. Climate Analysis Indicators Tool (CAIT) 2.0: WRI’s climate data explorer. Accessed Dec 2015. http://cait.wri.org Wunch KG, Alworth WL, Bennett JW (1999) Mineralization of benzo[a]pyrene by Marasmiellus troyanus, a mushroom isolated from a toxic waste site. Microbiol Res 154:75–79 Xia L, Xu X, Zhu W, Huang Q, Chen W (2015) A comparative study on the biosorption of Cd2+ onto Paecilomyces lilacinus XLA and Mucoromycote sp. XLC. Int J Mol Sci 16:15670–15687 Xu X, Xia L, Huang Q, JD G, Chen W (2012) Biosorption of cadmium by a metal-resistant filamentous fungus isolated from chicken manure compost. Environ Technol 33:1661–1670 Yazdani M, Yap CK, Abdullah F, Tan SG (2009) Trichoderma atroviride as a bioremediator of Cu pollution: an in vitro study. Toxicol Environ Chem 91(7):1305–1314 Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresour Technol 98:2557–2561 Zeng X, Tang J, Yin H, Liu X, Jiang P, Liu H (2010) Isolation, identification and cadmium adsorption of a high cadmium-resistant Paecilomyces lilacinus. Afr J Biotechnol 9(39):6525–6533 Zhao KL, Liu XM, Zhang WW, JM X, Wang F (2011) Spatial dependence and bioavailability of metal fractions in paddy fields on metal concentrations in rice grain at a regional scale. J Soil Sed 11:1165–1177 Zhu YG, Meharg AA (2015) Protecting global soil resource for ecosystem services. Ecosyst Health Sustain 1(3):11 Zou CS, Mo MH, YQ G, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379

Chapter 2

Marine-Derived Fungi: Prospective Candidates for Bioremediation Anjana K. Vala and Bharti P. Dave

2.1 Introduction Over the years, industrial processes, agricultural practices and many other anthropogenic activities release a lot of hazardous chemicals into the environment. It is essential to reduce their concentration to meet the ever-increasing legislative standards. While physicochemical methods for pollutant removal are less effective, costly, and generate sludge in most of the cases, many of them, though effective, are not feasible for large-scale applications (Akcil et al. 2015; Deshmukh et al. 2016). Bioremediation offers a promising solution to this. Among microorganisms, fungi exhibit unique traits like ability to grow in diverse habitats, greater growth ability, reach due to mycelial branching, capability to produce multitude of enzymes and accumulate metals etc. hence they are promising candidates for bioremediation (Vala et al. 2004; Deshmukh et al. 2016). Various mechanisms employed by fungi for remediating toxic, recalcitrant compounds are depicted in Fig. 2.1. Assessment of marine habitats for marine-derived fungi (as bioremediation agents) is all the more essential, as it may lead to screening fungal strains with better potentials because of their ability to grow under extreme conditions like high salinity and pH that may aid in industrial wastewater treatment. This chapter focuses on marine-derived fungi as promising candidates for bioremediation with reference to the major environmental pollutants: (a) synthetic dyes and textile effluents and (b) heavy metal and metalloids.

A.K. Vala (*) • B.P. Dave Department of Life Sciences, Maharaja Krishnakumarsinhji Bhavnagar University, Bhavnagar, India e-mail: [email protected]; [email protected] © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_2

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A.K. Vala and B.P. Dave

Fig. 2.1 Schematic representation of mechanisms employed by fungi for remediation of recalcitrant toxic compounds (Adopted from Deshmukh et al. 2016, Indian J Microbiol 56(3): 247–264)

2.2 M ycoremediation of Synthetic Dyes and Textile Dye Effluents Among the dyes belonging to classes of compounds with azo, anthraquinone, triphenylmethane, and heterocyclic polymeric structures, the largest and most versatile class of dyes, the azo dyes, constitute more than half of the yearly manufactured synthetic dyes (Diwaniyan et al. 2010; Bonugli-Santos et al. 2015). Annually over 800kt of dyes are produced worldwide. It has been forecast that world’s market for dyes and pigments would reach 26.53 billion USD by the year 2017 (Anonymous 2012; Rodriguez et al. 2015). Ten to 15% of unused dyes after the dyeing and subsequent washing processes enter the wastewater. Upon release, such dye-containing effluent not only imparts aesthetically unacceptable coloration to the water body but also results in reduced transmittance of sunlight leading to impaired primary production and interferes dilution of gasses and affects human health (Baughman and Weber 1994; Ciullini et al. 2008; Rodriguez et al. 2015). Health risks of dye exposure range from nausea, hemorrhage, and ulceration of skin and mucous membranes to severe damage to the kidney, reproductive system, liver, brain, and central nervous system. Many synthetic dyes are toxic, mutagenic, and carcinogenic. Most of the conventionally used physico-chemical methods for dye decolorization suffer from one or the other limitation. They are either expensive, chemical intensive, or have limited applicability. These limitations call for a more efficient and

2 Marine-Derived Fungi: Prospective Candidates for Bioremediation

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cost-effective treatment alternative for dye wastewaters. Bioremediation can be harnessed for such purpose as a promising alternative. Fungal cells can bring about dye decolorization by oxidative reactions generating nontoxic derivatives (Ciullini et al. 2008), ligninolytic enzymes produced by filamentous fungi have great relevance in bioremediation (Arun et al. 2008). Fungi do produce enzymes with low specificity, e.g., ligninolytic enzymes, which can bring about degradation of various xenobiotic compounds, including textile dyes. Lignin-degrading enzymes (LDEs) are categorized as: (a) the heme-containing peroxidases and (b) the copper-containing laccases. Lignin-degrading enzymes, being non-specific, efficiently attack aromatic compounds with little similarity to lignin (Field et al. 1992). This is the rationale behind the role of LDEs in textile dye degradation. Marine-derived fungi, being better adapted to perform under extreme conditions, are many a times more efficient than their terrestrial counterparts in treatment of colored effluents (Raghukumar et al. 2004; Bonugli-Santos et al. 2015). In India, significant work on degradation of various textile dyes has been carried out especially at the National Institute of Oceanography (a CSIR Laboratory), Goa. Raghukumar et al. (1999) reported a basidiomycetous fungus Flavodon flavus (Klotzsch) Ryvarden (strain 312), isolated from decaying sea grass from a coral lagoon off the West Coast of India, for the first time to produce all three major classes of extracellular lignin-modifying enzymes (LMEs): manganese-dependent peroxidase (MNP), lignin peroxidase (LIP), and laccase. When examined for decolorization of synthetic dyes, F. flavus (strain 312) was found to potentially degrade dyes Poly-B, Poly-R, Congo red, Remazol brilliant blue R, and Azure B, however, decolorization of brilliant green was observed to be relatively less efficient. Better degradation of all the dyes was seen in LN + IO medium, suggesting the potential of F. flavus for bioremediation of aromatic pollutants under marine conditions. The authors confirmed that decolorization was not due to pH changes as throughout the experiment, pH of the culture medium remained unchanged. Raghukumar (2000) reported that manganese-dependent peroxidase was always produced in cultures of F. flavus 312 containing dyes. In some cases, existence of a direct correlation between % decolorization and MNP activity suggested its involvement in the decolorization process. Ability to degrade paper mill effluent and synthetic dyes makes the fungus to be a potential candidate for bioremediation of colored industrial effluents. D’Souza et al. (2006) reported efficient decolorization of effluents from paper and pulp mills, textile and dye-making industries, and alcohol distilleries by a marine basidiomycetous fungal isolate NIOCC # 2a producing laccase as the main lignin-degrading enzyme. Decolorization of several synthetic dyes was also observed. The authors studied decolorization of effluents and dyes in the culture medium as well as using fungus free-culture supernatant and exopolymeric substances (EPS) produced by the fungus. Enhanced production of laccase was found during treatment indicating the synthetic dyes and effluent as laccase inducers, which could be an added advantage during bioremediation of industrial effluents. D’Souza-Ticlo et al. (2009a) identified the laccase hyperproducing marine- derived basidiomycetous fungus NIOCC #2a (MTCC 5159) at molecular level as

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Cerrena unicolor and characterized the laccase from the fungus. The fungus, having the ability to decolorize several dyes, produced three distinct laccases, viz., Lac I, Lac II and Lac III, each of them were resolved into four isozymes. Remarkable observations like heavy metal tolerance of Lac IId, its thermostability, and high optimum temperature for activity, along with high laccase titer in presence of seawater, led the authors to suggest marine-derived C. unicolor MTCC 5159 as a candidate for bioremediation of effluents containing dyes, lignin-related compounds, chlorides, and sulfates. Further, D’Souza-Ticlo et al. (2009b), employing response surface methodology (RSM), examined effects and interactions of medium components on laccase production by the marine-derived basidiomycete C. unicolor MTCC 5159. Biomass and laccase production were supported by a combination of low nitrogen and high carbon concentration. A single addition of CuSO4 acted as an inducer for laccase. Addition of Tween 80 positively affected biomass and in turn laccase activity. Decolorization and detoxification of two raw textile mill effluents with varying characteristics were carried out by four marine-derived fungi (Verma et al. 2010). One effluent (TEA) with pH 8.9 consisted of an azo dye, while the other (TEB) had a mixture of eight reactive dyes and a pH of 2.5. Among the four marine-derived fungi used, two were ascomycetes exhibiting rapid growth and high biomass yield, and two were basidiomycetes with comparatively high titer of laccase. Decolorization of TEA by 30–60% and TEB by 33–80% was achieved within 6 days by each of the fungi when used at 20–90% concentrations and salinity of 15‰. Two to three fold reduction in toxicity (LC50 values against Artemia larvae) and 70–80% reduction in COD and total phenolics were observed. Mass spectrometric scan analysis of treated effluent showed that most of the components were degraded. Explaining the bioremediation process, the authors suggested adsorption using ascomycetes as a mechanism for instant color removal that was followed by treatment with laccase from basidiomycetes that removed the adsorbed color from the fungal biomass. The authors envisaged high industrial scale applicability of the study. In general, time is the issue involved with dye decolorization and degradation. Verma et al. (2012) developed a two-step technique for bioremediation of Reactive Blue 4 (RB4), an anthraquinone dye, using a marine-derived fungus. Sixtyone percent color removal and twofold decrease in chemical oxygen demand by 12 h was achieved during the first step, where treatment of the dye at a concentration of 1000 mg l−1 was carried out with partially purified laccase of the test fungus. Characterization of the metabolites formed during enzymatic degradation revealed low-molecular-weight phenolic compounds as the final products. 2-Formylbenzoic acid, 1,2,4,5-tetrahydroxy-3-benzoic acid, 2,3,4-trihydroxybenzenesulfonic acid and 1,2,3,4-pentahydroxy benzene were identified as probable degradation products of RB4. In the second step, sorption of the laccase-treated dye was carried out on powdered fungal biomass, and reduction in color up to 93% within 10 min could be achieved. Two-step treatment of the dye also resulted in more than twofold decrease in toxicity. The authors suggested enzymatic oxidation followed by sorption of the degraded products on the fungal biomass as a means for rapid decolorization and detoxification of textile dyes.


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Sarvanakumar and Kathiresan (2014) reported bioremoval of malachite green by a marine Trichoderma Hypocrea lixii. Employing response surface methodology, individual and interaction effects of physical and chemical factors on dye degradation, and laccase production were studied. Dye degradation was confirmed by analytical techniques like FTIR, UV-Vis spectra, and scanning electron microscopy. Toxicity testing was carried out on Artemia salina and observed that while treatment with undegraded dye resulted in 100% mortality, it reduced to 2–5%, in case of treatment with the degraded dye solution. Synthetic dye decolorization ability of marine-derived fungi (isolated from seawater, marine sediments, and living sea grasses) from Manila Bay and Calatagan Bay, Philippines, was tested by Torres et al. (2011). Twentysix fungal isolates were screened, out of which 21 showed partial to full decolorization of 0.01% crystal violet. Test isolates Phialophora sp. (MF 6), Penicillium sp. (MF 49), and Cladosporium sp. (EMF 14) could decolorize 0.01% Congo red completely and 0.01% crystal violet up to 91%. The authors inferred enzyme production and/or biosorption as possible mechanism for dye decolorization. Remarkable contribution on bioremediation of textile dyes using marine-derived fungi has been from Dr. Lara Durães Sette’s group from Brazil. Bonugli-Santos et al. (2012) examined three basidiomycetes recovered from marine sponges, viz., Tinctoporellus sp. CBMAI 1061, Marasmiellus sp. CBMAI 1062 and Peniophora sp. CBMAI 1063, for their biotechnological potential for decolorization of dyes and treatment of colored effluents. All the three fungi produced ligninolytic enzymes under saline and nonsaline conditions. Up to 100% decolorization of dye Remazol brilliant blue R (RBBR) was achieved by the three fungi. Among the three, Tinctoporellus sp. CBMAI 1061 was observed to be the most efficient. The authors consider the salt-tolerant fungi and their salt-tolerant enzymes as targets for biotechnological applications, especially for bioremediation of environmental pollutants under saline and nonsaline conditions. The authors claim the work as the first report on the production of ligninolytic enzymes by sponge-derived fungi. As sponges are exposed to pollutants from water and accumulate them, it could be hypothesized that sponge-associated microbiota produce hydrolytic enzymes for converting the organic matter into nutrients (Wang 2006; Bonugli-Santos et al. 2012). Efficient degradation of Remazol brilliant blue R, a potentially toxic synthetic dye, using marine-derived fungus Tinctoporellus sp. CBMAI 1061, was revealed by Bonugli-Santos et al. (2012). However, the degradation products were not identified. Further, Rodriguez et al. (2015) investigated the RBBR transformation products by Tinctoporellus sp. CBMAI 1061 and kinetics of the degradation product. They observed formation of new anthraquinones 2–5 using NMR and MS analyses. Three tremulene terpenes have also been isolated as metabolism products from the RBBR degradation medium. Two of them bear novel 2-hydroxy- or 2-methoxy-3,4dihydro-2H-pyrrole N-oxide moieties. Bonugli-Santos et al. (2016) employed integrated statistical design to obtain enhanced decolorization of textile dye Reactive Black 5 (RB5) by a marine-derived basidiomycete Peniophora sp. CBMAI 1063. Effective decolorization (94%) of

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RB5 dye was achieved in saline conditions concurrently; 57% of total organic carbon (TOC) was removed in 7 days. Evaluation of mutagenicity revealed production of non-mutagenic metabolites. Studies related to contribution of ligninolytic enzymes in the RB5 dye decolorization revealed production of manganese peroxidase (MnP) and laccase (Lac), while lignin peroxidase (LiP) was not detected. A higher manganese peroxidase (MnP) gene expression and significant enzymatic activity in the early stage of dye decolorization along with the formation of p-Base and triaminohydroxynaphthalene disulfonic acid (TAHNDS) compounds was observed. The authors claim Peniophora sp. CBMAI 1063 as a target genetic resource for degradation of environmental pollutants in saline conditions. For removal of a wide range of pollutants, compared to conventional techniques, biosorption is an alternative technology, especially in developing countries (Chaukura et al. 2016). Biosorbents prepared from marine-derived fungi have also been examined for such application. Wang et al. (2015) prepared mycelial pellets using a marine-derived Penicillium janthinellum sp. strain (P1) and applied as biosorbents for removal of nine different dyes. Effective dye removal from solutions, strong salt tolerance, and high reusability were remarkable properties of the pellets. The adsorption isotherm studies suggested that biosorption process agreed with the Langmuir isotherm model, maximum biosorption capacity (for Congo red) was 344.83 mg g(dry)−1, and the biosorption process followed a pseudo-second-order kinetic model. Immobilization was employed by many workers for dye removal. Huiying et al. (2014) constructed and optimized a two-species whole-cell immobilization system using marine-derived fungus Pestalotiopsis sp. J63 spores and Penicillium janthinellum P1 pre-grown mycelia pellets. The use of immobilized pellets for treating paper mill effluent and decolorizing dye Azure B resulted in successful and rapid biodegradation of numerous insoluble fine fibers, and the decolorization ability of the immobilized pellets was found to be more superior than that of P1 mycelial pellets. Lu et al. (2016) prepared self-immobilization mycelial pellets using a marine- derived fungus Aspergillus niger. The pellets were used as biosorbents to investigate decolorization of an azo dye Congo red. Fitting of the biosorption process with models of pseudo-second-order kinetic and Langmuir isotherm with maximum adsorption ability of 263.2 mg g− 1 mycelium was revealed during the adsorption studies. Based on UV-Vis spectral analysis, the authors suggested decolorization to be accompanied by biodegradation of the dye. While studying the mechanistic aspects, the authors further suggest active zone on the surface of the pellet to be the main factor for efficient biosorption capability of the pellets. Flavodon flavus (Klotzsch) Ryvarden isolated from sea grass at Mjimwema in the Western Indian Ocean off the Coast of Dar es Salaam, Tanzania, was also investigated for lignocellulosic enzymes and their role in decolorization of raw textile wastewater and synthetic dyes (Mtui and Nakamura 2008). In low-carbon medium, the culture exhibited effective (92–100%) decolorization of raw textile wastewater


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and synthetic dyes like Remazol brilliant blue R (RBBR), brilliant green, Congo red, Reactive Black, and Reactive Yellow. SDS-PAGE analysis revealed bands of enzymes from F. flavus at relative molecular weights between 45 and 70 kDa. The lignin peroxidase (LiP) purified by ion exchange chromatography had a relative molecular weight of 46 kDa and isoelectric point of 3.8. Attention on decolorization of synthetic dyes has been given at National Research Centre, Egypt. Effect of various media and supplements on laccase activity of marine-derived fungus Alternaria alternata, and its application in synthetic dye decolorization, was examined by El Aty and Mostafa (2013). They concluded that A. alternata could produce appreciable amount of laccase using wheat bran. They observed 75.47% decolorization of synthetic Reactive Black dyes and about 69.35% decolorization of crystal violet, at 0.01% concentration, after 30 days. El Aty et al. (2016) optimized conditions for laccase production by a marine-derived fungus Alternaria tenuissima KM651985 using Plackett-Burman design and central composite design. They observed A. tenuissima KM651985 to efficiently decolorize two structurally different (azo and triphenylmethane) synthetic dyes, Congo red and crystal violet, while decolorization of crystal violet was by the crude enzyme was less efficient. Further, El Aty et al. (2017) immobilized Alternaria tenuissima KM651985 laccase covalently in Ca2+(AlgChG) beads. Properties of the enzyme improved due to immobilization. Due to remarkable activity of immobilized laccase in decolorization of two reactive dyes (Congo red and crystal violet) and in reduction in their toxicity, the authors recommend application of A. tenuissima KM651985 laccase at industrial scale. Yanto et al. (2014) studied decolorization and degradation of textile dyes Reactive Green 19 (RG 19), Reactive Red 4 (RR 4), and Reactive Orange 64 (RO64) in a liquid medium and bioreactor using immobilized mycelia of Pestalotiopsis sp. NG007. A high decolorization (20–98%) over 3 days in a wide range of pHs (3–12) and salinities (0–10% w/v) was noted. The mechanistic aspect of decolorization was attributed to adsorption (6–53%) and degradation due to enzymatic activities (34– 41%). Decolorization capability of the test strain for the three dyes was reported as RG19 > RO64 > RR4. The authors recommend the bioreactor system used in their study for its potential use in treatment of textile dye industrial effluents with varying pHs and salinities. Common effluent treatment plant (CETP) is set up in some cases where a group of diverse industries release their effluent which is treated before its discharge. A CEPT effluent receiving effluents from chemicals, dyes, and pharmaceutical industrial units was treated with algae (Ulva sp.) associated Aspergillus niger (Joshi et al. 2012), which could decolorize diluted and undiluted effluent samples. In both cases over 88% color removal was achieved after 6 days (Joshi et al. 2012). Besides removing color, the fungus also exhibited metal removal ability as revealed by decrease in concentration of metals like (Fe, Hg, Pb, and Zn).

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Fig. 2.2 Various means of fungus-metal interaction (Adopted from Harms et al. 2011, Nat Rev Microbiol 9:177–192)

2.3 Mycoremediation of Heavy Metals and Metalloids Fungi encounter metals due to occurrence of metals in natural environment as well as due to anthropogenic activities. In the marine subsurface, heavy metal concentrations possibly vary substantially with depth due to variations in the depositional environment when the sediments were originally deposited on the seafloor as well as subsequent impositions of metal-laden fluids. Microbial community composition is shaped by composition and concentrations of heavy metals (Oliveira and Pampulha 2006; Ravikumar et al. 2007; Pachiadaki et al. 2016). Metals having biological role or otherwise, if present above a certain threshold concentrations in bioavailable forms, would exert toxicity in several ways (Gadd 1993, 2007). However, many fungi exhibit tolerance toward metals due to various mechanisms that help them survive and grow even in metal-contaminated sites (Gadd 2007). A population shift from unicellular bacteria and streptomycetes to fungi has also been observed in contaminated soils (Chander et al. 2001a, b; Khan and Scullion 2000; Gadd 2007). As shown in Fig. 2.2, mechanisms of metal tolerance (and detoxification) in fungi range from metal immobilization (adsorption to cell wall, extracellular binding by polysaccharides and metabolites, extracellular precipitation of secondary minerals and intracellular sequestration using metallothioneins and phytochelatins, vacuolar localization) to reduction of metal uptake and/or increased efflux (Gadd 1993, 2007; Harms et al. 2011). Mycoremediation of two priority pollutants as per the list of EPA, i.e., chromium and arsenic, using marine-derived fungi is discussed.


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2.3.1 Chromium Chromium is one of the heaviest and most hazardous metals (Kocberber and Donmez 2007; Samuel et al. 2015). In the “Priority Pollutants” list of EPA, chromium occupies position 119 (https://www.epa.gov/sites/production/files/2015-09/ documents/priority-pollutant-list-epa.pdf). Battery manufacturing, dye, electroplating, metal finishing, metallurgical, tannery, textile, and wood preservation industrial effluents contain chromium, especially Cr(VI) (Farooq et al. 2010; Kocberber and Donmez 2007; Samuel et al. 2015). Chromium occurs in various valency states ranging from Cr(II) to Cr(VI). Among these, hexavalent chromium Cr(VI) is the most hazardous. The maximum permissible limit of Cr(VI) in natural water is 0.05 mg l−1 (US EPA 1988). Manifestations of Cr(VI) exposure at lower concentrations include respiratory tract disorders, allergies, and eczema, while at higher concentrations, it is carcinogenic causing colon cancer, digestive tract cancer and lung cancer (Kaufman 1970; Katz and Salem 1993; Costa 2003; Park et al. 2005; Kotas and Stasicka 2000). The negatively charged ions of Cr(VI) form complexes that easily penetrate the cell membrane through sulfate ionic channel and undergo a reduction leading to formation of harmful reactive intermediates hence exerting toxic effects (Wang and Shen 1995; Samuel et al. 2015). Techniques widely used for Cr(VI) removal like chemical precipitation, electrochemical treatment, electrodialysis, evaporation, ion exchange, liquid extraction, membrane process, reverse osmosis, and sorption methods are not so efficient as they involve high cost, risk of secondary pollution, and are not environment friendly. Though efficient, the use of activated carbon as adsorbent is also very expensive. Hence, emphasis is given on bioremediation of Cr(VI)-contaminated sites (Farooq et al. 2010; Kocberber and Donmez 2007; Ramrakhiani et al. 2011; Lui et al. 2007; Regine and Volesky 2000; Samuel et al. 2015). Biological removal of Cr(VI) has been reported using several organisms (Gupta et al. 2001; Horitsu et al. 1987; Komori et al. 1989; Merrin et al. 1998; Smith and Gadd 2000; Srinath et al. 2002; Subbaiah et al. 2008; Tucker et al. 1998; Wang and Shen 1995). Among them, fungi could be the most efficient due to the following reasons: (i) Fast growing ability and simple nutrient requirement (ii) Adaptability to stress conditions (iii) Ability to detoxify heavy metals by mechanisms including adsorption, extracellular and intracellular precipitation, ion exchange, and valence transformation (iv) The presence of complex cell wall made up of chitin and the presence of proteins, glucan, and polymers with functional groups like carboxyl, phosphoryl, hydroxyl, amino, and imidazole on their surface (Ramrakhiani et al. 2011; Samuel et al. 2015) While metal removal studies using terrestrial fungi are advanced, comparatively less information exist on their counterparts from marine environment (Taboski et al.

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2005; Vala and Upadhyay 2008; Vala 2010). Fungi in marine habitats are important members of the inshore microbiota (Millward et al. 2001; Hyde et al. 1998; Newell and Barlocher 1993) and encounter metal ions and complexes in large harbors. Assessment of these microbiota for removal of metals is an interesting area of research (Vala et al. 2004; Vala 2010). Exploring the newer sources of fungi for metal tolerance and removal, Vala et al. (2004) examined two seaweed-associated fungi Aspergillus flavus and A. niger for their Cr(VI) tolerance. Both the strains showed remarkable hexavalent chromium tolerance, and Cr content (mgg−1 dry wt) was found to be 22.26 and 18.1 in A. flavus and A. niger, respectively. Increase in Cr content (mg g−1 dry wt) was observed with increase in supplied Cr(VI) concentrations. El-Kassas and El-Taher (2009) isolated a strain of Trichoderma viride from seawater samples collected from the Mediterranean Sea. The fungus could tolerate Cr(VI) up to 1000 mg l−1 concentration. Transmission electron microscopic studies revealed that the mycelial and conidial structures were not affected by chromium accumulation. Further, the authors optimized Cr(VI) removal from aqueous solution by T. viride using response surface methodology (RSM) and observed the percentage Cr removal efficiency to be significantly influenced by contact time, biosorbent dosage, initial metal concentration, and pH. The authors viewed the highest chromium removal (4.66 mgg−1) capacity of marine T. viride as a promising property for its application for the mycoremediation of Cr(VI) from water systems. Khambhaty et al. (2009a) investigated hexavalent chromium removal potential of three marine aspergilli, namely, Aspergillus niger, A. wentii, and A. terreus, isolated from Gujarat coast and reported A. niger to be the most promising among the three. They carried out further studies related to evaluation of the best biosorption parameters and quantitative analysis of Cr(VI) sorption capacity using A. niger and observed that under optimum conditions 117.33 mg Cr(VI) could be adsorbed per gram of dead biomass of A. niger. Sorption efficiency of the biomass was found to be 100% at 10–100 mg l−1 and 95% at 150 mg l−1 of Cr(VI) concentrations. Further, Khambhaty et al. (2009b) carried out kinetics, equilibrium, and thermodynamic studies on Cr(VI) biosorption by marine Aspergillus niger. Based on the kinetics studies, they reported that the best fit to the experimental data was shown by the pseudo-second-order model. Authors speculated the possible involvement of film diffusion in the sorption process. Among the five two-parameter isotherms examined, Langmuir isotherm model provided the best fit to the experimental data. Based on the studies on thermodynamic parameters of the biosorption, the authors reported the biosorption process to be endothermic. The FTIR analysis of the biomass exposed to Cr(VI) revealed involvement of amino, −CH2, hydroxyl, and phosphorous groups for binding of Cr(VI) to A. niger. Gomathi et al. (2012) screened three species of thraustochytrids, viz., Aplanochytrium sp., Thraustochytrium sp. and Schizochytrium sp. for chromium accumulation efficiency. Further studies related to adsorption kinetics and optimization using response surface methodology were carried out using Aplanochytrium sp. 69.4% chromium removal was obtained by Aplanochytrium sp.


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Yeasts from marine environment have comparatively been less explored for metal removal. Bankar et al. (2009) studied Cr(VI) removal for the first time using two marine strains of Yarrowia lipolytica (NCIM 3589 and 3590, tropical marine and psychrotrophic marine, respectively). The authors observed maximum chromium biosorption at pH 1 and temperature 35 °C. Here also, enhanced biosorption was observed with increasing concentrations of Cr(VI) ions. Analysis using scanning electron microscope equipped with an energy-dispersive spectrometer (SEM- EDS) as well as with ED-X-ray fluorescence (ED-XRF) revealed surface sequestration of Cr(VI) by marine Yarrowia lipolytica. Involvement of amide, carboxyl, and hydroxyl groups on the cell surfaces in chromium binding was confirmed by Fourier transform infrared (FTIR) spectroscopy. Further, Rao et al. (2013) harnessed the reductive power of phyto-inspired Fe0/ Fe3O4 to enhance the Cr(VI) removal by Yarrowia lipolytica (NCIM 3589 and NCIM 3590). Fe0/Fe3O4 nanocomposite-modified cells of Yarrowia lipolytica (NCIM 3589 and NCIM 3590) were used for Cr(VI) removal under different conditions. Higher values of Langmuir and Scatchard coefficients exhibited by the surface modified yeast cells than the unmodified cells indicated the modified cells to be more efficient in Cr(VI) removal and observed that the specific uptake was almost three times higher than unmodified cells. Imandi et al. (2014) employed Doehlert experimental design and carried out optimization of chromium biosorption using marine yeast Yarrowia lipolytica. Effect of three independent variables pH, initial chromium concentration, and biomass dosage on chromium uptake was examined, and 40.32% chromium biosorption was obtained.

2.3.2 Arsenic Arsenic (As) is a toxic, nonessential metalloid that is rated 20th in natural abundance and has been classified as a group A and category 1 human carcinogen (US EPA, 1997; International Association for Research on Cancer IARC 2004; Vala 2010; Bahar et al. 2013). Arsenic occurs naturally in inorganic and organic forms, besides it is released into the environment by various anthropogenic activities including burning of fossil fuel, farming, mining, and industrial activities (Shrestha et al. 2008; Prasad et al. 2013). Inorganic form of arsenic is more toxic and exists as trivalent and pentavalent, i.e., in the As(III) and As(V) form, respectively (Pokhrel and Viraraghavan 2006). Compared to As(V), As(III) is ten times more toxic, though its percentage abundance is only 40% (Oremland and Stolz 2003; Shrestha et al. 2008). Both As(III) and As(V) exert cellular damages to biological systems but with different mechanism. As(III) uptake is believed to occur via transporters of glycerol and by reacting with free thiol groups in proteins; As(III) inhibits important metabolic reactions, e.g., coenzyme A production and citric acid cycle. As(V) shares structural analogy with inorganic phosphate; hence, its entry into the cell is facilitated via the phosphate uptake system resulting in disruption of metabolic reactions

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that require phosphorylation and inhibition of ATP synthesis (Shrestha et al. 2008; Dey et al. 2016; Vala 2010). It can be said that microbial arsenic tolerance study is as old as 1932. Thom and Raper (1932), while examining methylation of arsenic by fungi, observed that besides the fungi, which did so, a number of fungi including a few Mucor, Penicillium expansum, P. chrysogenum, P. roqueforti, Aspergillus flavus, A. oryzae, and Helminthosporium sp. exhibited good growth in presence of up to 0.2% As2O3. Belsky et al. (1970) reported arsenate to be a potent inhibitor of phosphate uptake in the marine fungus Dermocystidium sp. and the degree of inhibition was reported to be dependent on arsenate to phosphate ratio. Microorganisms including fungi in the marine environment play a significant role in reducing the toxicity of arsenic (Bełdowski et al. 2013). While a number of reports are available on marine bacterial role in arsenic remediation, only few reports exist on fungi from marine environment (Vidal and Vidal 1980; Takeuchi et al. 2007; Handley et al. 2009; Vala 2010; Keren et al. 2015; Khambholja and Kalia 2016). While examining the effect of copper-chrome-arsenate preservative and its constituents on the growth of aquatic microorganisms, Irvine and Jones (1975) observed marine fungi to be more tolerant than nonmarine fungi. Especially, the MIC value for As2O5 was 1220 mg l–l for marine fungus Dendryphiella salina, while that for nonmarine fungus Botryosporium sp. has the MIC value 224 mg l–l for As2O5. Kirby et al. (2002) studied arsenic concentrations and speciations in a mangrove ecosystem in Australia. They observed relatively higher arsenic concentration in epiphytic algae/fungi associated with mangrove fine roots as compared to that in mangrove leaves, bark, or main roots and algae/fungi attached to main roots. Gujarat is comprising of India’s 22% of coastline and has been observed to be a reservoir of fungal biota with diverse potentials including arsenic removal (Vala et al. 2000, 2004, 2010, 2012, 2016a, b; Khanbhaty et al. 2009a, b; Vala and Patel 2011; Vala and Dave 2015). Figure 2.3 shows the mycobiota isolated from the coastal habitats of Bhavnagar. To the best of authors’ knowledge, work on arsenic removal using fungi from marine habitats in India has been initiated for the first time by Bhavnagar University (now Maharaja Krishnakumarsinhji Bhavnagar University). We, at MK Bhavnagar University, took up the work on bioremediation of arsenic by facultative marine fungi. A facultative marine Aspergillus sp. isolated from coastal waters of Bhavnagar, West Coast of India, was examined for its arsenic tolerance and accumulation potential at supplied concentration 100 mg l–l of As(III) as sodium arsenite or As(V) as sodium arsenate (Vala and Upadhyay 2008). The fungus could tolerate the supplied As concentration; however, growth initiation lagged behind in case of exposure to As(V). As revealed by hydride generation atomic absorption spectrophotometry, accumulation of As(V) was more than As(III). The presence of arsenic in the biomass was further confirmed by energy-dispersive X-ray spectroscopic (EDX) analysis.


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Fig. 2.3 Marine-derived fungi from Bhavnagar coast, West Coast of India

Vala et al. (2010) examined tolerance of facultative marine Aspergillus flavus toward As(V) at concentrations 25 mg l–l and 50 mg l–l. The fungus isolated from coastal waters of Bhavnagar exhibited tolerance to test As(V) concentrations as reflected by luxuriant growth of the fungus at supplied As(V) concentrations. The increase in accumulation of arsenic was observed with increasing supplied As(V) concentrations. Vala et al. (2011) examined the tolerance of facultative marine Aspergillus niger to trivalent arsenic and also examined its arsenic removal potential. The fungus exhibited noteworthy tolerance to supplied As(III) concentrations (25, 50, and 100 mg l−1). Invariably, highest arsenic removal by A. niger (mg g−1 dry weight of biomass) was observed on day 3, and among different concentrations supplied, maximum content (mgg−1 dry weight of biomass) was observed in case of 100 mg l–l followed by 50 and 25 mg l–l As(III). Figure 2.4 shows growth of A. niger and in turn, its tolerance to different concentrations of As(III). Potential of A. niger as biosorbent has been reviewed by Vala (2009). Marine- derived A. niger was observed to further strengthen the perception. Vala and Patel

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Fig. 2.4 Growth of Aspergillus niger (a) on Petri plates with different concentrations of As(III) on day 7 (b) from left to right in control, 25, 50, and 100 mg l−1 As(III) on day 9

(2011) used heat-killed biomass of A. niger and examined its biosorption ability as a function of initial As(III) concentration. Increased biosorption was observed with increasing concentration of As(III). At all supplied concentrations, the fungus could remove >90% As(III). Highest biosorption observed was 108.083 mg g−1 at As concentration 600 mg l−1. The authors suggested the facultative marine A. niger biomass as efficient biosorbent with potential bioremediation ability. Two facultative marine fungi Aspergillus flavus and Rhizopus sp. isolated from the waters of the Bhavnagar coast, West Coast of India, were examined for their As(III) tolerance and removal efficiency (Vala and Sutariya 2012). Both the test isolates exhibited tolerance to sodium arsenite (As(III)) at concentrations 25 mg l–l and 50 mg l–l, as revealed by their biomass accumulation. Arsenic accumulation also was observed in both the fungi; Rhizopus sp. was observed to be a better accumulator. Here also, as in other cases, higher accumulation was observed with higher supplied As concentration which is suggestive of higher complexation rates between the metal and metal complexing group on the biomass, when the metal is present in higher concentrations. Aspergillus sydowii, isolated along Bhavnagar coast, exhibited noteworthy tolerance toward trivalent as well as pentavalent arsenic. The fungus tolerated arsenic at a concentration of 2000 mg l−1 (Vala 2017). Biovolatilization is considered as one of the mechanisms which can be efficiently harnessed for bioremediation of arsenic- contaminated sites. Volatilization of 15.75% of supplied As(III) by A. sydowii was observed, suggesting it as a potential candidate for arsenic bioremediation. Hence, explorations on arsenic bioremediation made at MK Bhavnagar University reveal marine-derived fungi in general and that isolated from Gujarat, as potential candidates for arsenic removal. Figure 2.5 shows growth of fungi from marine habitats in different concentrations of arsenite, while Fig. 2.6 shows scanning electron microscopic (SEM) images of A. niger and A. sydowii exposed to arsenate. The role of fungi in As biosequestration in hydrothermal fields has also been studied. Dekov et al. (2013) examined inorganic and biogenic As-sulfides


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Fig. 2.5 Growth of fungi (from left to right) in control, 25, 50, and 100 mg l−1 As(III) on day 9

Fig. 2.6 SEM image of (a) Aspergillus niger and (b) A. sydowii exposed to arsenite

p recipitation at seafloor hydrothermal fields and concluded that biogenic orpiment, As2S3, was represented by mineralized fungal hyphae. The authors claim this orpiment precipitation as a mechanism of hydrothermal As biosequestration. Yeasts in the marine environment play a crucial role in reducing toxicity of arsenic. However, they are not explored much for arsenic remediation. The marine yeast

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Rhodotorula rubra has been studied in detail for arsenic metabolism (Button et al. 1973; Vidal and Vidal 1980; Cullen and Reimer 1989; Maher and Butler 1988). Button et al. (1973) studied kinetics of phosphate-arsenate uptake, inhibition, and phosphate-limited growth of a marine yeast Rhodotorula rubra. They projected that the arsenic toxicity was directly related to phosphate concentration, as arsenate- phosphate concentration ratios in metabolic pools would be similar to external concentration ratios. Arsenate toxicity was observed to be competitively prevented by phosphate. Arsenic metabolism for marine yeast Rhodotorula rubra exposed to As(V) was studied by Vidal and Vidal (1980). Production of As(III), methylarsonic acid [CH3AsO(OH)2], dimethylarsinic acid (CH3)2AsO(OH), and volatile alkylarsines was revealed based on the qualitative determination of the metabolism products. The fungus brought about reduction of arsenate to arsenite. However, the produced arsenite was not accumulated, but some of it was transported into the culture medium; the remaining arsenite was methylated. Finally the dimethylarsenic acid was methylated further leading to formation of volatile alkylarsine. Unlike terrestrial fungi, R. rubra did not produce arsonium phospholipids. To the best of authors’ knowledge, there are no recent reports on interaction of marine yeasts with arsenic.

2.4 Conclusion Marine-derived fungi have been observed as promising candidates for bioremediation of various pollutants. However, yet their potential is comparatively untapped. Explorations of more and more marine habitats would reveal new mycobiota with application potentialities. Marine-derived fungi and especially their enzymes involved in bioremediation processes need to be studied in detail. Investigations on molecular details and gene transfer studies in suitable expression systems could be envisaged important in speeding up developing cost-effective applications for bioremediation on a larger scale. Acknowledgments Thanks are due to the Department of Science and Technology, Government of India, New Delhi, for financial support under Women Scientists’ Scheme [SR/WOS-A/ LS-307/2013(G)] to AKV.

References Akcil A, Erust C, Ozdemiroglu S, Fonti V, Beolchini F (2015) A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J Clean Prod 86:24–36 Anonymous (2012) Paint Coat Ind 28:8


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Arun A, Raja PP, Arthi R, Ananthi M, Kumar KS, Eyini M (2008) Polycyclic aromatic hydrocarbons (PAHs) biodegradation by basidiomycetes fungi, Pseudomonas isolate, and their cocultures: comparative in vivo and in silico approach. Appl Biochem Biotechnol 151:132–142 Bahar MM, Megharaj M, Naidu R (2013) Bioremediation of arsenic-contaminated water: recent advances and future prospects. Water Air Soil Pollut 224:1722 Bankar AV, Kumar AR, Zinjade SS (2009) Removal of chromium (VI) ions from aqueous solution by adsorption onto two marine isolates of Yarrowia lipolytica. J Hazard Mater 170(1):487–494 Baughman GL, Weber EJ (1994) Transformation of dyes and related compounds in anoxic sediment: kinetics and products. Environ Sci Technol 28:267–276 Bełdowski J, Szubska M, Emelyanov E (2013) Spatial variability of arsenic concentrations in Baltic sea surface sediments in relation to sea dumped chemical munitions. E3S Web of Conferences 1, 16002 doi: https://doi.org/10.1051/ e3sConf/ 201301160 02 Belsky MM, Goldstein S, Menna M (1970) Factors affecting phosphate uptake in the marine fungus Dermocystidium sp. J Gen Microbiol 62:399–402 Bonugli-Santos RC, Durrant LR, Sette LD (2012) The production of ligninolytic enzymes by marine-derived basidiomycetes and their biotechnological potential in the biodegradation of recalcitrant pollutants and the treatment of textile effluents. Water Air Soil Pollut 223:2333–2345 Bonugli-Santos RC, dos Santos Vasconcelos MR, Passarini MRZ, Vieira GAL, Lopes VCP, Mainardi PH, dos Santos JA, de Azevedo Duarte L, Otero IVR, da Silva Yoshida AM, Feitosa VA, Pessoa A Jr, Sette LD (2015) Marine-derived fungi: diversity of enzymes and biotechnological applications. Front Microbiol 6:269. https://doi.org/10.3389/fmicb.2015.00269 Bonugli-Santos RC, Vieira GAL, Collins C, Fernandes TCC, Marin-Morales MA, Murray P, Sette LD (2016) Enhanced textile dye decolorization by marine-derived basidiomycete Peniophora sp. CBMAI 1063 using integrated statistical design. Environ Sci Pollut Res 23:8659–8668 Button DK, Dunker SS, Morse ML (1973) Continuous culture of Rhodotorula rubra: Kinetics of phosphate-arsenate uptake, inhibition, and phosphate-limited Growth. J Bacteriol 113(2):599–611 Chander K, Dyckmans J, Höper H, Raubuch M (2001a) Long term effects on soil microbial properties of heavy metals from industrial exhaust deposition. J Plant Nutr Soil Sci 164(6):657–663 Chander K, Dyckmans J, Joergensen R, Meyer B, Raubuch M (2001b) Different sources of heavy metals and their long-term effects on soil microbial properties. Biol Fertil Soils 34(4):241–247 Chaukura N, Gwenzi W, Tavengwa N, Manyuchi MM (2016) Biosorbents for the removal of synthetic organics and emerging pollutants: opportunities and challenges for developing countries. Environ Dev 19:84–89 Ciullini I, Tilli S, Scozzafava A, Briganti F (2008) Fungal laccase, cellobiose dehydrogenase, and chemical mediators: combined actions for the decolorization of different classes of textile dyes. Bioresour Technol 99:7003–7010 Costa M (2003) Potential hazards of hexavalent chromate in our drinking water. Toxicol Appl Pharmacol 188:1–5 Cullen WR, Reimer KJ (1989) Arsenic speciation in the environment. Chem Rev 89:713–764 D’Souza DT, Tiwari R, Shah AK, Raghukumar C (2006) Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzym Microb Technol 38:504–511 D’Souza-Ticlo D, Garg D, Raghukumar C (2009a) Effects and interactions of medium components on laccase from a marine-derived fungus using response surface methodology. Mar Drugs 7:672–688 D’Souza-Ticlo D, Sharma D, Raghukumar C (2009b) A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus. Mar Biotechnol 11:725–737 Dekov VM, Bindi L, Burgaud G, Petersen S, Asael D, Rédou V et al (2013) Inorganic and biogenic As-sulfide precipitation at seafloor hydrothermal fields. Mar Geol 342:28–38 Deshmukh R, Khardenavis AA, Purohit HJ (2016) Diverse metabolic capacities of fungi for bioremediation. Indian J Microbiol 56(3):247–264 Dey U, Chatterjee SN, Mondal NK (2016) Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnol Rep 10:1–7

34


Diwaniyan S, Kharb D, Raghukumar C, Kuhad RC (2010) Decolorization of synthetic dyes and textile effluents by basidiomycetous fungi. Water Air Soil Pollut 210:409–419 El Aty AAA, Mostafa FA (2013) Effect of various media and supplements on laccase activity and its application in dyes decolorization. Malaysian J Microbiol 9(2):166–175 El Aty AAA, Hamed ER, El-Beih AA, El-Diwany AI (2016) Induction and enhancement of the novel marine-derived Alternaria tenuissima KM651985 laccase enzyme using response surface methodology: Application to Azo and Triphenylmethane dyes decolorization. J Appl Pharm Sci 6(4):6–14 El Aty AAA, Mostafa FA, Hassan ME, Hamed ER, Esawy MA (2017) Covalent immobilization of Alternaria tenuissima KM651985 laccase and some applied aspects. Biocatal Agricult Biotechnol 9:74–81 El-Kassas HY, El-Taher EM (2009) Optimization of batch process parameters by response surface methodology for mycoremediation of chrome-VI by a chromium resistant strain of marine Trichoderma viride. Am-Eurasian J Agric Environ Sci 5(5):676–681 Farooq U, Kozinski JA, Khan MA, Athar M (2010) Biosorption of heavy metal ions using wheat based biosorbents-A review of the recent literature. Bioresour Technol 101:5043–5053 Field JA, de Jong ED, Costa GF, de Bond JAM (1992) Biodegradation of polycyclic aromatic hydrocarbons by new isolates of white rot fungi. Appl Environ Microbiol 58:2219–2226 Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60 Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111(1):3–49 Gomathi V, Saravanakumar K, Kathiresan K (2012) Biosorption of chromium by mangrove- derived Aplanochytrium sp. Afr J Biotechnol 11(95):16177–16186 Gupta VK, Shrivastava AK, Jain N (2001) Biosorption of chromium(VI) from aqueous solutions by green algae Spirogyra species. Water Res 35:4079–4085 Handley KM, Héry M, Lloyd JR (2009) Redox cycling of arsenic by the hydrothermal marine bacterium Marinobacter santoriniensis. Environ Microbiol 11(6):1601–1611 Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192 Horitsu H, Futo S, Miyazawa Y, Ogai S, Kawai K (1987) Enzymatic reduction of hexavalent chromium by hexavalent chromium tolerant Pseudomonas ambigua G-1. Agric Biol Chem 51:2417–2420 Huiying C, Mingxia W, Yubin S, Shan-jing Y (2014) Optimization of two-species whole-cell immobilization system constructed with marine-derived fungi and its biological degradation Ability. Chin J Chem Eng 22(2):187–192 Hyde KD, Gareth Jones EB, Leano E, Pointing SB, Poonyth AD, Vrijmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161 IARC (2004) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Some Drinking-Water Disinfectants and Contaminants, including Arsenic, vol 84. IARC Press, Lyon. 192 IARC Monographs, vol. 86 Imandi SB, Chinthala R, Saka S, Vechalapu RR, Nalla KK (2014) Optimization of chromium biosorption in aqueous solution by marine yeast biomass of Yarrowia lipolytica using Doehlert experimental design. Afr J Biotechnol 13(12):1413–1422 Irvine J, Jones EBG (1975) The effect of a Copper-Chrome-Arsenate preservatives and its constituents on the growth of aquatic microorganisms. J Inst Wood Sci 7:1–5 Joshi HV, Vala AK, Bhatt PN, Anand N (2012) Treatment of CETP effluent by a seaweed associated Aspergillus niger isolate. In: Sahoo D, Kaushik BD (eds) Algal Biotechnology and Environment. I.K. International Publishing House, New Delhi, pp 193–197 Katz SA, Salem H (1993) The toxicology of chromium with respect to its chemical speciation: a review. J Appl Toxicol 13:217–224 Kaufman BD (1970) Acute potassium dichromate poisoning in man. Am J Dis Child 119:374–379 Keren R, Lavy A, Mayzel B, Ilan M (2015) Culturable associated-bacteria of the sponge Theonella swinhoei show tolerance to high arsenic concentrations. Front Microbiol 6:154. https://doi. org/10.3389/fmicb.2015.00154


35

Khambhaty Y, Mody K, Basha S, Jha B (2009a) Biosorption of Cr(VI) onto marine Aspergillus niger: experimental studies and pseudo-second order kinetics. World J Microbiol Biotechnol 25:1413–1421 Khambhaty Y, Mody K, Basha S, Jha B (2009b) Kinetics, equilibrium and thermodynamic studies on biosorption of hexavalent chromium by dead fungal biomass of marine Aspergillus niger. Chem Eng J 145:489–495 Khambholja DB, Kalia K (2016) Seasonal variation in arsenic concentration and its bioremediation potential of marine bacteria isolated from Alang-Sosiya ship-scrapping yard, Gujarat, India. Defence Life Sci J 1(1):78–84 Khan M, Scullion J (2000) Effect of soil on microbial responses to metal contamination. Environ Pollut 110:115–125 Kirby J, Maher W, Chariton A, Krikowa F (2002) Arsenic concentrations and speciation in a temperate mangrove ecosystem, NSW, Australia. Appl Organometal Chem 16:192–201 Kocberber N, Donmez G (2007) Chromium(VI) bioaccumulation capacities of adapted mixed cultures isolated from industrial saline wastewaters. Bioresour Technol 98:2178–2183 Komori K, Wang P, Toda K, Ohtake H (1989) Factors affecting chromate reduction in Enterobacter cloacae strain H01. Appl Microbiol Biotechnol 31:567–570 Kotas J, Stasicka Z (2000) Chromium occurrence in the environment and methods of its speciation. Environ Pollut 107:263–283 Lu T, Zhang Q, Yao S (2016) Efficient decolorization of dye-containing wastewater using mycelial pellets formed of marine-derived Aspergillus niger. Chin J Chem Eng 25:330–337. https://doi. org/10.1016/j.cjche.2016.08.010 Lui T, Li H, Li Z, Xiao X, Chen L et al (2007) Removal of hexavalent chromium by fungal biomass of Mucor racemosus: influencing factors and removal mechanism. World J Microbiol Biotechnol 23:1685–1693 Maher W, Butler E (1988) Arsenic in the marine environment. Appl Organomet Chem 2:191–214 Merrin JS, Sheela R, Saswathi N, Prakasham RS, Ramakrishna SV (1998) Biosorption of chromium VI using Rhizopus arrhizus. Ind J Exp Biol 36:1052–1055 Millward RN, Carman KR, Fleeger JW, Gambrell RP, Powell RT, Rouse MA (2001) Linking ecological impact to metal concentrations and speciation: a microcosm experiment using a salt marsh meiofaunal community. Environ Toxicol Chem 20:2029–2037 Mtui G, Nakamura Y (2008) Lignocellulosic enzymes from Flavodon flavus, a fungus isolated from Western Indian ocean off the coast of Dar es Salaam, Tanzania. Afr J Biotechnol 7(17):3066–3072 Newell SY, Barlocher F (1993) Removal of fungal and total organic matter from decaying cordgrass leaves by shredder snails. J Exp Mar Biol Ecol 171:39–49 Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil microbial characteristics. J Biosci Bioeng 102(3):157–161 Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 299:939–944 Pachiadaki MG, Rédou V, Beaudoin DJ, Burgaud G, Edgcomb VP (2016) Fungal and prokaryotic activities in the marine subsurface biosphere at Peru margin and Canterbury basin inferred from RNA-Based analyses and microscopy. Front Microbiol 7:846. https://doi.org/10.3389/ fmicb.2016.00846 Park D, Yun YS, Park JM (2005) Studies on hexavalent chromium biosorption by chemically treated biomass of Ecklonia sp. Chemosphere 60:1356–1364 Pokhrel D, Viraraghavan T (2006) Arsenic removal from an aqueous solution by a modified fungal biomass. Water Res 40:549–552 Prasad KS, Ramanathan AL, Paul J, Subramanian V, Prasad R (2013) Biosorption of arsenite (As+3) and arsenate (As+5) from aqueous solution by Arthrobacter sp. biomass. Environ Technol 34:2701–2708 Raghukumar C (2000) Fungi from marine habitats: an application in bioremediation. Mycol Res 104(10):1222–1226 Raghukumar C, D’Souza TM, Thorn RG, Reddy CA (1999) Lignin-modifying enzymes of Flavodon flavus, a basidiomycete isolated from a coastal marine environment. Appl Environ Microbiol 65:2103–2111

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Raghukumar C, Muraleedharan U, Gaud VR, Mishra R (2004) Simultaneous detoxification and decolorization of molasses spent wash by the immobilized white-rot fungus flavodon flavus isolated from a marine habitat. Enzym Microb Technol 35:197–202 Ramrakhiani L, Majumder R, Khowala S (2011) Removal of hexavalent chromium by heat inactivated fungal biomass of Termitomyces clypeatus: Surface characterization and mechanism of biosorption. Chem EngJ 171:1060–1068 Rao A, Bankar A, Kumar AR, Gosavi S, Zinjarde S (2013) Removal of hexavalent chromium ions by Yarrowia lipolytica cells modified with phyto-inspired Fe0/Fe3O4 nanoparticles. J Conta Hydrol 146:63–73 Ravikumar S, Williams GP, Shanthy S, Gracelin NA, Babu S, Parimala PS (2007) Effect of heavy metals (Hg and Zn) on the growth and phosphate solubilising activity in halophilic phosphobacteria isolated from Manakudi mangrove. J Environ Biol 28:109–114 Regine HSF, Volesky VB (2000) Biosorption: a solution to pollution. Int Microbiol 3:17–24 Rodriguez JPG, Williams DE, Sabater ID, Bonugli-Santos RC, Sette LD, Andersen RJ, Berlinck RGS (2015) The marine-derived fungus Tinctoporellus sp. CBMAI 1061 degrades the dye Remazol Brilliant Blue R producing anthraquinones and unique tremulane sesquiterpenes. RSC Adv 5(81):66360–66366 Samuel M, Abigail EA, Chidambaram R (2015) Isotherm modelling, kinetic study and optimization of batch parameters using response surface methodology for effective removal of Cr(VI) using fungal biomass. PLoS One 10(3):e0116884. https://doi.org/10.1371/journal.pone.0116884 Sarvanakumar K, Kathiresan K (2014) Bioremoval of the synthetic dye malachite green by marine Trichoderma sp. Springer Plus 3:631 Shrestha RA, Lama B, Joshi J, Sillanpää M (2008) Effects of Mn(II) and Fe(II) on microbial removal of arsenic(III). Environ Sci Pollut Res 15:303–307 Smith WL, Gadd GM (2000) Reduction and precipitation of chromate by mixed culture sulphate- reducing bacterial biofilms. J Appl Microbiol 88(6):983–991 Srinath T, Verma T, Ramteke PW, Garg SK (2002) Chromium (VI) biosorption and bioaccumulation by chromate resistant bacteria. Chemosphere 48(4):427–435 Subbaiah MV, Kalyani MVS, Reddy GS, Boddu VM, Krishnaiah A (2008) Biosorption of Cr(VI) from aqueous solutions using Trametes versicolor polyporus fungi. J Chem 5(3):499–510 Taboski MAS, Rand TG, Piorko A (2005) Lead and Cadmium uptake in the marine fungi Corollospora lacera and Monodyctis pelagia. FEMS Microbiol Ecol 53:445–453 Takeuchi M, Kawahata H, Gupta LP, Kita N, Morishita Y, Ono Y, Komai T (2007) Arsenic resistance and removal by marine and non-marine bacteria. J Biotechnol 127(3):434–442 Thom C, Raper KB (1932) The arsenic fungi of GOSIO. Science 76:548 Torres JMO, Cardenas CV, Moron LS, Guzman APA, dela Cruz TEE (2011) Dye decolorization activities of marine-derived fungi isolated from Manila Bay and Calatagan Bay. Philippine J Sci 140(2):133–143 Tucker MD, Barton LL, Thomson BM (1998) Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilised in polyacrylamide gels. J Ind Microbiol Biotechnol 20:13–19 US Environmental Protection Agency (1988) Toxicological review of hexavalent chromium, National Center for Environmental Assessment. Office of Research and Development, Washington, DC US EPA (US Environmental Protection Agency) (1997) IRIS (Integrated Risk Information System) On-line Database Maintained in Toxicology Data Network (TOXNET) by the National Library of Medicine. Bethesda, Maryland. Vala AK (2009) Aspergillus niger and heavy metal removal: a perception. Res J Biotechnol 4(1):75–79 Vala AK (2010) Tolerance and removal of arsenic by a facultative marine fungus Aspergillus candidus. Bioresour Technol 101:2565–2567 Vala AK (2017) On the extreme tolerance and removal of arsenic by a facultative marine fungus Aspergillus sydowii in: Gautam A, Pathak C (ed) Metallic contamination and its toxicity (Accepted)


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Vala AK, dave BP (2015) Explorations on marine-derived fungi for L-Asparaginase- enzyme with anticancer potentials. Curr Chem Biol 9(1):66–69 Vala AK, Patel RJ (2011) Biosorption of trivalent arsenic by facultative marine Aspergillus niger. In: Mason A (ed) Bioremediation: biotechnology, engineering and environmental management. Nova Science Publishers, New York, pp 459–464 Vala AK, Sutariya V (2012) Trivalent arsenic tolerance and accumulation in two facultative marine fungi. Jundishapur J Microbiol 5:542–545 Vala AK, Upadhyay RV (2008) On the tolerance and accumulation of arsenic by facultative marine Aspergillus sp. Res J Biotechnol 366–368 (special issue Proceedings of ISBT – 2008) Vala AK, Vaidya SY, Dube HC (2000) Siderophore production by facultative marine fungi. Indian. J Mar Sci 29:339–340 Vala AK, Anand N, Bhatt PN, Joshi HV (2004) Tolerance and accumulation of hexavalent chromium by two seaweed associated aspergilli. Mar Poll Bull 48(9&10):983–985 Vala AK, Davariya V, Upadhyay R (2010) An investigation on tolerance and accumulation of a facultative marine fungus Aspergillus flavus to pentavalent arsenic. J Ocean Univ China 9:65–67 Vala AK, Sutariya V, Upadhyay RV (2011) Investigations on trivalent arsenic tolerance and removal potential of a facultative marine Aspergillus niger. Environ Progr Sustain Energy 30(4):586–588 Vala AK, Chudasama B, Patel RJ (2012) Green synthesis of silver nanoparticles using marinederived fungus Aspergillus niger. Micro Nano Lett 7:859–862 Vala AK, Dudhagara D, Dave BP (2016a) Enhanced L-asparaginase production by a marine- derived euryhaline Aspergillus niger strain AKV MKBU – a statistical model. Indian J Marine Sci (Accepted for publication) Vala AK, Trivedi HB, Dave BP (2016b) Marine-derived fungi: potential candidates for fungal nanobiotechnology. In: Prasad R (ed) Advances and applications through fungal nanobiotechnology. Springer International Publishing, Cham, pp 47–69 Verma AK, Raghukumar C, Verma P, Shouche YS, Naik CG (2010) Four marine-derived fungi for bioremediation of raw textile mill effluents. Biodegrdation 21(2):217–233 Verma AK, Raghukumar C, Parvatkar RR, Naik CG (2012) A rapid two-Step bioremediation of the Anthraquinone Dye, Reactive Blue 4 by a marine-derived fungus. Water Air Soil Pollut 223:3499–3509 Vidal FV, Vidal MV (1980) Arsenic metabolism in marine bacteria and yeast. Mar Biol 60(1):1–7 Wang G (2006) Diversity and biotechnological potential of the sponge-associated microbial consortia. J Ind Microbiol Biotechnol 33:545–551 Wang YT, Shen H (1995) Bacterial reduction of hexavalent chromium. J Ind Microbiol 14:159–163 Wang MX, Zhang QL, Yao SJ (2015) A novel biosorbent formed of marine-derived Penicillium janthinellum mycelial pellets for removing dyes from dye-containing wastewater. Chem Eng J 259:837–844 Yanto DHY, Tachibana S, Itoh K (2014) Biodecolorization and biodegradation of textile dyes by the newly isolated saline-pH tolerant fungus Pestalotiopsis sp. J Environ Sci Technol 7(1):44–55

Chapter 3

Biofilm: A Next-Generation Biofertilizer Talat Parween, Pinki Bhandari, Zahid Hameed Siddiqui, Sumira Jan, Tasneem Fatma, and P.K. Patanjali

3.1 Introduction Biofilm can be defined as a thin layer of mucilage adhering to a solid surface containing bacterial community and other microorganisms. Biofilm develops by the attachment of microorganisms to surfaces. It is an attribute of microorganisms (bacteria) that is found everywhere either in natural or artificial surface (Stoodley et al. 2004; Stewart and Franklin 2008). Naturally, bacteria live in aggregates and attach to solid surfaces along with close contact to other bacterial cells (Webb et al. 2003; Parsek and Fuqua 2004; Stoodley et al. 2002). Along with various proteins, exopolysaccharides, and DNA, bacterial cells produce a variety of extracellular polymeric substances (EPS) while attached on the surface. It has diverse physiological structures, and its structure varies from cell to cell within it from each other. It also varies from cell to cell in terms of up- and downregulation of genes. The cells of biofilms are very responsive to a variety of functions of their environment such as they transform their metabolic functions, react to nutrient products, waste product gradients, engage cell-cell communication, and make contact with adjacent cells. During recent years, in the process of biofilm formation, primary scientific interest has grown exponentially, and studies of the regulation have begun to reveal

T. Parween • P. Bhandari (*) • P.K. Patanjali Institute of Pesticide Formulation Technology, Gurgaon, India e-mail: [email protected] Z.H. Siddiqui Department of Biology, University of Tabuk, Tabuk, Kingdom of Saudi Arabia S. Jan ICAR-Central Institute of Temperate Horticulture, Srinagar, India T. Fatma Department of Bioscience, Jamia Millia Islamia, New Delhi, India © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_3

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molecular mechanisms that are involved in the transition of the planktonic to the biofilm state of living. Biofilm formation is an important part of bacterial infection and disease, including tooth decay, endocarditis, and chronic lung infection in cystic fibrosis patients. Biofilms formed on abiotic surfaces are vital source for infections, such as biofilms formed on medical devices and implants (Donlan and Costerton 2002). Biofilms have a huge impact on various sectors and exhibit both harmful and beneficial activities in industrial, medical, and agricultural field. The significance of bacterial biofilms has highly stimulated the elucidation of the regulatory mechanisms involved in their formation, maturation, and dissolution. Formation of biofilm under varying stress conditions is a significant strategy adopted by bacterial strains for their successful survival in plant rhizosphere. The effect of biofilm forming plant growth-promoting rhizobacteria on salinity tolerance in barley was studied by Kasim et al. (2016). In this study, the activity of biofilm formation of 20 isolates and strains of plant growth-promoting rhizobacteria (PGPR) was determined under different salt concentrations which indicated that all of the 20 PGPRs have the activity of biofilm formation under 0.0, 250, 500, or 1000 mM NaCl which was increased with increasing salt concentration. Colonization and biofilm formation by rhizobacteria play an important role in plant pathogenesis and beneficial interactions (Bloemberg and Lugtenberg 2004). Plant growth-promoting rhizobacteria can be classified as (i) biofertilizers which fix nitrogen, (ii) phytostimulators which promote plant growth directly by production of hormones, and (iii) biocontrol agents which protect plants from infection by phytopathogenic organisms (Bloemberg and Lugtenberg 2004; Prasad et al. 2015). Efficient rhizobacterial biofilm formers should be able to (i) attach to the root surface, (ii) survive in the rhizosphere, (iii) make use of nutrients exuded by the plant root, (iv) proliferate and form microcolonies, (v) efficiently colonize the entire root system, and (vi) compete with indigenous microorganisms (Bloemberg and Lugtenberg 2004). In this chapter focus will be on formation of biofilm and various factors affecting its formation and regulation, ecological advantage and relevance of biofilms, and molecular mechanism of biofilm formation and biocontrol.

3.2 Formation of Biofilm Biofilm might be shaped as collection of substances including living tissues. Development of a biofilm starts with the connection of free-coasting microorganisms to a surface. While still not completely comprehended, it is suspected that the primary pilgrims of a biofilm hold fast to the surface at first through delicate, reversible attachment by means of Van der Waals strengths and hydrophobic effects. If the homesteaders are not instantly isolated from the surface, they can stay themselves all the more for all time utilizing cell bond structures, for example, pili. Hydrophobicity likewise assumes a vital part in deciding the capacity of microbes to frame biofilms, as those with expanded hydrophobicity have decreased shock

3 Biofilm: A Next-Generation Biofertilizer

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Fig. 3.1 Stages involved in biofilm formation (Source: Kulkarni 2016)

between the extracellular network and the bacterium (Santos et al. 2015; Puga et al. 2015; Allen et al. 2015a, b; Loera-Muro et al. 2015). The process of biofilm formation can be divided in distinct developmental steps (Fig. 3.1), which are similar in many bacterial species. The model of biofilm development includes: (i) Initial reversible connection of free swimming microorganisms to surface (ii) Permanent substance connection, single layer, bugs start making sludge (iii) Early vertical advancement (iv) Multiple towers with channels between, developing biofilm (v) Mature biofilm with seeding dispersal of all the free swimming miniaturized- scale living beings

3.3 Factor Affecting Biofilm Formation 3.3.1 Topography of Surface The solid substratum may have a few attributes that are vital in the observance procedure. The degree of microbial colonization seems to be high as the surface coarseness is more. This is because shear strengths are reduced, and surface zone is higher on rougher surfaces. Microorganisms adhere immediately to hydrophobic, nonpolar surfaces, e.g., Teflon and different plastics than to hydrophilic materials, for example, glass or metals (Kulkarni 2016).

3.3.2 Physicochemical Properties of Medium Different characteristics of the watery medium, for example, pH, supplement levels, ionic quality, and temperature, play a vital part in the rate of microbial observance to a substratum. Researcher found that an expansion in the centralization of a few

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Table 3.1 Summary of factors involved in biofilm formation Step of biofilm development Initial attachment to a surface

Factors involved Nutrient availability Stress factors (osmolarity, iron availability, temperature, pH, O2 tension) Iron availability Inorganic phosphate Hydrophobicity/hydrophilicity Flagella and swimming motility

Microcolony formation

Macrocolony formation

Maturation of biofilm

Detachment

Secreted DNA, proteins Pili and twitching Catabolite repression control protein (Crc) Virulence factor regulator (Vfr) Two-component regulatory system (gac) Exopolysaccharide production, alginate Quorum sensing Surfactants Quorum sensing Pheromones RpoS Nutrient limitation Surfactants

Organism Bacillus subtilis Staphylococcus epidermidis Staphylococcus aureus, Escherichia coli S. epidermidis Pseudomonas aureofaciens Pseudomonas fluorescens P. fluorescens P. aeruginosa E. coli S. epidermidis E. coli P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa; Vibrio cholera B. subtilis P. aeruginosa P. aeruginosa P. aeruginosa; B. subtilis

cations (Na, Ca, La, Fe, Mg particle) influenced the connection of microorganisms to glass surfaces, apparently by lessening the appalling powers between the adversely charged bacterial cells and the glass surfaces (Kulkarni 2016).

3.3.3 Hydrodynamics To change in the morphology of biofilms, laminar and turbulent flows are responsible. It is a patchy biofilm formation under laminar flow that shows presence of rough cell aggregates, whereas an elongated biofilm formed under turbulent flow though their morphology is similar like laminar flow biofilms. Cell size and cell motility are also equally important factors involved in biofilm formation (Kulkarni 2016) (Table 3.1).


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3.3.4 Horizontal Gene Transfer The adaptation of microorganisms in new environment occurs because evolution of microbial community takes place. This adaptation is attributed by horizontal gene transfer instead of genetic mutation. Mobile genetic elements such as plasmids, transposons, bacteriophages, etc. are responsible for this genetic transfer. Because of them some microbes are able to express genes responsible to a specific surface where bacteria have decided to settle (Kulkarni 2016).

3.3.5 Quorum Sensing Quorum sensing is a process of cell signaling, in which microorganisms can communicate with each other. Here some extracellular molecules, e.g., acyl-homoserine lactone, are released from one cell and diffuse in environment toward the other one. Such molecules are responsible for making biofilms powerful (Loera-Muro et al. 2015; Islam et al. 2015; Xu and Gu 2015; Pereira et al. 2015; Fard et al. 2015; Maurer et al. 2015).

3.4 Regulation of Biofilm Formation 3.4.1 Initiation of Biofilm Formation It was suggested that the biofilm formation was initiated when bacteria sense certain environmental factors (transition), which may be from planktonic growth to life on a surface (Davey et al. 2000; Stanley and Lazazzera 2004). These signals regulate the surface attachment and formation of microcolony which differ between species to species and maintain the natural habitat of the bacterial species (e.g., a high- osmolarity environment in the case of Staphylococcus epidermidis and S. aureus and a low-osmolarity environment in the case of Escherichia coli). The factors which influence the attachment at the initial stages were osmolarity, pH, iron availability, oxygen tension, and temperature (Fletcher et al. 1996; Nyvad et al. 1990; O’Toole et al. 2000). Whereas inorganic phosphate (Pi) acts as a key environmental factor for Pseudomonas spp. (e.g., for P. aureofaciens and P. fluorescens) by modulating the Phoregulon, which is formed by the PhoR/PhoB two- component regulatory system. Another method is gac system and is highly conserved in pseudomonads and other gram-negative bacteria (Laville et al. 1992). A recent study showed that a P. aeruginosa gacA mutant attaches to the substratum but does not aggregate and does not form microcolonies (Parkins et al. 2001). In E. coli, the EnvZ/OmpR signaling system under conditions of moderate increase of osmolarity is activated (Pratt and Silhavy 1995), suggesting that

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o smolality would stimulate stable cell-surface interactions. However, under high osmolality in a non-favorable environment, the bacterial cells remain in the planktonic phase and free to relocate to more environmentally favorable conditions. The global carbon metabolism is regulated by Crc. This Crc regulates the expression of pilA and pilB which encode for structural protein of type IV pili in P. aeruginosa (O’Toole et al. 2000). This Crc protein is activated by tricarboxylic acid cycle (TCA) intermediates, ensuring that the environmental biofilm formation contains carbon source of P. aeruginosa (O’Toole and Kolter 1998). The involvement of flagella and pili also reported in the initiation of the early attachment processes of E. coli (Genevaux et al. 1996). In Bacillus subtilis, it is a complex regulatory mechanism as well as a number of environmental factors also involved in the initiation of biofilm formation (Wise and Price 1995). The response regulator Spo0A is active under starvation and high cell density (Sonenshein 2000), indicating that these conditions may reflect the environmental conditions under which there is a physiological advantage for B. subtilis to form a biofilm. Finally, the nature of bacterial surface may have a dramatic effect on the attachment governed by electrostatic interactions and depends on hydrophobicity of a bacterial cell due to its LPS composition (De Weger et al. 1989). For example, Dekkers et al. (1998) showed that the presence of the O antigen is necessary for colonization of plant roots by P. fluorescens, associated with the production of EPS (extracellular polymeric substances). The alginate is also known to have a function as an EPS in biofilm production by P. aeruginosa (Govan et al. 1996).

3.4.2 Maturation of the Biofilm Matured biofilms can be thick and homogeneous, or they can consist of complex structures composed of pillars with water channels to allow for nutrient influx and waste efflux (Davey and O’Toole 2000). It was shown that the maturation of biofilm is to be controlled by the availability of nutrients and quorum sensing. In P. aeruginosa, the depth status of the biofilm maturity is reduced by the transcriptional factor RpoS (Whiteley et al. 2001). RpoS production is regulated in gram-negative bacteria in response to different stress conditions including nutrient limitation (Venturi 2003). Thus, RpoS activation signals that nutrients are limiting in P. aeruginosa biofilm, but in E. coli, is required for the initiation of biofilm formation (Adams and McLean 1999), suggesting an analogous role of RpoS in E. coli to the role of Spo0A in biofilm formation by B. subtilis. As a biofilm becomes larger and older, bacterial cells in the center of the film had reduced access to nutrients, producing starvation signal, which activate RpoS in P. aeruginosa to reduce the biofilm thickness. Interestingly, in Vibrio cholerae the thickness is regulated by quorum sensing in mature biofilm (Zhu and Mekalanos 2003).


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3.5 Regulation of the Biofilm Architectural Structure The production of surfactant is required for the architectural structure by reducing the surface tension by B. subtilis and P. aeruginosa to form a biofilm (Branda et al. 2001; Davey et al. 2003). Lipopeptide production is required to form the spore- containing fruiting bodies, which is found at the surface of the B. subtilis biofilm (Branda et al. 2001). In P. aeruginosa, rhamnolipid surfactant production is required for the maintenance of the pillar structures and water channel structures (Davey et al. 2003). In both cases, production of surfactant is regulated by quorum sensing, in B. subtilis by the ComX pheromone and the ComP sensor kinase (Lazazzera et al. 1999) and in P. aeruginosa by the lasI-lasR quorum sensing system (Pearson et al. 1997). Both the formation of fruiting bodies in B. subtilis, which results in the dissemination of spores in a new environment, and the formation of water channels in P. aeruginosa will finally result in the acquisition of nutrients.

3.6 Ecological Advantage and Relevance of Biofilms 3.6.1 Defense Cells are usually surrounded by an extrapolymeric substance matrix in a biofilm, which forms a key component in increasing the resistance and stability against environmental stress factors to the biofilms. The matrix contains mixture of extracellular polysaccharides (EPS), proteins, nucleic acids, and other substances, among these, EPS is the widely studied. Also it provides protection against a variety of environmental stresses, such as UV radiation, pH shifts, osmotic shock, and desiccation (Flemming et al. 2000). EPS also adsorb dissolved organic compounds, such as diclofop-methyl (an herbicide) and other xenobiotics, which is essential in establishing a mechanism by which the bacterial community can concentrate essential nutrients and growth components (Wolfaardt et al. 1998). The tolerance of biofilms against the antimicrobial agents by restricting the diffusion of compounds from the surrounding environment into the biofilm by EPS matrix (Gilbert et al. 1997).

3.6.2 Nutrient Availability and Metabolic Cooperation Syntrophic relationship can be provided by biofilms, in which two metabolically distinct bacteria depend on each other to utilize certain substrates for growth. It has been well studied with reference to methanogenic degradation (Schink et al. 1997). Recently, Kuiper et al. (2001) reported that P. putida strain PCL1445, which was isolated during a selection procedure together with strain PCL1444 from a grass plant heavily polluted by PAHs, does not grow on naphthalene in a pure culture but

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only in the presence of PCL1444. Thus, it was suggested that naphthalene degradation intermediates produced by PCL1444 can be used by PCL1445 in the rhizosphere, resulting in a symbiotic relationship (Kuiper et al. 2001).

3.6.3 Colonization The formation of biofilm provides a special mechanism by which organisms establish and maintain themselves in an unfavorable environment. Plants not only benefit the rhizobacteria for nutrients, but it also influences the plant in a direct or indirect way. Bacteria (Pseudomonas), which are ubiquitous, are frequently associated with plants either as mutualists, saprophytes, or pathogens and therefore have a strong impact on agriculture. The P. syringae which is a plant pathogen survives on aerial parts of host-plants (Hirano and Upper 2000). P. putida is commonly found in the rhizosphere (the root surface and surrounding soil area) and plays a protecting role against an attack of pathogenic microorganisms, directly by affecting the survival or activity of the pathogen or indirectly by the induction of systemic resistance in the plant. The direct mechanism includes the production of antibiotics (e.g., phenazines and HCN) and/or competition for certain nutrients, in particular Fe3+ via the synthesis of siderophores and subsequent uptake of Fe3+-siderophore complexes (Bloemberg and Lugtenberg 2001; Das et al. 2007). The capability of several strains of P. putida is to metabolize toxic aromatic compounds which, in combination with efficient rhizosphere colonization called rhizoremediation (Kuiper et al. 2004).

3.6.4 Acquisition of New Genetic Traits For horizontal gene transfer, plant-associated bacterial populations are the hotspots due to the close proximity of biofilm cells (Dekkers et al. 2000). It provides an ideal environment condition for horizontal exchange, the rapid spread of phages, conjugation, and uptake of plasmid DNA by competent bacteria. Plasmids and phages modified themselves to promote the transition of growth to biofilm mode in their host by cell-cell signaling (Ghigo 2001). Interestingly, this transfer mechanism was regulated by quorum sensing in plant-associated bacteria like Rhizobium and Agrobacterium (He et al. 2003; Piper et al. 1993).

3.7 M olecular Mechanism of Biofilm Formation and Biocontrol tapA-sipW-tasA and epsA-O are two matrix genes that are involved in biofilm formation. They are responsible for the synthesis of two major matrix components: amyloid-like fibers and an exopolysaccharide (Branda et al. 2006; Romero et al. 2011).


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Unknown signal Signal input

YwcC

Spo0A~ P

SlrA

sinl

abbA

SlrA

abrB

AbbA

Sinl

AbrB

SinR

SlrA

SlrR

SlrR SinR

eps

RemA hog

tapA

lytA bslA

DegU ~P lytF

Matrix genes ON DegS EpsE

Fig. 3.2 Regulatory network governing biofilm formation. Schematic diagram of the complex regulatory pathways that control gene transcription during growth as a biofilm. It includes boxes indicating proteins, open reading frames (ORFs), arrows indicate activation, and triangles show repression. Moreover indirect activation and repression, active gene transcription, translation, absence of gene transcription, transcriptional repressor and protein–protein interaction is shown. Here protein that is able to bind to DNA to activate transcription, flagellum with the curved arrow indicating rotation and the cross indicating inhibition of flagella rotation. Vertical rectangles labelled with “signal input” indicate sensor kinases for the Spo0A pathway

The two matrix operons are directly controlled by a repressor SinR (Chu et al. 2006). Derepression is triggered by SinI, an anti-repressor whose gene is activated by phosphorylated Spo0A (Spo0A~P) (Kearns et al. 2005; Chai et al. 2011). Spo0A~P has a major importance for biofilm formation which acts as a master regulatory protein. A network of kinases and phosphatases controls phosphorylation of Spo0A in

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response to various environmental signals (Ireton et al. 1993; Perego et al. 1994). Spo0A~P also represses the gene for AbrB, a repressor that contributes to repression of the matrix operons (Fig. 3.2). Under as yet poorly defined conditions, matrix gene expression is alternately turned on by a Spo0A~P-independent pathway consisting of TetR, a YwcC-type repressor, and SlrA, a paralogue of SinI whose gene is repressed by YwcC. SlrA contributes to biofilm formation by antagonizing SinR and thereby derepressing matrix genes.

3.8 Conclusion Biofilm biofertilizer (BFBF) is an eco-friendly and economical technology that could lead to a sustainable agriculture without hampering yields. The prospects that BFBF can be applied on a significant scale are greater than ever before. The main drivers for success will be the increasing price of chemical fertilizers and the need to minimize the production of greenhouse gases such as carbon dioxide and nitrous oxide. Achieving such an “evergreen revolution” will still be extremely challenging, but there are many indicators that it can now succeed. Similarly beneficial and pathogenic bacteria remain present in the rhizosphere to combat. It is the battlefield for microbes to either win their goal of plant growth promotion or affect the health of plant by inducing plant diseases. To fulfil the future demand of a growing population for food, healthy and high yielding plants are the requirement. Use of microbes in the form of biofertilizer for plant growth promotion and biocontrol activity is a hope for the food security issue. To combat with pathogenic microbes, the concept of biofilm formation by the PGPRs has great potential in it. They can communicate with each other by quorum sensing and can confuse the pathogenic bacteria. It is an ominous need to discover many more microorganisms with the capability of biofilm formation to participate in biocontrol activities and ensure the healthy life of plants and the nation. Moreover mechanism behind biofilm formation and its contribution in biocontrol should be addressed optimistically.

References Adam JL, McLean RJ (1999) Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol 65:4285–4287 Allen H, Dasgupta TS, Todd SP (2015a) Eccrine Sweat Duct Occlusion by Staphylococcal-Derived Biofilms: An Unexpected Signature Finding of Eczema in Dermatologic Diseases. J Clin Exp Dermatol Res. 6:310 Allen HB, Goyal K, Ogrich L (2015b) Biofilm formation by malassezia furfur/ovale as a possible mechanism of pathogenesis in Tinea versicolor. J Clin Exp Dermatol Res. 6:311 Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:43–350 Bloemberg GV, Lugtenberg BJJ (2004) Bacterial biofilms on plants: relevance and phenotypic aspects. In: Ghannoum M, O’Toole GA (eds) Microbial Biofilms. ASM Press, Washington, DC, pp 141–159


49

Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621–11626 Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol J 59:1229–1238 Chai Y, Norman T, Kolter R, Losick R (2011) Evidence that metabolism and chromosome copy number control mutually exclusive cell fates in Bacillus subtilis. Eur Mol Biol Org J 30:1402–1413 Chu F, Kearns DB, Branda SS, Kolter R, Losick R (2006) Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol Microbiol J 59:1216–1228 Das A, Prasad R, Srivastava A, Giang PH, Bhatnagar K, Varma A (2007) Fungal siderophores: structure, functions and regulations. In: Varma A, Chincholkar SB (eds) Microbial Siderophores, vol 12. Springer-Verlag, Berlin Heidelberg, pp 1–42 Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. MicrobiolMol Biol Rev 64:847–867 Davey ME, Caiazza NC, O’ Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa. J Bacteriol 185:1027–1036 de Weger LA, Bakker PAHM, Schippers B, van Loosdrecht MCM, Lugtenberg BJJ (1989) Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharide are affected in their ability to colonize potato roots. In: Lugtenberg B (ed) Signal Molecules in Plants and Plant-Microbe Interactions. Springer, Berlin, Heidelberg, NewYork Dekkers LC, van der Bij AJ, Mulders IHM, Phoelich CC, Wentwoord RAR, Glandorf DCM, Wijffelman CA, Lugtenberg BJJ (1998) Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and NADH: ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol Plant Microbe Interact 11:763–771 Donlan RM, Costerton JW (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193 Fard SS, Amin M, Khodaparast L et al (2015) Detection of biofilm phenotype of isolated Staphylococcus epidermidis from respiratory catheters of hospitalized patients and evaluation the effect of antibodies against SesC protein on biofilm formation. Clin Microbiol 4:221 Flemming HC, Wingender J, Mayer C, Korstgens V, Borchard W (2000) Cohesiveness in biofilm matrix polymers. In: Allison D, Gilbert P, Lappin-Scott HM, Wilson M (eds) Community Structure and Cooperation in Biofilms. SGM Symposium Series 59. Cambridge University Press, Cambridge, pp 87–105 Fletcher M (1996) Bacterial attachment in aquatic environments: a diversity of surfaces and adhesion strategies. In: Fletcher M (ed) Bacterial Adhesion: Molecular and Ecological Diversity. Wiley, New York, pp 1–24 Genevaux P, Bauda P, DuBo MS, Oudega B (1996) Identification of Tn10 insertions in the rfaG; rfaP and galU genes involved in lipopolysaccharide core biosynthesis that affects Escherichia coli adhesion. Arch Microbiol 172:1–8 Ghigo JM (2001) Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442–445 Gilbert P, Das J, Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160–167 Govan JRW, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574 Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol J 2:95–108 He X, Chang W, Pierce DL, Seib LO, Wagner J, Fuqua C (2003) Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J Bacteriol 185:809–822 Hirano SS, Upper CD (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 641:624–653 Ireton K, Rudner DZ, Siranosian KJ, Grossman AD (1993) Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev J 7:283–294

50

T. Parween et al.

Islam N, Ross JM, Marten MR (2015) Proteome analyses of Staphylococcus aureus biofilm at elevated levels of NaCl. Clin Microbiol 4:219 Kasim WA, Gaafar RM, Rania M, Abou A, Omar MN, Hewait HM (2016) Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley. Ann Agri Sci 61:217–227 Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol J 55:739–749 Kuiper I, Bloemberg GV, Lugtenberg BJ (2001) Selection of a plant–bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microb Interact 4:1197–1205 Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact Rev 7:6–15 Kulkarni M (2016) Biofilms: A policy of microbes to strengthen their viability. Microbiol. Int J 1(2):104 Laville J, Voisard C, Keel C, Maurhofer M, Defago G, Haas D (1992) Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root-rot of tobacco. Proc Natl Acad Sci USA 89:1562–1566 Lazazzera BA, Palmer T, Quisel J, Grossman AD (1999) Cell-density control of gene expression and development in Bacillus subtilis. In: Dunny GM, Winans SC (eds) Cell-Cell Signaling in Bacteria. American Society for Microbiology Press, Washington, DC, pp 27–47 Loera-Muro A, Ramírez-Castillo FY, Avelar-González FJ et al (2015) Biofilms in the Porcine Respiratory Disease Complex and Biofilms. J Bacteriol Parasitol 6:247 Maurer S, Fouchard P, Meyle E et al (2015) Activation of neutrophils by the extracellular polymeric substance of S. epidermidis biofilms is mediated by the bacterial heat shock protein Groel. J Biotechnol Biomater 5:176 Nyvad B, Kilian M (1990) Microflora associated with experimental root surface caries in humans. Infect Immun 58:1628–1633 O’Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: A genetic analysis. Mol Microbiol 28:449–461 O’Toole GA, Gibbs KA, Hager PW, Phibbs PV, Kolter R (2000) The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bacteriol 182:425–431 Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226 Parsek MR, Fuqua C (2004) Biofilms: Emerging themes and challenges in studies of surface- associated microbial life. Bacteriol J 186:4427–4440 Pearson JP, Pesci EC, Iglewski BH (1997) Roles of Pseudomonas aeruginosa las and rhl quorum- sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767 Perego M, Hanstein C, Welsh KM, Djavakhishvili T, Glaser P, Hoch JA (1994) Multiple protein- aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in Bacillus subtilis. Cell J 79:1047–1055 Pereira J, Tavares FP, Lima KC et al (2015) Relation between dental implant joint surfaces and biofilm formation. Dentistry 5:296 Piper KR, Beck von Bodman S, Farrand SK (1993) Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448–450 Prasad R, Kumar M, Varma A (2015) Role of PGPR in soil fertility and plant health. In: Egamberdieva D, Shrivastava S, Varma A (eds) Plant Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants. Springer International Publishing, Cham, pp 247–260 Pratt LA, Silhavy TJ (1995) Porin regulon of Escherichia coli. In: Hoch JA, Silhavy TJ (eds) Two- Component Signal Transduction. American Society for Microbiology Press, Washington, DC, pp 105–127


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Puga CH, Orgaz B, Muñoz S et al (2015) Cold stress and presence of pseudomonas fluorescens affect listeria monocytogenes biofilm structure and response to chitosan. J Mol Genet Med 9:180 Romero D, Vlamakis H, Losick R, Kolter R (2011) An accessory protein required for anchoring and assembly of amyloid fibres in Bacillus subtilis biofilms. Mol Microbiol J 80:1155–1168 Santos ALS, Mello TP, Ramos LS et al (2015) Biofilm: A robust and efficient barrier to antifungal chemotherapy. J Antimicro1 1:e101 Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280 Sonenshein AL (2000) Control of sporulation initiation in Bacillus subtilis. Curr Opin Microbiol 3:561–566 Stanley NR, Lazazzera BA (2004) Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol 52:917–924 Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210 Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Ann Rev Microbiol J 56:187–209 Venturi V (2003) Control of rpoS transcription in Escherichia coli and Pseudomonas aeruginosa: Why so different? Mol Microbiol 49:1–9 Webb JS, Givskov M, Kjelleberg S (2003) Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol J 6:578–585 Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864 Wise AA, Price CW (1995) Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor sigma B in response to environmental signals. J Bacteriol 177:123–133 Wolfaardt GM, Lawrence JR, Roberts RD, Caldwell DE (1998) In situ characterization of biofilm exopolymers involved in the accumulation of chlorinated organics. Microbial Ecol 35:213–223 Xu D, Gu T (2015) The war against problematic biofilms in the oil and gas industry. J Microb Biochem Technol. 7:124 Zhu J, Mekalanos JJ (2003) Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5:647–656

Chapter 4

Fungi: A Remedy to Eliminate Environmental Pollutants Sunita J. Varjani and Rajal K. Patel

4.1 Introduction Environmental pollution by various pollutants poses irresistible and irreparable deterioration of air, water, and soil. Major sources of pollutants are industrial effluents, mining activities, sewage sludge, inadequate use of fertilizers, pesticides, and insecticides, etc. (Peng et al. 2008; Bagul et al. 2015; Varjani 2017). All these pollutants can be divided into two major groups, (i) organic and (ii) inorganic, which can cause adverse effect on flora, fauna, and human health (Varjani et al. 2015). Moreover, some of toxic pollutants, viz., heavy metals, polyaromatic compounds, pesticides, and radionuclides, are non-biodegradable in nature which renders hazardous impact on humans and environment, globally (Berreck et al. 1992; Peng et al. 2008; Abdel-Shafy and Mansour 2016). Hence, there is need to develop treatments that can minimize or even eliminate such pollutants from environment (Varjani 2017). There are a number of physicochemical and biological processes that are commonly employed to remove pollutants from industrial wastewaters before their discharge in the environment (Fomina and Gadd 2014; Varjani and Upasani 2016). Bioremediation is the use of biological interventions of biodiversity for mitigation (and wherever possible, complete elimination) of the noxious effects caused by environmental pollutants in a given site (Peng et al. 2008; Varjani 2017). These technologies have become attractive alternatives to conventional cleanup technologies due to relatively low capital costs and their inherently aesthetic nature (Prasad 2011; Varjani et al. 2015). The aim of bioremediation is the application of S.J. Varjani (*) School of Biological Sciences and Biotechnology, Indian Institute of Advanced Research, Gandhinagar, Gujarat, India e-mail: [email protected] R.K. Patel Gujarat Ecological Education and Research, Foundation, Indroda Nature Park, Gandhinagar, Gujarat, India © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_4

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biosystems such as microbes and higher organisms like plants (phytoremediation) to reduce the potential toxicity of chemical contaminants in the environment by degrading, transforming, and immobilizing these undesirable compounds (Ezeonu et al. 2012; Peng et al. 2008; Varjani 2016). Fungi prove to have high potential in the degradation of high-molecular-weight compounds and therefore are used widely to remediate environmental pollution. With the adaptability of fungi, mycoremediation could be an alternate way to ensure good cleaning efficiency during the winter when necessary growth conditions for plant-based systems are lacking (Esterhuizen- Londt et al. 2016). Therefore, remediation with fungi can be suitable method to improve environment quality and sustainability. The purpose of this chapter is to provide knowledge about major environmental pollutants and use of fungi to treat these contaminants present in environment. The chapter also gives brief introduction to fungi and its classes.

4.2 Environmental Pollution Rapid urbanization and intensified industrialization all over the world have posed a major risk to the environment (Prasad 2011). Environment (French word Environ = surrounding) includes biotic components like plant, animals, microbes, etc. and abiotic components like air, water, soil, light, etc. (Goel 2006; Mullai 2012). Environmental pollution is defined as negative or undesirable change in environment, which has detrimental effect on it (Varjani 2017). Natural environment consists of four interlinking systems, namely, the atmosphere, the hydrosphere, the lithosphere, and the biosphere. These four systems are in constant change, and such changes are affected by human activities and vice versa (Mullai 2012). Figure 4.1 shows the three major kinds of pollution that occur in the environment.

Fig. 4.1 Types of environmental pollution

Air Pollution

Environmental Pollution Water Pollution

Soil pollution

4 Fungi: A Remedy to Eliminate Environmental Pollutants

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Environmental pollution is classified in various groups. For instance, pollution of air is termed as atmospheric pollution; the pollution of hydrosphere or water is termed as water pollution. Pollution due to disposal of wastewater is termed as industrial effluent pollution. Similarly, indiscriminate dispersal of domestic sewage is called domestic effluent pollution. In addition to these, pollution of lithosphere or land is called soil pollution. For instance, pesticide residue contributes toward soil pollution. Urban areas are blessed with the menace of noise, which at times becomes intolerable and is called noise pollution (Khopkar 2005).

4.2.1 Major Environmental Pollutants Pollutants are difficult to concisely define. They exist in several forms including solids, liquids, vapors, gases, ions, and mixtures of these primary states of matter. Pollutants may persist in environment for a short time (e.g., short-lived reactive chemical species with lifetime less than 1 s) or for several years (e.g., very small particles and nonreactive gases). Tables 4.1, 4.2, and 4.3 give a detailed account of major air, water, and soil pollutants, their sources, and effects.

4.3 Classification of Fungi Fungus is a large group of organisms that includes yeasts and molds as well as more familiar mushrooms. These organisms are classified as a kingdom, Fungi, which is separate from plants, animals, protists, and bacteria. Figure 4.2 describes the four major classes of fungi. Fungi are not able to ingest their food like animals do, nor can they manufacture their own food, the way plants do. Instead, fungi feed by absorption of nutrients from environment around them. They accomplish this by growing through and within substrate on which they are feeding. The hyphae secrete digestive enzymes which break down substrate, making it easier for fungus to absorb nutrients which substrate contains. With the growth of industry, there has been a considerable increase in discharge of industrial waste to environment, chiefly soil and water, which has led to accumulation of heavy metals, especially in urban areas (Dixit et al. 2015).

4.3.1 Ascomycetes This phylum contains a large number of species. They commonly develop by sexual reproduction, but asexual reproduction is also common. The spores of these fungi formed inside the saclike structure called an ascus. The cells of ascomycete hyphae may contain many nuclei with septate hyphae, e.g., morels (Morchella sp.) (Ravan and Johnson 2002).

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Table 4.1 Types of air pollutants, their sources, and effects (According to Flagan and Seinfeld 1988; Sivasakthivel and Reddy 2011) Sr. no. 1

Pollutant Carbon monoxide (CO)

Sources Cars, trucks, buses, small engines, and some industrial processes are major sources Wood stoves, cigarette smoke, and forest fires

2

Nitrogen oxides (NOx)

Burning fuels in motor vehicles, power plants, and industries Residential sources that burn fuels

3

Sulfur dioxide (SO2)

4

Volatile organic compounds Particulate matter (PM)

Burning fossil fuels (gasoline, oil, natural gas) Released from petroleum refineries, paper mills, chemical, and coal burning power plants Emitted as gases (fumes) through burning fuels, cleaning supplies, paints, and solvents Some particles are directly emitted from cars, trucks, buses, factories, construction sites, tilled fields, unpaved roads, and burning wood Other particles are indirectly formed when gases from burning fuels react with sunlight and water vapor Metal processing with the highest levels of lead generally found near land smelters Other sources include waste incinerators, utilities, and lead acid battery manufacturers No primary sources Formed as a secondary pollutant from atmospheric reactions involving hydrocarbons and oxides of nitrogen

5

6

Lead

7

Ozone (O3)

Effects Interferes with the blood’s ability to carry oxygen, slowing reflexes, and causing drowsiness Headaches and stress on heart In high concentrations, CO can cause death Make the body vulnerable to respiratory infections, lung disease, and possibly cancer It contributes to brownish haze seen over congested areas and to acid rain Easily dissolves in water and forms acids which can cause metal corrosion and fading/ deterioration of fabrics It easily dissolves in water and forms an acid which contributes to acid rain Lakes, forests, metals, and stone can be damaged by acid rain Smog formation and can cause serious health problems They may also harm plants Reduces visibility and causes variety of respiratory problems Particulate matter has also been linked to cancer It can also corrode metal; erode building and sculptures and soil fabrics Cause organ and neurological damage in humans and animals Lead can also slow down growth rate in plants

Major constituent of photochemical smog Highly phytotoxic Irritate lung airways and cause wheezing and coughing Repeated exposure can cause permanent lung damage


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Table 4.2 Types of water pollutants, their sources, and effects (According to Goel 2006; Bagul et al. 2015) Sr. no. 1

2

3

4

Pollutant Pathogens

Organic pollutants Oil and grease Pesticides/ weedicides Plastics Detergents Inorganic pollutants Fertilizers (phosphates and nitrates) Acids and alkalis Radioactive materials

5

Heat

6

Sediments

Sources of pollutants Sewage, human and animal wastes, natural and urban runoff from land and industrial waste, etc. Automobile and machine waste, tanker spills, offshore oil leakage Chemicals used for better yield from agriculture, industrial, and household waste Agricultural runoff Mine drainage, industrial waste, natural and urban runoff

Natural sources, uranium mining and processing, hospitals and research laboratory using radioisotopes Cooling water for industrial, nuclear, and thermal plants Natural erosion, runoff from agricultural land and construction sites

Effects and significance Depletion of dissolved oxygen in water (foul odor), health effects (outbreaks of waterborne diseases) Disruption of marine life, aesthetic damage Toxic effects (harmful for aquatic life) Possible genetic defects and cancer Fish kill, eutrophication aesthetics Algal bloom and eutrophication, cause methemoglobinemia Kill freshwater organisms, unfit for drinking, irrigation, and industrial use Cancer and genetic defects

Decreases solubility of oxygen in water, disrupts aquatic ecosystem Affects water quality, reduces fish population

4.3.2 Zygomycetes The zygomycetes (phylum Zygomycota) lack septa in their hyphae except when they form sporangia or gametangia. They are mostly microscopic in nature. This kind of fungi developed sexually as well as asexually. They are multinucleate and lack septa. Asexual reproduction occurs more frequently than sexual reproduction, e.g., Rhizopus (black bread mold) (Ravan and Johnson 2002).

4.3.3 Basidiomycetes All members of the Basidiomycota produce their spores on a characteristic cell called basidium and reproduce by sexual means. Asexual reproduction occurs occasionally. A basidiomycete mycelium made up of monokaryotic hyphae is called primary mycelium, e.g., Agaricus (mushroom) (Ravan and Johnson 2002).

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Table 4.3 Types of soil pollutants, their sources, and effects (According to Ashraf et al. 2014) Sr. no. 1

Pollutant Chemicals, radioactive material, toxic gases

Sources of pollutants Industrial effluent and emission of gases from stack gas

2

Heavy metals

3

Sewage and sewage sludge

4

Pesticides

Industrial effluent, mine washing, fungicides, insecticides Uncontrolled disposal of sewage and other liquid water Agricultural effluent from animal husbandry Drainage of irrigation water and urban runoff Agricultural use

Effects and significance Pollution of underground water by seepage Ecological imbalance Releases toxic gases which harms flora and fauna Radioactive waste causes health problem, increased salinity Toxic to plants, find specific adsorption site in soil, great affinity with organic matter which form stable complexes thereby leading to reduced nutrient content Changes in soil leaching pattern, changes in humus content and porosity Chemical changes: soil reaction, base exchange status, salinity quantity, and availability of nutrients

Affects plant growth Accumulation in higher concentration are toxic Aromatic organic compounds have long persistence time in soil causing soil toxicity

Eumycotina (Fungi)

Ascomycetes (Sac fungi)

Zygomycetes (Zygot forming fungi)

Basidiomycetes (Club fungi)

Deuteromycetes (Imperfect fungi)

Fig. 4.2 Fungal classification

4.3.4 Deuteromycetes Members of this family do not reproduce sexually. Most are thought to be derived from Ascomycota. A well-known penicillin antibiotic is derived from genera Penicillium of this phylum. A number of imperfect fungi occur widely on food. Fusarium species growing on spoiled food produce highly toxic substances such as trichothecenes, e.g., Penicillium and Aspergillus (Ravan and Johnson 2002).


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Apart from this, fungi form two key mutualistic symbiotic associations, viz., lichen and mycorrhizae. Mycorrhizae are used to remediate different environmental pollutants from soil as they have association with plant roots (Ravan and Johnson 2002).

4.4 Bioremediation “Remediate” means to solve a problem, and “bioremediate” environment means to use biological systems to solve an environmental problem such as contaminated soil or groundwater (Chibuike 2013). Bioremediation is the use of living microorganisms/plants to degrade environmental pollutants or to prevent pollution (Barr and Aust 1994; Varjani 2017). In other words, it is a technology for removing pollutants from the environment, thus restoring original natural surroundings and preventing further pollution (Thakur 2014). The goal of bioremediation is employment of biosystems such as microbes and higher organisms like plants (phytoremediation) and animals to reduce potential toxicity of chemical contaminants in environment by degrading, transforming, and immobilizing these undesirable compounds (Sasikumar and Papinazath 2003).

4.5 Mycoremediation Mycoremediation is the use of fungi to degrade or remediate pollutants (Esterhuizen-Londt et al. 2016). A wide array of materials can be degraded or deteriorated by fungi, and extensive research on mycoremediation shows that it represents a clean method to treat soil and water without formation of metabolites which are dangerous to the environment and human health. Fungi have been recognized to degrade various compounds/materials (Berreck et al. 1992; Gaikwad and Sonawane 2012; Abdel-Shafy and Mansour 2016). Polyethylene, with a molecular weight of 4000–28,000, is bioremediated by cultivation of Penicillium simplicissimum YK (Yamada-Onodera et al. 2001). Saccharomyces cerevisiae was used for removal of heavy metals like lead and cadmium from contaminated soil and revealed 65–79% biosorption of heavy metals within 30 days (Damodaran et al. 2011). Mucor hiemalis was shown to be an effective fungus for b ioremediation of pharmaceutical xenobiotics, e.g., acetaminophen (Esterhuizen-Londt et al. 2016). Fungi are also useful in bioremediation of hydrocarbon pollutants (Norton 2012; Varjani 2017). Mycorrhiza- assisted remediation not only ensures the removal of soil pollutants but also improves the structure of soil and helps in plant nutrient acquisition. Mycorrhizal fungi also detoxify the organic and inorganic toxic substances (Chibuike 2013). Ulfig et al. (2006) reviewed the ability of keratinolytic fungi to remove hydrocarbons from different media. Fungi are especially well suited to PAH degradation relative to other bacterial decomposers (Peng et al. 2008).

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4.5.1 Fungi: An Environmental Indicator Fungi are useful to indicate various types of environmental contaminants; however, they are unable to map the pollution. Thelephora caryophyllea accumulates metals in the soil (Maurice and Lagerkvist 2000). The pathogenic and allergic spores of Aspergillus, Rhizopus, and Alternaria are indicative of air pollution (Gaikwad and Sonwane 2012). The ectotrophic symbiosis, i.e., mycorrhiza-forming fungi and mycorrhizal roots, is highly responsive to air pollution and can be used as bioindicators (Fellner 1990). Yeasts are used in various tests for determination of mutagenic or carcinogenic action. Due to limited permeability, yeast cells exhibit lower sensitivity to mutagens or carcinogens than do bacteria. The general permeability of Saccharomyces cerevisiae cells can be enhanced by mutation, and on this basis, a more sensitive test has been developed to study environmental pollution (Terziyska et al. 2000). Recent advances in knowledge of multicolored fluorescent proteins from yeasts and fungi have opened a door regarding the sensing systems used for environmental pollutants (Singh 2006).

4.5.2 Fungi: Remediation of Pollutants In any ecosystem, fungi are among the major decomposers of plant polymers such as cellulose, hemicellulose, and lignin (Pletsch et al. 1999; Christian et al. 2005). With the adaptability of fungi, mycoremediation could be an alternate way to ensure greater cleaning efficiency during the winter when the necessary growth conditions for plant-based systems are lacking (Steffen et al. 2007). Remediation using fungi, especially mycoremediation of soils, has been demonstrated in several cases (Shah et al. 1992; Yamada-Onodera et al. 2001; Hamman 2004; Siddiquee et al. 2015; Esterhuizen-Londt et al. 2016). Fungi have proven to modify soil permeability and ion exchange capacity and detoxify contaminated soil. Edible and/or medicinal fungi also play a role as natural environmental r emediators (Pletsch et al. 1999), as do aquatic fungi (Kshirsagar 2013). Fungi are usually slow in growth and often require substrates for co-metabolism. The mycelial growth habit of these organisms is responsible for rapid colonization of substrates (Siddiquee et al. 2015). Myco-transformation is a term used to describe biotransformation of pollutants in simpler molecules by using fungi. Brown rot and white rot are categories of fungi that produce different suites of digestive enzymes that have each shown potential for mycoremediation (Shah et al. 1992; YamadaOnodera et al. 2001; Christian et al. 2005; Kshirsagar 2013). It has been proposed that fungi might be deployed in biodegradation of sites that are polluted by complex mixtures of PAH, for example, from creosote, coal tar, and crude oil (Adenipekun and Lawal 2012).


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4.5.3 R ole of White-Rot and Brown-Rot Fungi in Bioremediation White-rot fungi produce digestive enzymes that preferentially degrade lignin, a component of wood that is broadly similar in molecular structure to petroleum hydrocarbons (Shah et al. 1992; Kshirsagar 2013; Varjani 2017). Bumpus et al. (1985) proposed the use of this fungus in bioremediation as Phanerochaete chrysosporium have extracellular oxidative ligninolytic enzymes that have the ability to degrade toxic or insoluble compounds more efficiently than other fungi or microorganisms. In addition to P. chrysosporium, several other white-rot fungi (e.g., Pleurotus ostreatus, Trametes versicolor, Bjerkandera adusta, Lentinula edodes, Irpex lacteus) are known to degrade these compounds (Bumpus et al. 1985; Shah et al. 1992; Hamman 2004; Adenipekun and Lawal 2012; Siddiquee et al. 2015). It has been estimated that approximately 30% of the literature on fungal bioremediation is concerned with white-rot fungi (Singh 2006; Rhodes 2014). As stated by Christian et al. (2005), white-rot fungi secrete enzymes such as lignin peroxidases, manganese peroxidases, and laccases, and they are able to mineralize a wide range of highly recalcitrant organo-pollutants that are similar in structure to lignin. As white-rot fungi grow by hyphal extension, they can reach pollutants in soil easily than other organisms. Soils may also be decontaminated from crude oil, with requirement that lignocellulosic substrates (e.g., sawdust straw and corncob) are also provided, to support growth of fungal species in soil (Lang et al. 1995). Brown- rot fungi degrade cellulose in the cell wall, leaving lignin as a typically brownish deposit. Wetzstein et al. (1997) have reported degradation of enrofloxacin (a fluoroquinolone antibacterial drug) used in veterinary medicine using brown-rot fungus named Gloeophyllum striatum.

4.5.4 Techniques Used in Mycoremediation Lamar and White (2001) advocated a four-phase strategy for implementation of mycoremediation. This includes (i) bench-scale treatability, (ii) on-site pilot testing, (iii) production of inoculums, and (iv) full-scale application. Substrates such as wood chips, wheat straw, peat, corncobs, sawdust, a nutrient- fortified mixture of grain and sawdust, bark, rice, annual plant stems and wood, fish oil, alfalfa, spent mushroom compost, sugarcane bagasse, coffee pulp, sugar beet pulp, okra, canola meal, cyclodextrins, and surfactants can be used in inoculum production both off-site or on-site or as mixed with contaminated soils to improve the processes of degradation (Singh 2006; Rhodes 2014). It is critical to attain the correct nitrogen/carbon ratio in substrates used so to avoid any impeding effect on efficiency of fungi in bioremediation process. Fungal inocula coated with alginate, gelatin, agarose, carrageenan, chitosan, etc., in form of pellets, may offer a better outcome than with inocula produced using bulk substrates (Rhodes 2014).

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4.5.4.1 Mycofiltration The idea of mycofiltration was germinated in the year 1970 by Paul Stamets during his study at Evergreen State College, Olympia, Washington. He found that fungi with their threadlike mycelium have the capability of absorbing tobacco smoke, ink, and water. The garden giant mushrooms were also used in mycofiltration to clean up the flow of fecal coliform-contaminated water (Stamets 2011). In mycofiltration, the mycelia are used as a filter to remove toxic materials and microorganisms from water in soil. This ecologically rational biotechnology is a promising technique for enhancing the management of storm water and agricultural runoff. The approach of adding cultivated fungi to surface water management practices was invented by Stamets in the late 1980s (Stamets 2005). A mycofilter is basically a hessian sack filled with wet straw, wood chip, and mycelium (non-fruiting part of fungi). They look like slightly moldy sandbags and do the important work of cleaning. Likewise mycofiltration is also used to remove E. coli from storm water and results highlight challenges of using traditional microbial indicator methods, such as enzyme-linked chromogenic media, to assess capacity for eco-technologies like mycofiltration to remove pathogens from polluted waters (Taylor et al. 2015). Some species of mushroom are also known to act as mycofilters and remove toxins from polluted waters. Figure 4.3 describes steps for preparation of mycofilters used in contaminated river/streams.

1.

2.

3 4.

• Preperation of material • 2a: Building of mycofilters- Material needed: Straw, wood chip, hessian sacks, mycellium spawn, plentiful supply of fresh water • 2b: Work in pair- One to hold the bag open and the other to scoop in the material. • 2c: Layers of material: i) good layer of wet straw, ii) a scoop or two of wood chip, iii) generous sprinkling of mycelium was added and the layering process repeated, until bags were tightly packed and full • Put the finished sacks into rubble bags to protect them • Put them in garden for the development of mycelium for few weeks • Installation: Install the sacks by sream/ river/contaminated sites

Fig. 4.3 Illustration of the steps involved in preparation of mycofilter


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4.5.5 Fungi and PAHs (Polyaromatic Hydrocarbons) PAHs are building blocks of life and they are very common on planet earth. However, accumulation and chemical alteration of these PAHs are following a pattern now dominated by actions of humans (Fernandez-Luqueño et al. 2011; Norton 2012). PAHs form when carbon materials are burned incompletely. Furthermore, large amounts of PAHs are extracted, refined, and transported which contaminate environment. Major anthropogenic sources of PAHs include residential heating, coal gasification and liquefying plants, carbon black, coal-tar pitch and asphalt production, coke and aluminum production, catalytic cracking towers, and related activities in petroleum refineries and motor vehicle exhaust (Peng et al. 2008; Fernandez-Luqueño et al. 2011; Abdel-Shafy and Mansour 2016). Because of hydrophobic nature of PAHs, they can easily accumulate in fatty tissue and spread throughout the food chain (Christian et al. 2005; Fernandez-Luqueño et al. 2011; Varjani 2017). Most harmful among PAHs are those with more than four rings; they are often mutagenic and carcinogenic which emphasizes the importance of their removal from environment (Steffen et al. 2007; Varjani et al. 2015). Biodegradation of PAHs has been studied for more than 20 years, and already in the 1980s, a basidiomycete, the white-rot fungus Phanerochaete chrysosporium, was shown to be capable of degrading PAHs (Steffen et al. 2007). Fungi can degrade high-molecular-weight PAHs when compared to bacteria which can degrade relatively smaller molecules, and therefore they are well suited to PAH degradation (Peng et al. 2008). They also function well in nonaqueous environments where hydrophobic PAHs accumulate; a majority of other microbial degradation occurs in aqueous phase. Also, they can function in very low-oxygen conditions that occur in heavily PAH-contaminated zones (Fernandez-Luqueño et al. 2011). There are more than 50 fungal species or groups that can degrade various PAHs effectively as reviewed by Fernandez-Luqueño et al. (2011). A wide variety of fungi have evolved effective mechanisms to attack specific PAHs (AbdelShafy and Mansour 2016). One reason for this ability lies in the similarity between lignin, a long aromatic family of molecules that is present in wood, and PAHs (McCrady 1991; Shah et al. 1992; Kshirsagar 2013). Lignin is found in all vascular plants, mostly between cells but also within the cells and in the cell walls. It makes vegetables firm and crunchy (McCrady 1991; Shah et al. 1992). It functions to regulate the transport of liquid in living plants, and it enables trees to grow taller and compete for sunshine. It is very resistant to degradation being held together with strong chemical bonds; it also appears to have a lot of internal H bonds. It is bonded in complex and various ways to carbohydrates (hemicelluloses) in wood (McCrady 1991). White-rot fungi are well known for their ability to ultimately transform lignin to CO2 in nature through a process called mineralization; fungi are equipped with certain extracellular enzymes, such as phenol oxidases (laccase) and peroxidases, which are capable of oxidizing lignin and other compounds through a formal abstraction of one electron (Mai et al. 2004; Varjani 2016).

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Steffen et al. (2007) have reported that oyster mushroom, Pleurotus ostreatus, can degrade 80–95% of all PAHs present in soil. Many species of white-rot fungi have been studied extensively and are ubiquitous PAH degraders. Two main pathways are identified for these basidiomycetes; first is the cyctochrome 450 system, much like the system in mammal livers that break down large molecules into metabolites; however, many of these metabolites are toxic themselves. The second one, i.e., lignin extracellular degradation pathway, is preferable because the metabolites are fully broken down into carbon dioxide. A mixture of bacteria and white-rot fungi could complete the degradation of PAH most effectively as the fungi break down the largest molecules of PAHs into low-molecular-weight compound and bacteria can then act on those molecules (Peng et al. 2008). Fungi can degrade polyvinyl alcohol (PVA) as well. According to research work carried out by Jecu et al. (2010), Aspergillus niger can substantially degrade the PVA, starch, and glycerol. They examined degradation under scanning electron microscope and observed significant changes in polymer surface aspects depending on medium culture composition, the presence of supplementary carbon source facilitating microbial growth and degradation process. There is a scope for the use of fungi in decomposing in situ intractable, persistent, and highly toxic pollutants, including TNT (2,4,6-trinitrotoluene) (Stamets 2005). By inoculating a plot of soil contaminated using diesel oil, with mycelia from oyster mushrooms (Pleurotus ostreatus), it was found that after 4 weeks, 95% PAHs had been converted to nontoxic compounds. It seems that the naturally present community of microbes acts in concert with fungi to decompose contaminants, finally to CO2 and H2O (Rhodes 2014). Fungi have an astonishing potential to clean up contaminated environments.

4.6 Conclusion Fungi are efficient in degradation of high-molecular-weight compound into simpler compound via enzyme activity. The research in this field has shown that there is a fungus to degrade every type of environmental pollutant. Mycoremediation has ability to transform contaminated wasteland into a diversified ecosystem. However, application of this technology is difficult; skilled and trained personnel with proper knowledge of the subject are required to do the work of fungal remedy. Furthermore, there is a need to carry out research on potentiality of mushroom and also to exploit other species of fungi for degradation of pollutants. Acknowledgment We express our sincere gratitude to academic and administrative staff of the University and Institute of Advanced Research for their kind support.


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References Abdel-Shafy HI, Mansour MS (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25(1):107–123 Adenipekun CO, Lawal R (2012) Uses of mushrooms in bioremediation: a review. Biotechnol Mol Biol Rev 7:62–68 Ashraf MA, Maah MJ, Yusoff I, Hernandez-Soriano M (2014) Soil contamination, risk assessment and remediation. Environmental risk assessment of soil contamination. Intech, Rijeka Bagul VR, Shinde DN, Chavan RP, Patil CL (2015) Causes and impacts of water pollution on rivers in Maharashtra: a review. Res J Chem Environ Sci 3:1–4 Barr DP, Aust SD (1994) Pollutant degradation by white rot fungi. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 49–72 Berreck M, Ohenoja E, Haselwandter K (1992) Mycorrhizal fungi as bioindicators of radioactivity. In: Teller A, Mathy P, Jeffers JNR (eds) Responses of forest ecosystems to environmental changes. Springer, Dordrecht, pp 800–802 Bumpus JA, Tien M, Wright D, Aust SD (1985) Oxidation of persistent environmental pollutants by a white rot fungus. Science 228:1434–1436 Chibuike GU (2013) Use of mycorrhiza in soil remediation: a review. Sci Res Essays 8:679–1687 Christian V, Shrivastava R, Shukla D, Modi HA, Vyas BRM (2005) Degradation of xenobiotic compounds by lignin-degrading white-rot fungi: enzymology and mechanisms involved. Indian J Exp Biol 43:301–302 Damodaran D, Suresh G, Mohan R (2011) Bioremediation of soil by removing heavy metals using Saccharomyces cerevisiae. In: 2nd international conference on environmental science and technology, IPCBEE, vol. 6 Dixit R, Deepti M, Kuppusamy P, Singh UB, Sahu A, Shukla R, Singh BP et al (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212 Esterhuizen-Londt M, Schwartz K, Pflugmacher S (2016) Using aquatic fungi for pharmaceutical bioremediation: uptake of acetaminophen by Mucor hiemalis does not result in an enzymatic oxidative stress response. Fungal Biol 120:1249–1257 Ezeonu CS, Tagbo R, Anike EN, Oje OA, Onwurah IN (2012) Biotechnological tools for environmental sustainability: prospects and challenges for environments in Nigeria-a standard review. Biotechnol Res Int 2012:1–26 Fellner R (1990) Mycorrhiza-forming fungi as bioindicators of air pollution. Agric Ecosyst Environ 28:115–120 Fernandez-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez-Suárez C, Vázquez-Núñez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil- possibilities and challenges: a review. Environ Sci Pollut Res 18:12–30 Flagan RC, Seinfeld JH (eds) (1988) Fundamentals of air pollution engineering, Prentice-Hall, Inc., Englewood Cliffs, New Jersey Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14 Gaikwad K, Sonawane M (2012) Fungi as bio-indicators of air quality. Int J Life Sci Pharma Res 2:25–28 Goel PK (ed) (2006) Water pollution: causes, effects and control. New Age International, New Delhi, India Hamman S (2004) Bioremediation capabilities of white rot fungi. Biodegradation 52(16):11 Jecu L, Gheorghe A, Rosu A, Raut I, Grosu E, Ghiurea M (2010) Ability of fungal strains to degrade PVA based materials. J Polym Environ 18(3):284–290 Khopkar SM (2005) Environmental pollution monitoring and control. New Age International Pvt Ltd Publishers, New Delhi, India Kshirsagar AD (2013) Application of bioremediation process for wastewater treatment using aquatic fungi. Int J Curr Res 7:1737–1739

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Lamar RT, White RB (2001) Mycoremediation- commercial status and recent developments. In: 6th international in situ and on site bioremediation symposium, pp 263–278 Lang E, E’Uer G, Kleeberg I, Martens R, Zadrazil F (1995) Interaction of white rot fungi and soil microorganisms leading to biodegradation of soil pollutants. In: Contaminated soil’95. Springer, Dordrecht, pp 1277–1278 Mai C, Schormann W, Majcherczyk A, Hüttermann A (2004) Degradation of acrylic copolymers by white-rot fungi. Appl Microbiol Biotechnol 65:479–487 Maurice C, Lagerkvist A (2000) Using Betula pendula and Telephora caryophyllea for soil pollution assessment. J Soil Con 9:31–50 McCrady E (1991) The nature of lignin. At http://cool.conservation-us.org/byorg/abbey/ap/ap04/ ap04–4/. Last accessed 9 Jan 2017 Mullai MMJ (2012) Urbanization and its impact on environment in Pudukkottai. Ph.D. thesis, Tamilnadu, India Norton JM (2012) Fungi for bioremediation of hydrocarbon pollutants, vol 10. University of Hawai‘i at Hilo, Hawai‘i Community College, Hilo, pp 18–21. Last accessed 2 Jan 2017 Peng R, Ai-Sheng X, Yong X, Xiao-Yan F, Feng G, Wei Z, Yong-Sheng T, Quan-Hong Y (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955 Pletsch M, de Araujo BS, Charlwood BV (1999) Novel biotechnological approaches in environmental remediation research. Biotechnol Adv 17:679–687 Prasad MNV (2011) A state-of-the-art report on bioremediation, its applications to contaminated sites in India. Ministry of Environment & Forests, Government of India, New Delhi Raven PH, Johnson GB (eds) (2002) Biology, 6th edn. McGraw-Hill, Boston, pp 719–732 Rhodes CJ (2014) Mycoremediation (bioremediation with fungi)–growing mushrooms to clean the earth. Chem Spec Bioavailab 26(3):196–198 Sasikumar CS, Papinazath T (2003) Environmental management: bioremediation of polluted environment. In: Martin J, Madha Suresh BV, Vasantha Kumaran T (eds) Proceedings of the third international conference on environment and health, of Madras and Faculty of Environmental Studies, York University, pp 465–469 Shah MM, Barr DP, Chung N, Aust SD (1992) Use of white rot fungi in the degradation of environmental chemicals. Toxicol Lett 64:493–501 Siddiquee S, Rovina K, Al Azad S, Naher L, Suryani S, Chaikaew P (2015) Heavy metal contaminants removal from wastewater using the potential filamentous fungi biomass: a review. J Microb Biochem Technol 7:384–393. https://doi.org/10.4172/1948-5948.1000243 Singh H (2006) Mycoremediation: fungal bioremediation. Wiley, London Sivasakthivel T, Reddy SKK (2011) Ozone layer depletion and its effects: a review. Int J Environ Sci Develop 2:30–37 Stamets P (2005) Mycelium running: how mushrooms can help save the world. Random House Digital Inc, Berkeley Stamets P (2011) Growing gourmet and medicinal mushrooms. Ten Speed Press, Berkeley Steffen KT, Schubert S, Tuomela M, Hatakka A, Hofrichter M (2007) Enhancement of bioconversion of high-molecular mass polycyclic aromatic hydrocarbons in contaminated non-sterile soil by litter-decomposing fungi. Biodegradation 18(3):359–369 Taylor A, Flatt A, Beutel M, Wolff M, Brownson K, Stamets P (2015) Removal of Escherichia coli from synthetic storm water using mycofiltration. Ecol Eng 78:79–86 Terziyska A, Waltschewa L, Venkov P (2000) A new sensitive test based on yeast cells for studying environmental pollution. Environ Pollut 109(1):43–52 Thakur M (2014) Mycoremediation-a potential tool to control soil pollution. Asian J Environ Sci 9(1):24–31 Ulfig K, Przystas W, Plaza G, Miksch K (2006) Biodegradation of petroleum hydrocarbons by keratinolytic fungi. In: Soil and water pollution monitoring, protection and remediation. Springer, Dordrecht, pp 553–564 Varjani SJ, Upasani VN (2016) Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM 5514. Bioresour Technol 222:195–201


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Varjani SJ (2016) Microbial laccases and nanobiotechnology: environmental perspective. In: Prasad R (ed) Advances and applications through fungal nanobiotechnology. Springer International Publishing, Cham, pp 253–264 Varjani SJ, Rana DP, Jain AK, Bateja S, Upasani VN (2015) Synergistic exsitu biodegradation of crude oil by halotolerant bacterial consortium of indigenous strains isolated from on shore sites of Gujarat, India. Int Biodeterior Biodegrad 103:116–124 Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286 Wetzstein HG, Schmeer N, Karl W (1997) Degradation of the fluoroquinolone enrofloxacin by the brown rot fungus Gloeophyllum striatum: identification of metabolites. Appl Environ Microbiol 63(11):4272–4281 Yamada-Onodera K, Mukumoto H, Katsuyaya Y, Saiganji A, Tani Y (2001) Degradation of polyethylene by a fungus, Penicillium simplicissimum YK. Polym Degrad Stab 72(2):323–327

Chapter 5

Mycoremediation: Decolourization Potential of Fungal Ligninolytic Enzymes Hesham A. El Enshasy, Siti Zulaiha Hanapi, Soad A. Abdelgalil, Roslinda Abd Malek, and Avnish Pareek

5.1 Introduction The progress in industrialization and urbanization in order to fulfil the rapid growth of human population and living standard has led to advance technology associated with environmental pollution. One of these is the modernization and growth of textile production. Textile industry is diverse, heterogeneous and characterized by high consumption of water, fuel and chemicals. It has been recently reported that there are more than 100,000 different types of dyes available commercially (Daassi et al. 2014). On top of the textile, dyes are also widely consumed in paper and pulp industries, pharmaceutical, tannery and many other industries. It is estimated that the global textile mills including yarn and fabric market value forecast are currently worth about 800 million USD in 2015 (Lu 2016). The other side of these industries showed that textile’s effluent contributed to 17–20% of freshwater pollution which are mostly nondegradable (Gupta et al. 2015). This untreated dye effluent created H.A. El Enshasy (*) Faculty of Chemical Engineering and Energy, Universiti Teknologi Malaysia, Johor Bahru, Malaysia Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia City of Scientific Research and Technological Applications, Alexandria, Egypt e-mail: [email protected] S.Z. Hanapi • R.A. Malek Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia S.A. Abdelgalil Institute of Bioproduct Development, Universiti Teknologi Malaysia, Johor Bahru, Malaysia City of Scientific Research and Technological Applications, Alexandria, Egypt A. Pareek Department of Applied Biotechnology, College of Applied Sciences, Ministry of Higher Education, Sur, Sultanate of Oman © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_5

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enormous environmental threat by releasing the remaining dye chemicals into the receiving water bodies which are toxic to human, plant, animal and other components of ecosystem (Ayed et al. 2011). In addition, these dye-rich and toxic wastewater effluents should be treated properly and removed. The remediation of colour from textile wastewater has been reviewed recently (Gupta et al. 2015; Singh et al. 2015). Several chemical and physical approaches have been used widely. However, current technologies encountered its own challenges, and some also show ineffective results to decolourize and remove colour from the wastewater effluent (Saxena et al. 2017). Some organic colours used in the dyeing process represent high chemical and photolytic stability which is not easily to be degraded by conventional effluent treatment (Carmen and Daniela 2012). Therefore, major dyes from this group are considered as high potential pollutants (Suteu et al. 2011). For the past few years, biological treatment of wastewater using different biological systems raises the attention due to their relative cost-effectiveness and environmentally friendly practices (Ghaly et al. 2014). The application of microorganisms especially fungi presented remarkable removal of dyes in wastewater plant and great reduction in their toxicity level. White-rot fungi of moderate ligninolytic enzyme activity became a model of bioremediation with most of the research done up to now (Parmar et al. 2015). However, application in large-scale wastewater treatment plants using variety of microbial and enzymatic methods is still facing many challenges before it would be considered as an outstanding industrial-scale enzyme-mediated dye removal (Imran et al. 2015). Therefore, this review provides comprehensive information on the environmental impact of textile dyes and outlines the key current techniques applied in bioremediation of these compounds. The environmental compatibility, versatility, energy efficiency, safety and cost-effectiveness in removing dyes from wastewater bodies will be also highlighted. The growing field of mycoremediation in detoxifying wastewater using white-rot fungi is discussed in details particularly in factor effecting the cell growth, enzyme productivity and methods of enhancement of dye removal.

5.2 Classification of Dyes The textile dyes are mainly classified in two practical ways based on their chemical structure and application characteristics according to the colour index (C.I.). This colour index is published by the Society of Dyers and Colourists (United Kingdom) in cooperation with the American Association of Textile Chemists and Colourists (AATC). Under this category, each dye is represented in two numbers referring to the basis of colouristic and chemical classification. A colouristic generic name or C.I. generic name for dyes includes acid, basic, direct, disperse, mordant, reactive, sulphur dye, pigment, vat and azo insoluble, while using chemical based, the C.I. constitution number is presented via nitro, azo, carotenoid, diphenylmethane, xanthene, acridine, quinoline, indamine, sulphur, amino- and hydroxy ketone, anthraquinone, indigoid, phthalocyanine and inorganic pigment. Besides, dyes also have

5 Mycoremediation: Decolourization Potential of Fungal Ligninolytic Enzymes

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been classified based on its source of materials, nature of respective chromophores and methods of application. Table 5.1 summarizes dye classification and characteristics of those mostly used in textile industries.

5.3 C haracteristics of Wastes Produced by the Textile Finishing Industry The pollutant features of textile wastes differ widely among various organic substances. The constituent’s important parameters of textile wastewater such as temperature, solids, odour, colour and the degree of treatment depend to its influent and effluent characteristics (Upadhye and Joshi 2012). However, the contribution of each constituent may vary in place depending on the type of job undertaken. Each waste such as dyes, starches and detergents demands different pollution prevention and treatment approaches. Dyes not only contain toxic compounds such as heavy metals which can accumulate in environment and organisms, but they also interfere with sunlight penetration into water, retard photosynthesis and affects gas solubility in water bodies (Szalinska et al. 2010; Daâssi et al. 2013). The undesirable substances should be removed to prevent septic conditions and avoid rendering the stream water unsuitable for municipal, industrial, agricultural and residential uses. However, not only dyes but also other wastes such as solids in textile wastewater from fibrous substrate and process chemicals may also potentially inhibit the growth of plant life in water courses. Some of synthetic dyes such as azo, anthraquinone, heterocyclic, triphenylmethane or phthalocyanine are usually designed to be resistant to light, biological activity, ozone and other degradative environment in order to increase the quality of the textile. These resistance characteristics are related to the chemical structure of dye as such reactive cleavage of its azo group (Zheng et al. 2013) or mutagenic formation of aromatic amines (anilines) (Martins et al. 2001). Therefore, discharge of dye-containing effluents promotes escalating problem because of their colour and their hazardous and carcinogenic breakdown products (Mugdha and Usha 2012). Even with lower amount of pollutant in textiles, water with the presence of dyes (60%)/24 h S.F. Turq Blue (81.3%), S.F. Black CKF (74.2%) and S.F. Red C4BLN dye (67.8%)/12 h Reactive Black 5, Acid Orange 7 and Congo red azo dyes (70–92%) Indigo carmine (90.18%)/6 h

Bilal et al. (2015)

Neoh et al. (2015) Li et al. (2015) Qin et al. (2014)

Wastewater (85–93%)/6 days

Pakshirajan and Radhika (2013) Chanwun et al. (2013)

Peroxidases

LiP, MnP, Lac

Pleurotus eryngii

Aniline blue, malachite green, methyl green, water blue (83–97%)/24 h Brilliant green, bromocresol purple, crystal violet, fuchsin, methyl violet (49–68%)/4 h Reactive Black 5 (93.56%)/72 h

Lac

Lac Lac, MnP

Basidiomycete sp. L-168 Pleurotus ostreatus, P. chrysosporium Pleurotus ostreatus P. ostreatus

Remazol Brilliant Blue R (98.53%)/5 days Reactive dye blue (85–92.92%)/10 days Disperse violet (97.67%)/3 days Direct blue (99%)/18 h

Lac

Armillaria sp.

LiP, MnP, Lac

Crepidotus variabilis

Remazol Brilliant Blue R (86%)/96 h Remazol Brilliant Blue R (92%), raw textile water (58%)/14 days

LiP, MnP, Lac

Ling et al. (2015)

Remazol Brilliant Violet 5R (94–96.0%)/5 h 25 types of textile dyes Malachite green (73%) and methylene blue (35%)/3 h

Cerrena sp. Aureobasidium pullulans, Cladosporium werneckii Phanerochaete chrysosporium Hevea brasiliensis

LiP, MnP

References Bilal and Asgher (2015)

Yang et al. (2014) Ademakinwa and Agboola (2014)

Hadibarata et al. (2013) Narkhede et al. (2013) Kiran et al. (2012) Devi et al. (2012) Vishwakarma et al. (2012) Hadibarata et al. (2012) Mangamuri et al. (2012) (continued)


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Table 5.5 (continued) Enzymes Lac, MnP

Fungi produced Trametes trogii

LiP, MnP, Lac

Datronia sp.

Dyes (percentage of decolourized)/decolourization time Fast Blue RR (65%), azure B (30%), methylene blue (30%)/24 h Remazol Brilliant Blue R (RBBR) and Reactive Black 5 (RB5)

References Grassi et al. (2011) Vaithanomsat et al. (2010)

LiP lignin peroxidase, MnP manganese peroxidase, Lac laccase, CMcase carboxymethyl cellulase, Xyl xylanase

5.6.1.1 Lignin Peroxidase (LiP; EC 1.11.1.14) Starting from the early 1980s, a large amount of information on peroxidases from P. chrysosporium has been accumulated (Tien and Kirk 1983). Crystal models have been described by Miki et al. (2006), and a complete review about this class of peroxidases has been presented within the years (Martinez et al. 2005). The first cDNA clones of LiPs were isolated from strain BLM-F-1767 by using synthetic oligonucleotide probes based on partial amino acid sequences of LiP isoenzyme H8 (Zhang and Reddy 1988). Lignin peroxidase in fungi is always reported globular in structure of helical glycoproteins, with approximate molecular weight in the range of 30–50 KDa with an isoelectric point (pI) between 3.0 and 5.0 (Tien and Tu 1986). The optimum pH and temperatures for LiPs are varied and reported to be between 2–5 and 30–60°C, respectively (Ten Have et al. 1998). In sulphonated azo dye degradation, two electrons were oxidized by the H2O2 oxidized forms of LiP in the phenolic ring which resulted in the productin of a free radical (which bearing to the azo linkages) which lead to the production of phenyldiazene (Shree Nath, 2014). However, there are a large number of published studies that described the role of lignin peroxidase in dye degradation (Chen et al. 2011; Imran et al. 2015; Nguyen and Juang 2013). 5.6.1.2 Manganese Peroxidase (E.C. 1.11.1.13) The first extracellular manganese peroxidase from P. chrysosporium Burds BLM- 1767 was purified by using chromato-focusing column chromatography (Paszczyński et al. 1985). The purification resulted in molecular mass of 45–47 kDa and contained an easily dissociable haem which required Mn2+ ion for its activity. Multiple isoforms of different molecular weights have been also isolated from many members of white-rot fungi family (Godfrey et al. 1990; Hildén et al. 2005; Pease et al. 1989). This enzyme has optimum pH range between 4 and 7 and temperatures of 40–60°C (Baborová et al. 2006; Martinez et al. 1996). MnPs utilize H2O2 to oxidize compounds such as vanillyl acetone, 2,6-dimethyloxyphenol, curcumin, syringic

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acid, guaiacol, syringaldazine, divanillyl acetone and coniferyl alcohol. The previous studies showed that the degree of azo dye decolourization increased in the presence of MnP such as in the case of Schizophyllum sp. (Yao et al. 2013). In other dye decolourization study by white-rot fungi Ganoderma lucidum, MnP caused maximum decolourization of S.F. Turq Blue dye up to 81.3%, followed by S.F. Black CKF to 74.2% and S.F. Red C4BLN dye to 67.8% within 12 h which confirmed its catalytic potential to degrade and mineralize dyes and coloured effluents (Bilal et al. 2015). 5.6.1.3 Versatile Peroxidase (EC 1.11.1.16) Versatile peroxidase (VP) is also known as hybrid peroxidase or manganese-lignin peroxidase and characterized by a unique combining catalytic properties of manganese peroxidase (oxidation of Mn II), lignin peroxidase (Mn-independent oxidation of non-phenolic aromatic compounds) and plant peroxidase (oxidation of hydroquinones and substituted phenols) (Ruiz-Dueñas et al. 2009). The high redox-potential compounds such as dye Reactive Black 5 (RB5) as well as a wide variety of phenols, including hydroquinones, are efficiently oxidized by VPs (Gomez-Toribio et al. 2001). Due to their dual oxidative properties as a result of hybrid molecular structures which provide multiple binding sites, this enzyme has wide range of redox potentials, including low- and high-redox potentials, and this gives VP superiority compared to both LiPs and MnPs (Camarero et al. 1999). However, the production and application of VP are always hindered by its low yield in large-scale production and thus become less attractive industrially. Some works had suggested the enhancement of the enzyme produced using some approaches such as DNA recombinant technology or using heterologous expression system (Dashtban et al. 2010). A complete oxidative catalytic reaction of VP has been described recently (Busse et al. 2013; Ravichandran et al. 2016).

5.6.2 Azoreductase (EC 1.7.1.6) Azoreductases are reducing enzymes used for dye degradation, they are mainly monomeric, but a few are also reported as dimeric and tetrameric in nature (Bafana and Chakrabarti 2008). These enzymes catalyse reductive cleavage of electrophilic azo groups (−N = N–) and other compounds containing azo bond by transferring electrons via soluble flavins to azo dyes to produce aromatic amines. However, these enzymes are usually inactivated in the presence of oxygen. Besides their presence in different fungal strains, azoreductases have also been detected in bacteria, algae and yeast (Chengalroyen and Dabbs 2013).


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5.6.3 Laccases (E.C 1.10.3.2) Laccases differ from lignin peroxidase and manganese peroxidase in their ability to proceed their oxidative activity in the absence of H2O2 (Yaropolov et al. 1994). In other words, the laccases from fungi are able, in particular, to degrade lignin in the absence of peroxidases (Eggert et al. 1997). Laccase was known before as polyphenol oxidase in the family of blue multi-copper oxidases which catalyse the one- electron of four reducing-substrate molecules during oxidation of an array of aromatic substrates preferably phenolic compounds, concomitantly with the reduction of molecular oxygen to water (Mayer and Staples 2002). However, it has been reported that fungal laccases have higher redox potential than bacterial or plant laccases with up to +800 mV (Kunamneni et al. 2007). Although there are several reports on the removal of dyes from wastewater using both bacterial and fungal laccases, enzymes secreted by white-rot fungi are usually considered as the most effective laccases for dye degradation process (Mirzadeh et al. 2014). Recent applications of laccase include also the process of bleaching of denim fabrics (Yavuz et al. 2014), stimulated in non-enzymatic homo- and/or hetero-coupling reaction to produce variable colour palette for textiles (Sousa et al. 2013). Recent research reported also that the combination of enzymatic treatment with ultrasound increases the efficiency of dye removal in wastewater (Goncalves et al. 2015).

5.7 Decolourization of Dye Using Fungal Biofactories Efficient decolourization of dye is always affected by various factors such as medium composition, pH, temperature, C/N ratio, incubation time, aeration and agitation and initial dye concentration. The decolourization rate is also influenced not only by a single factor but usually as a result of interactions between factors in defining tolerance capacity of each fungus towards colour reduction (Kaur et al. 2015).

5.7.1 Media Composition The decolourization rate of textile dyes is extremely variable and depends strongly on the components of medium. The composition used and their interaction during cultivation play a critical role in the fungal growth and enzyme production. The dye effluents from textile industry usually have complex structure with low nutrients. Therefore, supplementation of the effluents with external carbon and nitrogen sources along with mineral nutrients and other necessary ingredients is essential to improve dye decolourization process (Singh 2006).

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5.7.1.1 Carbon Source The presence of carbon sources in the medium plays an important role for the fungal growth, and also, it supplies the oxidants which mediate the decolourization of dyes. Fungal culture generally requires a source of carbon, organic compound, such as meat extract, peptone, molasses or combination of complex carbon and nitrogen, salts and others such as yeast extract to enhance dye decolourization and degradation. Although fungi are known to metabolize wide range of carbon sources, the extent of decolourization is greatly dependent on the types and concentration of carbon source applied. Based on elemental analysis, fungal cell contains high carbon of about 50% of its weight. Therefore, utilization of carbon from external sources is essential for growth building blocks such as carbohydrates, proteins, lipids and nucleic acids (Mannan et al. 2007). However, fungi only consumed about 2–7% of nitrogen (McKinney 2004). In most studies reported by previous authors, glucose concentration plays a key role in dye removal by fungi. Rohilla et al. (2012) reported that glucose could be appointed as the most suitable carbon source to give maximum decolourization activity at about 90.57%, followed by fructose (87.22%) and sucrose (74.06%). Similar finding has been also proposed by Hadibarata and Ayu Kristanti (2011), as they found also the superiority of glucose when applied in decolourization compared to other carbon sources. Besides the type of carbon source applied, glucose concentration plays also a critical role in dye decolourization process (Asgher et al. 2008; Iqbal et al. 2011). Earlier study by Radha et al. (2005) showed that 5.0 g L−1 glucose was sufficient to achieve maximum dye decolourization by Phanerochaete chrysosporium. However, beyond this level significant reduction in dye decolourization was observed as a result of change in the metabolic pathways. Other studies, carried out by Patel and Gupte (2014), have found that maltose gives a significant effect in the rate of decolourization, almost 1.6 times higher than glucose at maximal rate at about 91.35% followed by other carbon sources in the sequence of sucrose > starch > lactose > fructose > xylose with the range between 74 and 89% dyes decolourized. In addition, cellulose and its derivatives were not supported in dye decolourization process (Kumar et al. 2011). 5.7.1.2 Nitrogen Source Nitrogen is a second essential component of media after carbon based on its requirement for the microbial growth and enzyme production. The utilization to nitrogen-rich compound is a controversial issue, since examples of enzyme productivity enhancement and dye decolourization have been described under both limiting and nonlimiting conditions. The early study showed that the productivity of manganese peroxidase (MnP) and laccase was enhanced under nitrogen-limited conditions during dye decolourization (Swamy and Ramsay 1999a), while the productivity of Bjerkandera adusta lignin peroxidase and manganese peroxidase was improved in nitrogen-sufficient media (Heinfling et al. 1998). It was report that white-rot fungi are able to utilize wide range of both inorganic (ammonium salts) and organic nitrogen


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sources for their growth and dye decolourization (Radha et al. 2005; Kumar et al. 2012). It was reported that the supplementation of dye effluents with suitable nitrogen sources resulted in significant increase in dye degradation (Shree Nath 2014). 5.7.1.3 Mineral Salts In addition to carbon and nitrogen sources, different minerals are also required to enhance cell metabolism and enzymatic activities. The dye biotransformation/decolourization process and microbial growth usually required certain mineral salts or trace metals such as iron, copper and manganese and/or different oxidizing mediators (like veratryl alcohol, tryptophan and aromatics, e.g. phenol and aniline) beside carbon and nitrogen sources to promote the decolourization process (Couto and Toca-Herrera 2007).

5.7.2 pH The efficiency of decolourization rate of fungi is highly dependent on pH. The optimal pH for effective degradation is usually between 3 and 6. The pH value during the degradation is important especially in the process of colour removal due to availability of some components in the textile wastewater that is soluble in a certain range of pH (Harbaijan 2005). It is in fact that pH change during cultivation may affect the enzymatic processes and dye decolourization capacity as well (Asgher et al. 2008). In addition, the ionization state of the functional groups (carboxyl, hydroxyl and amino groups) located on the fungal or bacterial cell wall is highly affected by the pH (Won et al. 2009). Different dyes were successfully decolourized under variable pH condition. For example, the highest rate of Reactive Red M5B decolourization occurred at pH 5.0 (Patel and Gupta 2014), NOVACRON Reactive Black at pH 4.5 (Bibi et al. 2013) and Brilliant green at pH 6.0 (Hadibarata and Ayu Kristanti 2011), and methylene blue, acid green, Congo red and Vat magenta were best decolourized at pH 5.0 (Khataee et al. 2009).

5.7.3 Temperature Temperature is one of the most critical parameters which usually has a strong influence on the growth and enzyme production, thus affecting decolourization rate accordingly. The optimal temperature for decolourization process is varied from one strain to another. Most of fungi exhibited optimal growth and maximal dye decolourization rate under mesophilic condition, i.e. at temperatures ranging between 25 and 35°C (Parshetti et al. 2007). However, Yang et al. (2009) studied the effect of temperature on decolourization of RBBR by Trametes sp. They reported

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that the minimum rate on decolourization of RBBR was obtained at 70°C and maximum decolourization was attained at temperature between 50 and 60°C. Temperature is a good environmental factor to enhance biodegradation activities which attributed to rapid biochemical reactions such as growth, metabolism, enzyme secretion and cell permeability. In general, the increment in fungi growth might mean maximum in the rate of dye removal in the ecosystem.

5.7.4 Agitation and Aeration Aeration and agitation are essential parameters for growth of obligate aerobes and dye degradation process. It was found that increasing the rate of aeration and agitation increases nutrient distribution and oxygen transfer, and thus the dye decolourization rates were enhanced as compared to the stationary cultures (Chakraborty et al. 2013). The disadvantage for static culture is oxygen limitation in the inner layers of culture that can cause inhibition to the oxidative enzymes and limits colour removal process. Theoretically, dissolved oxygen level should be manipulated to enhance physiology and metabolism of fungi, which can be done using different agitation speed or adjustments of airflow rate in the bioreactor or cultivation conditions. Recent study by Rani et al. (2014) had confirmed that decolourization is maximal under agitation conditions. Agitation provides better oxygenation in fungal culture which supports better cell growth and expression of enzymes which are needed to react with the dye molecules during decolourization process. Agitation enhanced the decolourization rate for dye basic fuchsin (81.85%) followed by Nigrosin (77.47%), malachite green (72.77%) and dye mixture (33.08%) by A. niger, whereas P. chrysosporium can perform about 90.15% colour reduction with the Nigrosin (90.15%) followed by basic fuchsin (89.8%), malachite green (83.25%) and mixture (78.4%).

5.7.5 Dye Concentration The concentration of dye is one of the main factors which affects the dye removal capacity of the microbes. It was reported that initial dye concentration should not exceed 1000 mg L−1 for efficient decolourization by microbial strains (Shree Nath 2014). Previouse reports have presented that the rate of decolourization is decreased by increasing dye concentration. The main effect contribution to this phenomenon is the toxicity of the dyes against fungus growth (or co-contaminants) when applied at high concentration. Besides, the decrease in decolourization rates may be caused due to inadequate biomass concentration (improper cell-to-dye ratio) which decreases the capability to uptake high concentration of dyes during treatment process (Saratale et al. 2011). One of these phenomena had been studied by Gahlout et al. (2013) for Ganoderma cupreum AG-1, which observed the reduction of decolourization percentage from 98 to 93% when dye concentration was increased from 0.1 up to 5.0 g L−1.


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5.7.6 Inoculum Size Decolourization process was found to be also dependent on the size of inoculum used. For instance, optimum fungal biomass and high functionality were reported using 2% of spore suspension inoculum which provide decolourization performance of about 88% of Reactive Black 5 using fungal strain of Datronia sp. (Vaithanomsat et al. 2010). Meanwhile, in other studies 10% of inoculum size for Phanerochaete chrysosporium, approximately containing about 3.2 × 105 cell per ml, gives a maximum decolourization rate (Shahvali et al. 2000; Radha et al. 2005).

5.8 B ioprocess Development for Remediation of Azo Dyes Containing Wastewater Growing research in this field encouraged other researchers to focus on the area of process of cell growth and production of high cell mass with great enzyme activities. However, the application of white-rot fungi in large-scale waste treatment has been impeded by the lack of bioreactor systems that can control growth of fungi and sustain the steady production of high levels of ligninolytic enzymes throughout the cultivation period (Karthikeyan and Sahu 2014). So far, most of the studies using bioreactors have been conducted on a relatively small scale faced with overgrowth of organism into clump which at the end blocked the pipework or grow on the surfaces of pH and dissolved oxygen electrodes. Therefore, larger-scale test for decolourization purposes using these fungi needs further research and development. Current situation showing that bioreactor coupled with membrane and other solid immobilization carrier slowly replaced the application of aerated column, airlift and stirred tank bioreactor, giving better results compared to free mycelium. Stirred tank is not presumably used due to the concern about the effects of shear forces on enzymes and mycelial structure during cultivation in reactor, while airlift reactor is still preferable since it provides uniform mixing and good aeration with lower power input (Srikanlayanukul et al. 2006). Application of different types of reactor using white-rot fungi in the purpose of dye removal is summarized in Table 5.6. Much works had presented dealing with batch, repeated batch culture and fed- batch culture compared to continuous culture. However, each method has its own advantages and disadvantages (Rodarte-Morales et al. 2012). Batch is simple in terms of operation and covers variety of reaction types but limited in operation range. On the other hand, continuous reactor offers wider o perating changes and is easy to scale up. However, it is always associated with high cost and relatively wasteful on product during start-up and shutdown. Fed-batch culture is presumably used for decolourization study in case of non-toxic effluents and high substrate concentration, while if the fungus degraded the toxic components in the effluents, repeated batch becomes more suitable for this process.

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Table 5.6 Types of bioreactor and operation mode used in fungal treatment of wastewater and its efficiency in decolourizing dyes Fungus Coriolus versicolor Phanerochaete chrysosporium Coriolopsis gallica

Trametes pubescens

Trichoderma viride Pleurotus florida Curvularia lunata URM 6179 and Phanerochaete chrysosporium Trametes versicolor Phoma sp. (DSM 22425) Trametes versicolor

Type of reactor Membrane bioreactor Repeated batch Immobilized cells in Ca-alginate beads

Batch bubble column reactor (BBC) Fixed bed reactor (FBR) Stirrer tank reactor (STR) Membrane bioreactor Solid state fermentation Static bioreactors under aerated and non-aerated conditions Bubble column reactor Bubble column reactors Membrane- integrated reactor system

Trametes versicolor Aspergillus terreus Coriolus versicolor

Trametes versicolor I

Stirred tank bioreactor Membrane bioreactor Pilot plant air-pulsed bed bioreactor

Dyes (maximum decolourization) Wastewater (98%) Poly R-478 Poly S-119 Remazol Brilliant Blue R, Reactive Black 5 and Grey Lanaset G (>70%) Bismark Brown R (51.2%) Wastewater BBC (30%)/FBR (33.1%) STR (86%)

Red CLB (93–97%) Remazol Brilliant Blue R (46%) Indigo dye (96%)

Reactive Black 5 dye (86 and 87%) MWW containing acid dyes by 61% 98, 88, 80 and 78% were obtained for Red FN-2BL, Red BWS, Remazol Blue RR and Blue 4BL Reactive Black S (91–99%) Dye sulphur black (75.24% in 24 h) Synthetic wastewater containing dye (98% in 1 day) Grey Lanaset G (98% for 48 h and >78% for the next 3 months) Wastewater (40–60% for 15 days)

References Hossain et al. (2015) Karthikeyan and Sahu (2014) Daassi et al. (2014)

Spina et al. (2014)

Vinodha et al. (2013) Sathishkumar et al. (2013) Miranda et al. (2013)

Castillo-Carvajal et al. (2012) Junghanns et al. (2012) Mendoza et al. (2011)

Ottoni et al. (2011) Andleeb et al. (2010) Hai and Yamamoto (2009) Blánquez et al. (2008)

(continued)


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Table 5.6 (continued) Fungus Coriolus versicolor Trametes versicolor

Type of reactor Membrane reactor Fluidized bioreactor

Coriolus versicolor RC3 Coriolus versicolor

Repeated batch bioreactor Sequential batch bioreactor Rotating contactor reactor Membrane bioreactor (MBR)

Trametes versicolor Trametes versicolor

P. chrysosporium Trametes versicolor

Pulsed packed-bed bioreactors Stirred tank reactors

Dyes (maximum decolourization) Poly S119 (99% in 15 h) Grey Lanaset G (>90%) (> 90%) Remazol Brilliant Violet (>90%) Reactive Blue 4 and Reactive Red 2 (>70%) Reactive Blue 19, Reactive Blue 49 and Reactive Black 5 (99% in 8 h) Poly R-478 (65–80%) Reactive Black 5, Reactive Red 198 and Reactive Blue 19 (91–99%)

References Hai et al. (2006) Romero et al. (2006) Srikanlayanukul et al. (2006) Sanghi et al. (2006) Nilsson et al. (2006) Kim et al. (2004)

Mielgo et al. (2002) Borchert and Libra (2001)

Development broth in submerged fermentation for the enhanced production of enzymes for dye decolourization requires a detailed knowledge of the growth characteristics and fungal cell physiology. It involved not only the diversified metabolites that require different physiological conditions (Papagianni 2004). Henceforth, the hurdle issues involved in precise physiological conditions and the correct stage of development are an area worthy of being studied in depth for maximal enzyme production. Many scientists have discussed a real issue in the effect of fungal morphology in submerged fermentation in order to make optimal use of their potential production capacities. Aspergillus niger has become a model in fungal morphological study in which impressive landscape of results about fungal morphology and metabolite overproduction was reported (Krull et al. 2010). The factors involved in the changes and control of filamentous fungal morphology were characterized further involving different process parameters such as power input through stirring and aeration, mass transfer characteristics, pH value, osmolality, the presence of solid microparticles and surface properties of fungal spores and hyphae (El-Enshasy 2007; Krull et al. 2013; Quintanilla et al. 2015). Thereby, the need to produce enzymes commercially at competitive prices with high activities may be enhanced by other substantial areas such as protein engineering. However, recent protein engineerig research help to design highly efficient enzymes with wide range of applications (Mate and Alcade 2016).

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5.9 D ecolourization of Home-Made Textile Industry in Malaysia Textile industry is the third largest sector earner after electronic and palm oil sectors in Malaysia, estimated about RM 18.0 million (US$5.4 million) according to manufactured exports in 2007 (Siddiquia et al. 2011). One of the textile arts of Malaysia goes to Malaysian heritage textile industry called batik. This home-made dyed cloth industry is popular in the east coast of Peninsular Malaysia such as in Terengganu and in Kelantan as well as in Indonesia and Thailand. It is traditionally inherited from generation to generation, painting with different motifs according to its origin. For instance, batik produced in Indonesia (java) is more colourful which means more dyes are used (Boehike 2005). In the process of batik painting, a lot of dyes, waxes and chemicals (such as ludigol, sodium silicate, sodium carbonate, sodium alginate and potassium aluminium sulphate) are used (Ahmad et al. 2012). However, the most used dyes in batik are Remazol and Vinyl Sulphone fibre- reactive dyes (Rashidi et al. 2012). Reactive dyes used in batik textile are highly stable, excellent in colourfastness, bright coloured and easy to apply. Conventionally at the end of the process, the wax is eliminated using boiling water in order to make the dyes fixed and washable. To accomplish this, large amount of water is used and usually discharged to water bodies without proper treatment. The batik wastewater sample was characterized in terms of the biochemical oxygen demand (BOD), chemical oxygen demand (COD), pH, temperature, total suspended solid (TSS) and turbidity (Khalik et al. 2015). The characteristics of batik effluent are shown in Table 5.7. The textile dyeing industry has been put under immense pressure to reduce the colour of process waters directly discharged to municipal water treatment facilities. Considering the visible colour present in the textile effluent, their removal is always connected with the decolourization activities to reduce dye content to acceptable levels. In Malaysia, according to the environmental quality regulations of the industrial effluent guidelines in 2009, there are limits of colour in effluents after discharge, which are 100 platinum-cobalt (PtCo) units according to

Table 5.7 Characteristics of batik dyeing wastewater (Adapted from Khalik et al. 2015) Parameters DOa (mg/L) CODb (mg/L) TSSc (mg/L) pH λmaxd (nm)

Medium-scale batik industry wastewater 8300 20,100 3000 7.5 575

DO: Dissolved oxygen COD: Chemical oxygen demand c TSS: Total suspended solids d λmax: Maximum absorption wavelength a

b

Small-scale batik industry wastewater 6900 14,500 1840 6.9 585


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standard A and 200 platinum-cobalt (PtCo) units according to standard B (DOE 2010). Unfortunately, the lack of public awareness among local manufacturers in terms of respecting the local environmental quality requirements and standards led to poor actions and social responsibilities. The decolourization studies in batik dyeing effluent raise attention since it has been recognized to cause vast pollution in wastewater. The intensity of water use in batik industry could be significantly reduced by using the technology that enables to reuse or recycle wash water back to the process after sufficient treatment. Othman et al. (2011b) explore the liquid-liquid extraction methods using tridodecylamine (TDA) in kerosene to remove Black B dye and Remazol Brilliant Orange 3R from batik industry water. New application of nano-membrane was also widely studied and proved to be efficient in removing different fibre-reactive dyes (Rashidi et al. 2012; Rashidi et al. 2015). The using of adsorbent agent such as beads of silica- filled ERN/PVC types to treat batik effluents was demonstrated by Abdullah et al. (2012) by showing 88% efficient removal of dyes with an adsorption capacity of 2.67 mg dye per kg of beads. While most of the studies only focus either in extracting or removing the dyes, Othman et al. (2011a) had discovered better degradation of dyes using dual techniques of liquid membrane emulsion (LME), and it is more advantageous since it is proved to reduce the cost due to the ability to concentrate the pollutant up to 100 times. According to Pang and Abdullah (2013), biological method for textile treatments becomes nascent in Malaysia influenced by the economic impact at present. A recommendation was made to meet the desired water quality by the sequential use of chemical treatments (separation of coloured from non-coloured wastewater) followed by the biological treatments (to remove organic matters) before the final treatment by adsorption or membrane separation as polishing purposes. A study by Siddiquia et al. (2011) presented a natural remediation and biofouling potential of real batik textile dyes using potent Bacillus sp. In contrary, Nguyen et al. (2012) denied this treatment as the fouling would decrease the membrane flux during the separation processes either on the surface of a membrane or within its pores. Another report on bacterial remediation to decolourize batik wastewater was carried out using Lactobacillus delbrueckii under different cultivation conditions (Zuraida et al. 2013). From this study, a microbe showed optimum colour removal (45–60%) in less than 72 h under static condition at pH 6.0 and temperature of 37°C. However, a limited number of studies have been carried out for decolourization and treatment of toxic batik dyeing wastewater effluent using fungal cells. Srikanlayanukul et al. (2006) have reported the potential application of Coriolus versicolor to decolourize synthetic textile wastewater and real wastewater from batik dyeing factory. Other study also reported the potential of integrating membrane technology with biological reactors for the treatment of batik dyeing wastewaters by a combination of three generic membrane processes within bioreactors, for separation and recycle of solids, for bubble-less aeration of the bioreactor and for the extraction of priority organic pollutants from hostile textile dyeing wastewaters (Ramlee et al. 2014).

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5.10 Other Applications of Mycoremediation Mycoremediation is nascent for the purpose to reduce the environmental pollution based on its low-cost, high efficiency, natural, safe and fast process. Mycoremediation is only one step in the complex process of environmental recovery as well as in stabilizing the contaminated environment and in restoring habitat.

5.10.1 Treatment for Heavy Metal Pollution Heavy metal pollution in soil is one of the most dangerous contaminants which has high negative impact on human, animal health as well as the overall ecosystem. Currently, conventional methods such as chemical precipitation, electrodialysis, coagulation or flocculation, ultrafiltration, reverse osmosis, adsorption, evaporation, ion exchange, electrowinning and cementation are used widely. Along with the development of microbial industry and technology, various types of endophytic fungi have been shown to be highly effective and economically feasible for the removal of toxic metals from effluent. Many research in this field revealed that fungi contained high percentage of cell wall materials which support high activities for metal binding properties to adsorb heavy metal. Some fungi are characterized by their hyperaccumulation capacity such as in case of absorption of heavy metals in the fruiting bodies of mushroom (Thakur 2014; Jagtap et al. 2003). Removal of a wide range of heavy metals such as Cu, Cd, Cr, Pb and Zn had been reported by Singh and Gauba (2014) by Galerina vittiformis. Marasmius oreades is a well- known fungus for its capacity for accumulation of bismuth and titanium. Pacheco et al. (2015) reported on the potential application of Phanerochaete chrysosporium and Trametes versicolor for the removal of Cr3+ at concentrations between of 0.5 and 1 mg L−1, whereas T. versicolor is able to absorb Pb2+ at concentrations between 0.25 and 2 mgL−1. Phanerochaete chrysosporium exhibited good capacity for removing heavy metals such as Zn (II) and Pb (II) through biosorption with the efficiency of about 57% and 87%, respectively, at concentration 100 mg L−1, pH 6.0, 150 rpm and 5 gL−1 of biomass concentration (Marandi et al. 2010). In other study conducted by Mohsenzadeh and Shahrokhi (2014), they reported that Trichoderma asperellum is capable to absorb Cd up to 76.17% or approximately 10.75 mg/g in alkaline pH. According to Qayyum et al. (2016), two indigenous fungal isolates, Aspergillus flavus and R. pusillus, can act as potential biosorbent in removing of Pb, Cd and Cr with maximum uptake of 39.58, 68.02 and 68.87 mg g−1, respectively. S. bovinus has also the capacity to accumulate Hg at low-level polluted soils (Saba et al. 2016).


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5.10.2 B iodegradation of Polycyclic Aromatic Hydrocarbon (PAH) Compounds Polycyclic aromatic hydrocarbon (PAH) compounds are over 100 groups of different chemicals that formed during the incomplete burning of coal, oil and gas, garbage or other organic substances like tobacco or charbroiled meat. PAHs are the class of hydrocarbons containing two or more fused aromatic hydrocarbons and considered as potent environment pollutants of oil, tar and coal residues. Generally, PAHs are toxic, carcinogenic and mutagenic. Therefore, their presence in environment is of great concern and has deleterious effect on human health (Gupte et al. 2016). The ability of fungi in biodegradation of hydrocarbon water contamination released from petrochemical industry is well documented. Generally, hydrocarbon components composed of hydrogen and carbon belong to the family of carcinogens and neurotoxic organic pollutant. Most of the current industrial treatment methods of PAH include incineration, mechanical and chemical methods. The limitations of these methods are mainly the high cost and production of large amount of contaminants. It was reported that few species of fungi have high PAH biodegradation capacity. This biological process involved metabolism of PAH during fungal growth, mineralization of the PAH and biotransformation. It has been reported that Phanerochaete, Trametes, Bjerkandera and Pleurotus are potent strains for PAH biodegradation (Gupte et al. 2016; Bamforth and Singleton 2005; Hestbjerg et al. 2003). The fungal species P. chrysosporium has been known for its biodegradation capacity and thus plays an important role in PAH removal (Thakur 2014; Adenipekun and Lawal 2012). It is also reported that the P. ostreatus produced high activities in degrading PAHs with positive correlations in the increment concentration of PAHs (Tirado-Torres et al. 2016).

5.10.3 Biopulping Biopulping is another application of biotechnology as alternative for traditional chemical pulping. According to Bajpai (2012), biopulping is commonly related to the initial process of fermentation using fungus on woodchips through solid-state fermentation during the production of mechanical or chemical pulping. The colonization of woodchips by white-rot fungi is considered as the most proficient group to degrade lignin in wood with selective type of degradation, hence leaving the hemicellulose and cellulose relatively intact. Moreover, based on their fast growth behaviour and ability to degrade both of hard and soft woods, they have high potential application in biopulping (Singh et al. 2010). The well-known white-rot fungal strain Phanerochaete chrysosporium has been recognized as the best candidate used in biopulping (Kang et al. 2007). However, other potential white-rot fungi such as Pycnoporus coccineus (Couturier et al. 2015), P. ostreatus and T. versicolor also have been recently used in this process (Bari et al. 2015).

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5.10.4 Biogas Production Lignocellulosic wastes are renewable, cheap and widely available resources, which are suitable for sustainable policy for the production of biodiesel, bioethanol, biogas, biohydrogen and other chemicals (Liu et al. 2014). However, the lignin content in the feedstock hindered the biogas production and thus needs to be removed. Biogas is generally generated from anaerobic digestion (AD) units of organic feedstocks from industrial and agricultural wastes, sewage sludge and wastewater (Chen et al. 2010). The produced biogas is composed of methane, carbon dioxide and other trace gases. The pretreatment of waste materials before AD is considered important to improve biodegradability and biogas production from lignocellulosic materials by speeding up the hydrolysis step. The integration of different pretreatment methods including physical, chemical and biological is a common industrial practice (Sari and Budiyono 2014). A recent study of Ali and Sun (2015) showed that using integration approach in milling (physical), addition of NaOH and NH4OH (chemical) and fungal pretreatment using A. terreus and T. viride (biological) enhance methane gas under anaerobic fermentation condition. Pretreatment using Trichoderma reesei resulted in significant improvement in biogas production from Sisal leaf decortications residue (SLDR) (Muthangya et al. 2009). The production of methane from pretreatment straw with Ceriporiopsis subvermispora has also been also enhanced through time of the digestion process (Vasmara et al. 2015). As fungi have been used in this process, the production of several types of enzyme cocktails (laccase, peroxidase and cellulase) along with the production of biogas and bioethanol has been observed from pretreatment using Pleurotus florida in the softening process of paddy straw (Malayil and Chanakya 2016).

5.11 Conclusion The textile dyeing industry is considered as one of the most polluter industries in the world; it produces huge amounts of toxic and persistent and intensely coloured effluents causing severe environmental pollution. Therefore, the treatment of textile dyeing industrial effluents is necessary prior to final discharge to the environment. As result of complexity in chemical structure of the reactive dyes and their colour index, the conventional physico-chemical strategy can contribute to many environmental problems. In response to environmental regulations, research efforts have been paid towards finding novel strategy for decolourization with minimal impact on ecosystems. Mycoremediation is one of the green chemistry strategies which is considered as the safest, least disruptive and most cost-effective treatment in comparison with traditional physico-chemical treatments for decolourization processes. Three essential mechanisms (biosorption, biodegradation and bioaccumulation) are utilized by fungal strains for the removal of recalcitrant dyes from environment. In order to achieve ultimate benefit from fungal decolourization potential, the different


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essential factors should be considered during dye removal processes such as medium composition, pH, temperature, TOC/N ratio, incubation time aeration and agitation and initial dye concentration. Recently, enzymatic mycoremediation has received much attention from researchers for decolourization/degradation of textile dyes. Based on the high capacity of white-rot fungi to produce and excret decorlizing enzymes, they become one of interesting funcal group in mycoremediation research and applications. Enzymatic degradation of synthetic azo dyes is very promising and an effective decolourization process. The most important enzymes involved in decolourization process are laccases, lignin peroxidase (LiP), manganese peroxidase (MnP), versatile peroxidase (VP) and azoreductase. Finally, mycoremediation plays critical role in reducing environmental pollutants not only through dye decrolorization but also by remediation of other harzardous havey metal, and xenobiotics such as polyacrylic aromatic hydrocarbons (PAHs). Therefore, mycoremediation is considered as an important process for environmental protection.

References Abdullah N, Othaman R, Abdullah I, Jon N, Baharum A (2012) Studies on the adsorption of phenol red dye using silica-filled ENR/PVC beads. JETEAS 3:845–850 Ademakinwa NA, Agboola FK (2014) Production of laccase by Auerobasidium Pullulans and Cladosporium Werneckii under optimized conditions: applications in decolourization of textile dyes. RRJMB 3(2):32–40 Adenipekun CO, Lawal R (2012) Uses of mushrooms in bioremediation: a review. Biotechnol Mol Biol Rev 7(3):62–68 Ahmad A, Harris W, Ooi B (2012) Removal of dye from wastewater of textile industry using membrane technology. Jurnal Teknologi 36:31–44 Ali NF, El-Mohamedy RSR (2012) Microbial decolourization of textile waste water. J Saudi Chem Soc 16:117–123 Ali SS, Sun J (2015) Physico-chemical pretreatment and fungal bio-treatment for park wastes and cattle dung for biogas production. Springer Plus 4:712–725 Andleeb S, Atiq N, Ali MI, Razi-ul-Hussnain R, Shafique M, Ahmad B, Ghumro PB, Hussain M, Hameed A, Ahmad S (2010) Biological treatment of textile effluent in stirred tank bioreactor. Int J Agric Biol 12:256–260 Asgher M, Kausar S, Bhatti HN, Shah SAH, Ali M (2008) Optimization of medium for decolorization of solar golden yellow R direct textile dye by Schizophyllum commune IBL-06. Int Biodeter Biodergr 61:189–193 Asgher M, Shahid M, Kamal S, Iqbal HMN (2014) Recent trends and valorization of immobilization strategies and ligninolytic enzymes by industrial biotechnology. J Mol Catal B Enzym 101:56–66 Ayed L, Bakhrouf A, Achour S (2011) Application of the mixture design to decolorize effluent textile wastewater using continuous stirred bed reactor. Water SA 2(37):21–26 Baborová P, Möder M, Baldrian P, Cajthamlová K, Cajthaml T (2006) Purification of a new manganese peroxidase of the white-rot fungus Irpex lacteus, and degradation of polycyclic aromatic hydrocarbons by the enzyme. Res Microbiol 157:248–253 Babu BR, Parande A, Raghu S, Kumar TP (2007) Cotton textile processing: waste generation and effluent treatment. J Cotton Sci 11(3):141–153 Bafana A, Chakrabarti T (2008) Lateral gene transfer in phylogeny of azoreductase enzyme. Comput Biol Chem 32:191–197

96


Bajpai P (2012) Biopulping. In: Biotechnology for pulp and paper processing. Springer US, Boston, pp 67–92 Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736 Bari E, Nazarnezhad N, Kazemi SM, Tajick GMA, Mohebby B, Schmidt O, Clausen CA (2015) Clausen comparison between degradation capabilities of the white rot fungi Pleurotus ostreatus and Trametes versicolor in beech. Int Biodeter Biodergr 104:231–237 Bibi I, Bhatti HN, Asgher M (2013) Bioremediation of wastewater containing reactive dyes by Agaricus bisporus a21: effect of supplements and redox mediators. Pak J Agric Sci 50(3):445–453 Bilal M, Asgher M (2015) Sandal reactive dyes decolorization and cytotoxicity reduction using manganese peroxidase immobilized onto polyvinyl alcohol-alginate beads. Chem Cent J 9:47–60 Bilal M, Asgher M, Ramzan M (2015) Purification and biochemical characterization of extracellular manganese peroxidase from Ganoderma lucidum IBL-05 and its application. Sci Res Essays 10:456–464 Blánquez P, Sarrà M, Vicent T (2008) Development of a continuous process to adapt the textile wastewater treatment by fungi to industrial conditions. Process Biochem 43:1–7 Boehike H (2005) Encyclopedia of clothing and fashion volume1. Academic Dress to Eyeglasses/ Thomos Gale Corporation, Columbus, pp 123–130 Borchert M, Libra JA (2001) Decolorization of reactive dyes by the white rot fungus Trametes versicolor in sequencing batch reactors. Biotechnol Bioeng 75:313–321 Brown ME, Chang MCY (2014) Exploring bacterial lignin degradation. Curr Opin Chem Biol 19:1–7 Busse N, Wagner D, Kraume M, Czermak P (2013) Reaction kinetics of versatile peroxidase for the degradation of lignin compounds. Am J Biochem Biotechnol 9(4):365–394 Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J Biol Chem 274:10324–10330 Carmen Z, Daniela S (2012) Textile organic dyes–characteristics, polluting effects and separation/ elimination procedures from industrial effluents–a critical overview. In: Organic pollutants ten years after the Stockholm convention-environmental and analytical update. InTech, Rijeka, pp 55–81 Castillo-Carvajal L, Ortega-Gonzále K, Barragán-Huerta BE, Pedroza-Rodríguez AM (2012) Evaluation of three immobilization supports and two nutritional conditions for reactive black 5 removal with Trametes versicolor in air bubble reactor. Afr J Biotechnol 11:3310–3320 Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Kenneth N (ed) Timmis handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 2079–2110 Chakraborty S, Basak B, Dutta S, Bhunia B, Dey A (2013) Decolorization and biodegradation of congo red dye by a novel white rot fungus Alternaria alternata CMERI F6. Bioresour Technol 147:662–666 Chander M, Arora D (2007) Evaluation of some white rot fungi for their potential to decolourise industrial dyes. Dyes Pigments 72:192–198 Chanwun T, Muhamad N, Chirapongsatonkul N, Churngchow N (2013) Hevea brasiliensis cell suspension peroxidase: purification, characterization and application for dye decolorization. AMB Express 3:14–22 Chen Y, Yang G, Sweeney S, Feng Y (2010) Household biogas use in rural China: a study of opportunities and constraints. Renew Sustain Energy Rev 14:545–549 Chen M, Zeng G, Tan Z, Jiang M, Li H, Liu L, Zhu Y, Yu Z, Wei Z, Liu Y, Xie G (2011) Understanding lignindegrading reactions of ligninolytic enzymes: binding affinity and interactional profile. PLoS One 6:1–8 Chengalroyen MD, Dabbs ER (2013) The microbial degradation of azo dyes-minireview. World J Microbiol Biotechnol 29:389–399


97

Chiong T, Lau S, Khor E, Danquah M (2014) Enzymatic approach to phenol removal from wastewater using peroxidases. OA. Biotechnology 10:3–9 Couto R, Toca-Herrera JL (2007) Laccase production at reactor scale by filamentous fungi. Biotechnol Adv 25:558–569 Couturier M, Navarro D, Chevret D, Henrissat B, Piumi P, RuizDuenas FJ, Martinez AT, Grigoriev IV, Riley R, Lipzen A, Berrin JG, Master ER, Rosso MN (2015) Enhanced degradation of softwood versus hardwood by the white rot fungus Pycnoporus coccineus. Biotechnol Biofuels 8:216–231 Daâssi D, Mechichi T, Nasri M, Rodriguez-Couto S (2013) Decolorization of the metal textile dye Lanaset Grey G by immobilized white-rot fungi. J Environ Manag 129:324–332 Daassi D, Rodriguez-Couto S, Nasri M, Mechichi T (2014) Biodegradation of textile dyes by immobilized laccase from Coriolopsis gallica into Ca-alginate beads. Int Biodeter Biodegr 90:71–78 Dashtban M, Schraft H, Tarannum A, Syed TA, Qin W (2010) Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Biol 1(1):36–50 Dawkar VV, Jadhav UU, Tamboli DP, Govindwar SP (2010) Efficient industrial dye decolorization by Bacillus sp. VUS with its enzyme system. Ecotoxicol Environ Saf 73:1696–1703 Devi VM, Inbathamizh L, Ponnu TM, Premalatha S, Divya M (2012) Dye decolorization using fungal laccase. Bull Environ Pharmacol Life Sci 1:67–71 DOE (2010) DOE (Department of environment), environmental quality (Industrial effluents) regulations. Official website of department of environment, Ministry of Natural Resources and Environment, Malaysia. https://www.doe.gov.my/portalv1/wpcontent/uploads/2015/01/ Environmental_Quality_Sewage_And_Industrial_Effluents_Regulations_1979__P.U.A_12-79.pdf Duran N, Rosa MA, D’Annibale A, Gianfreda L (2002) Applications of laccases and probable dietary intake with the mushroom meal. Environ Sci Pollut Res 23:14549–14559 Eggert C, Temp U, Eriksson KEL (1997) Laccase is essential for lignin degradation by the white- rot fungus Pycnoporus cinnabarinus. FEBS Lett 407:89–92 El-Enshasy HA (2007) Filamentous fungal cultures – process characteristics, products, and applications. In: Yang S-T (ed) Bioprocessing for value-added products from renewable resources. Elsevier, Amsterdam, pp 225–261 Eswaramoorthi S, Dhanapal K, Chauhan D (2008) Advanced in textile waste water treatment: the case for UV-ozonation and membrane bioreactor for common effluent treatment plants in Tirupur, Tamil Nadu India, Environment with People’s Involvement & Co-ordination in India, Coimbatore Gahlout M, Gupte S, Gupte A (2013) Optimization of culture condition for enhanced decolorization and degradation of azo dye reactive violet 1 with concomitant production of ligninolytic enzymes by Ganoderma cupreum AG-1. Australas Biotechnol 3:143–152 Gerardi MH (2006) Wastewater bacteria. Wiley, Hoboken Ghaly A, Ananthashankar R, Alhattab M, Ramakrishnan V (2014) Production, characterization and treatment of textile effluents: a critical review. J Chem Eng Process Technol 5:1–18 Godfrey BJ, Mayfield MB, Brown JA, Gold MH (1990) Characterization of a gene encoding a manganese peroxidase from Phanerochaete chrysosporium. Gene 93:119–124 Godliving Y, Mtui S (2012) Lignocellulolytic enzymes from tropical fungi: types, substrates and applications. Sci Res Essays 7:1544–1555 Gomez-Toribio V, Martinez AT, Martinez MJ, Guillen F (2001) Oxidation of hydroquinones by the versatile ligninolytic peroxidase from Pleurotus eryngii. H O generation and the influence of Mn. Eur J Biochem 268:4787–4793 Gomez-Eyles JL, Collins CD, Hodson ME (2011) Using deuterated PAH amendments to validate chemical extraction methods to predict PAH bioavailability in soils. Environ Pollut 159:918–923 Goncalves I, Silva C, Cavaco-Paulo A (2015) Ultrasound enhanced laccase applications. Green Chem 17:1362–1374

98


Grassi E, Scodeller P, Filiel N, Carballo R, Levin L (2011) Potential of Trametes trogii culture fluids and its purified laccase for the decolorization of different types of recalcitrant dyes without the addition of redox mediators. Int Biodeter Biodegr 65:635–643 Gupta V, Khamparia S, Tyagi I, Jaspal D, Malviya A (2015) Decolorization of mixture of dyes: a critical review. GJESM 1:71–94 Gupte A, Tripathi A, Rudakiya D, Patel H, Gupte S (2016) Bioremediation of Polycyclic Aromatic Hydrocarbon (PAHs): a perspective. The Open Biotech J 10(Suppl-2, M9):363–378 Hadibarata T, Ayu Kristanti R (2011) Effect of environmental factors in the decolorization of remazol brilliant blue r by Polyporus sp. S133. J Chil Chem Soc 57(2):1095–1098 Hadibarata T, Yusoff A, Aris A, Salmiati HT, Kristanti R (2012) Decolorization of azo, triphenylmethane and anthraquinone dyes by laccase of a newly isolated Armillaria sp. F022. Water Air Soil Pollut 223:1045–1054 Hadibarata T, Adnan LA, Yusoff ARM, Yuniarto A, Zubir MMFA, Khudhair AB, Teh ZC, Naser MA (2013) Microbial decolorization of an azo dye reactive black 5 using white rot fungus Pleurotus eryngii F032. Water Air Soil Pollut 224:1–9 Hai FI, Yamamoto K (2009) Suitability of membrane bioreactor for treatment of recalcitrant textile dye wastewater utilising white rot fungi. Int J Environ Eng 2:43–55 Hai FI, Yamamoto K, Fukushi K (2006) Membrane coupled fungi reactor an innovative approach to bioremediation of hazardous dye wastewater. Environ Sci 13(6):317–325 Hai FI, Yamamoto K, Fukushi K (2007) Hybrid treatment systems for dye wastewater. Crit Rev Environ Sci Technol 37(4):315–377 Hao OJ, Kim H, Chiang PC (2000) Decolorization of wastewater. Crit Rev Environ Sci Technol 30:449–505 Heinfling A, Martínez MJ, Martínez AT, Bergbauer M, Szewzyk U (1998) Transformation of industrial dyes by manganese peroxidases from Bjerkandera adusta and Pleurotus eryngii in a manganese-independent reaction. Appl Environ Microbiol 64:2788–2793 Hestbjerg HP, Willumsen A, Christensen M, Andersen O, Jacobsen CS (2003) Bioaugmentation of tar-contaminated soils under field conditions using Pleurotus ostreatus refuse from commercial mushroom production. Environ Toxicol Chem 22:692–698 Hildén K, Martinez AT, Hatakka A, Lundell T (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent. Fungal Genet Biol 42:403–419 Hossain K, Ismail N, Rafatullah M, Quaik S, Nasir M, Maruthi A, Shaik R (2015) Bioremediation of textile effluent with membrane bioreactor using the white rot fungus Coriolus versicolor. JPAM 9:1979–1987 Imran M, Crowley DE, Khalid A, Hussain S, Mumtaz MW, Arshad M (2015) Microbial biotechnology for decolorization of textile wastewaters. Rev Environ Sci Biotechnol 14:73–92 Iqbal HMN, Asgher M, Bhatti HN (2011) Optimization of physical and nutritional factors for synthesis of lignin degrading enzymes by a novel strain of Trametes versicolor. Bioresources 6(2):1273–1287 Jagtap VS, Sonawane VR, Pahuja DN, Rajan MG, Rajashekharrao B, Samue AM (2003) An effective and better strategy for reducing body burden of radio strontium. J Radiol Prot 23(3):317–326 Junghanns C, Neumann JF, Schlosser D (2012) Application of the aquatic fungus Phoma sp. (DSM 22425) in bioreactors for the treatment of textile dye model effluents. J Chem Technol Biotechnol 87:1276–1283 Kang KY, Sung JS, Kim DY (2007) Evaluation of white rot fungi for biopulping of wood. Mycobiology 35(4):205–209 Karthikeyan MR, Sahu O (2014) Treatment of dye waste water by bioreactor. IJEBB 2:25–29 Kaur B, Kumar B, Garg N, Kaur N (2015) Statistical optimization of conditions for decolorization of synthetic dyes by Cordyceps militaris MTCC 3936 using RSM. Biomed Res Int:536745. https://doi.org/10.1155/2015/536745 Khalik WF, Ho LN, Ong SA, Wong YS, Yusoff NA, Ridwan F (2015) Decolorization and mineralization of batik wastewater through solar photocatalytic process. Sains Malays 44:607–612


99

Khandare RV, Govindwar SP (2015) Phytoremediation of textile dyes and effluents: current scenario and future prospects. Biotechnol Adv 33(8):1697–1714 Khataee AR, Zarei M, Pourhassan M (2009) Application of microalga Chlamydomonas sp. for biosorptive removal of a textile dye from contaminated water: modelling by a neural network. Environ Technol 30:1615–1623 Kim TH, Lee Y, Yang J, Lee B, Park C, Kim S (2004) Decolorization of dye solutions by a membrane bioreactor (MBR) using white rot fungi. Desalination 168:287–293 Kiran S, Ali S, Asgher M, Anwar F (2012) Comparative study on decolorization of reactive dye 222 by white rot fungi Pleurotus ostreatus IBL-02 and Phanerochaete chrysosporium IBL-03. Afr J Microbiol Res 6:3639–3650 Krull R, Cordes C, Horn H, Kampen I, Kwade A, Neu T, Nörtemann B (2010) Morphology of filamentous fungi: linking cellular biology to process engineering using Aspergillus niger. In: Biosystems Engineering II (ed) Christoph Wittmann and Krull Rainer. Springer, Berlin Heidelberg, pp 1–21 Krull R, Wucherpfennig T, Esfandabadi ME, Walisko R, Melzer G, Hempel DC, Kampen I, Kwade A, Wittmann C (2013) Characterization and control of fungal morphology for improved production performance in biotechnology. J Biotechnol 163:112–123 Kumar VV, Kirupha SD, Periyaraman P, Sivanesan S (2011) Screening and induction in laccase activity in fungal species and its applications in dye decolorization, Afr J Microbial Res 5:1261–1267 Kunamneni A, Ballesteros A, Plou FJ, Alcalde M (2007) Fungal laccase-a versatile enzyme for biotechnological applications. Communicating current research and educational topics and trends in. Appl Microbiol 1:233–245 Lange H, Decina S, Crestini C (2013) Oxidative upgrade of lignin–recent routes reviewed. Eur Polym J 49:1151–1173 Lavanya C, Dhankar R, Chhikara S, Sheoran S (2014) Degradation of toxic dyes: a review. IJCMAS 3:189–199 Leelakriangsak M, Borisut S (2012) Characterization of the decolorizing activity of azo dyes by Bacillus subtilis azoreductase AzoR1. Songklanakarin J Sci Technol 34:509–516 Li H, Zhang R, Tang L, Zhang J, Mao Z (2015) Manganese peroxidase production from cassava residue by Phanerochaete chrysosporium in solid state fermentation and its decolorization of indigo carmine. Chinese J Chem Eng 23:227–233 Ling ZR, Wang SS, Zhu MJ, Ning YJ, Wang SN, Li B, Yang AZ, Zhang GQ, Zhao XM (2015) An extracellular laccase with potent dye decolorizing ability from white rot fungus Trametes sp. LAC-01. Int J Biol Macromol 81:785–793 Liu C, Wang H, Karim AM, Sun J, Wang Y (2014) Catalytic fast pyrolysis of lignocellulosic biomass. Chem Soc Rev 43:7594–7623 Lu S (2016) Market size of the global textile and apparel industry: 2014 to 2018. https://shenglufashion.wordpress.com/2015/08/09/market-size-of-the-global-textile-and-apparel-industry2014-to-2018/ Malayil S, Chanakya HN (2016) Fungal enzyme cocktail treatment of biomass for higher biogas production from leaf litter. Procedia Environ Sci 35:826–832 Mangamuri UK, Muvva V, Poda S, Kamma S (2012) Characteristics and dyes biodegradation potential of crude ligninolytic enzymes from white rot fungus Crepidotus variabilis isolated in coastal Tanzania. Malays. J Microbiol 8:83–91 Mannan S, Fakhrul-Razi A, Alam Md Z (2007) Optimization of process parameters for the bioconversion of activated sludge by Penicillium corylophilum, using response surface methodology. J Environ Sci 19:23–28 Marandi R, Doulati Ardejani F, Amir Afshar H (2010) Biosorption of lead (II) and zinc (II) ions by pre-treated biomass of Phanerochaete chrysosporium. IJMEI 1:9–16 Martinez MJ, Ruiz-Dueñas FJ, Guillén F, Martinez AT (1996) Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. Eur J Biochem 237:424–432 Martinez A, Speranza M, Ruiz-Duenas F, Ferreira P, Camarero S, Guillen F, Martinez M, Gutierrez A, del Rio J (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204

100


Martins M, Ferreira I, Santos I, Queiroz M, Lima N (2001) Biodegradation of bioaccessible textile azo dyes by Phanerochaete chrysosporium. J Biotech 89:91–98 Mate DM, Alcalde M (2016) Laccase: a multipurpose biocatalyst at the forefront of biotechnology- mini-review. Microb Biotechnol. https://doi.org/10.1111/1751-7915.12422 Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565 Mbolekwa Z (2007) Removal of reactive dyes from dye liquor using activated carbon for the reuse of water, salt and energy-degree of masters of science in engineering university of Kwazulu- natal, Durban, South Africa. http://www.wrc.org.za/Knowledge%20Hub%20Documents/ Research%20Reports/1542-1-08.pdf McKinney ML (2002) Urbanization, biodiversity, and conservation. BioSci 52:883–890 McKinney RE (2004) Environmental pollution control microbiology. Marcel Dekker, Inc, New York Mendoza L, Jonstrup M, Hatti-Kaul R, Mattiasson B (2011) Azo dye decolorization by a laccase/mediator system in a membrane reactor: enzyme and mediator reusability. Enzym Microb Technol 49:478–484 Miao Y (2005) Biological remediation of dyes in textile effluent: a review on current treatment technologies. Bioresour Technol 58:217–227 Mielgo I, Moreira MT, Feijoo G, Lema JM (2002) Biodegradation of a polymeric dye in a pulsed bed bioreactor by immobilised Phanerochaete chrysosporium. Water Res 36:1896–1901 Miki Y, Tanaka H, Nakamura M, Wariishi H (2006) Isolation and characterization of a novel lignin peroxidase from the white-rot basidiornycete Trametes cervina. J Fac Agr Kyushu Univ 51:99–104 Miranda RCM, Gomes EB, Pereira N Jr, Marin-Morales MA, Machado KMG, Gusmão NB (2013) Biotreatment of textile effluent in static bioreactor by Curvularia lunata URM 6179 and Phanerochaete chrysosporium URM 6181. Bioresour Technol 142:361–367 Mirzadeh SS, Khezri SM, Rezaei S, Forootanfar H, Mahvi AH, Faramarzi MA (2014) Decolorization of two synthetic dyes using the purified laccase of Paraconiothyrium variabile immobilized on porous silica beads. J Environ Health Sci Eng 12:6–14 Mohsenzadeh F, Shahrokhi F (2014) Biological removing of cadmium from contaminated media by fungal biomass of Trichoderma species. J Environ Health Sci Eng 12:102–108 Mugdha A, Usha M (2012) Enzymatic treatment of wastewater containing dyestuffs using different delivery systems. Sci Rev Chem Commun 2:31–40 Muthangya M, Mshandete AM, Kivaisi AK (2009) Two-steps biological pretreatment of sisal leaf decortication residues for enhanced anaerobic digestion for biogas production. Int J Mol Sci 10:66–73 Narkhede M, Mahajan R, Narkhede K (2013) Ligninolytic enzyme production and Remazol brilliant blue R (RBBR) decolorization by a newly isolated white rot fungus: Basidiomycota spp. L-168. Int J Pharm Bio Sci 4:220–228 Neoh CH, Lam CY, Lim CK, Yahya A, Bay HH, Ibrahim Z, Noor ZZ (2015) Biodecolorization of recalcitrant dye as the sole sourceof nutrition using Curvularia clavata NZ2 and decolorization ability of its crude enzymes. Environ Sci Pollut R 22:11669–11678 Nguyen TA, Juang RS (2013) Treatment of waters and wastewaters containing sulfur dyes: a review. Chem Eng J 219:109–117 Nguyen T, Roddick FA, Fan L (2012) Biofouling of water treatment membranes: a review of the underlying causes, monitoring techniques and control measures. Membranes 2:804–840 Nilsson I, Möller A, Mattiasson B, Rubindamayugi MST, Welander U (2006) Decolorization of synthetic and real textile wastewater by the use of white rot fungi. Enzym Microb Technol 38:94–100 Novotný Č, Cajthaml T, Svobodova K, Šušla M, Šašek V (2009) Irpex lacteus, a white-rot fungus with biotechnological potential-review. Folia Microbiol 54:375–390 Othman N, Djamal R, Mili N, Zailani S (2011a) Removal of red 3BS dye from wastewater using emulsion liquid membrane process. J Appl Sci 11:1406–1410


101

Othman N, Mili N, Wong YM (2011b) Liquid-liquid extraction of black B dye from liquid waste solution using tridodecylamine. J Environ Sci Technol 4:324–331 Ottoni C, Lima L, Santos C, Lima N (2011) Bioreactor for the decolourisation of textile dye using ligninolytic fungi under high alkaline and salt conditions. In: Bioreactor for the decolourisation of textile dye using ligninolytic fungi under high alkaline and salt conditions, FEMS 2011-4th congress of European microbiologists Pacheco JS, Santana M, Aguilar Uscanga MG, Cavazos Garduño A, Serrano Niño J, Gómez H, Aguilar Uscanga B (2015) Ability of Phanerochaete chrysosporium and Trametes versicolor to remove Zn , Cr , Pb metal ions. Terra Latinoam 33:189–198 Pakshirajan K, Radhika P (2013) Enzymatic decolourization of textile dyeing wastewater by the white rot fungus Phanerochaete chrysosporium. TLIST 2:42–48 Pang YL, Abdullah AZ (2013) Current status of textile industry wastewater management and research progress in Malaysia: a review. Clean-Soil Air Water 41:751–764 Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259 Parmar B, Mervana P, Vyas B (2015) Degradation of textile dyes by white rot basidiomycetes. Life sci leafl 59:62–75 Parshetti GK, Kalme SD, Govindwar SP (2007) Biodegradation of reactive blue-25 by Aspergillus ochraceus NCIM-1146. Bioresour Technol 98:3638–3642 Paszczyński A, Huynh VB, Crawford R (1985) Enzymatic activities of an extracellular, manganese- dependent peroxidase from Phanerochaete chrysosporium. FEMS Microbiol Lett 29:37–41 Patel Y, Gupte A (2014) Biological removal of synthetic textile dye reactive red M5B by isolated white rot fungal culture AGYP-1 under optimized culture conditions. Int J Agric Environ Biotechnol 7:499–510 Pease EA, Andrawis A, Tien M (1989) Manganese-dependent peroxidase from Phanerochaete chrysosporium. Primary structure deduced from cDNA sequence. J Biol Chem 264:13531–13535 Pereira L, Alves M (2012) Dyes-environmental impact and remediation. In: environmental protection strategies for sustainable development. Springer, New York, pp 111–162 Prieto A, Möder M, Rodil R, Adrian L, Marco-Urrea E (2011) Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products. Bioresour Technol 102:10987–10995 Qayyum S, Khan I, Farhana Maqbool F, Zhao Y, Gu Q, Peng C (2016) Isolation and characterization of heavy metal resistant fungal isolates from industrial soil in China. Pakistan J Zool 48:1241–1247 Qin X, Zhang J, Zhang X, Yang Y (2014) Induction, purification and characterization of a novel manganese peroxidase from Irpex lacteus CD2 and its application in the decolorization of different types of dye. PLoS One 9(11):1–13 Quintanilla D, Hagemann T, Hansen K, Gernaey KV (2015) Fungal morphology in industrial enzyme production-modelling and monitoring. Adv Biochem Eng Biotech 149:29–54 Radha KV, Regupathi I, Arunagiri A, Murugesan T (2005) Decolorization studies of synthetic dyes using Phanerochaete chrysosporium and their kinetics. Process Biochem 40(10):3337–3345 Ramlee NA, Rodhi M, Anak Brandah A, Anuar A, Alias N, Tengku Mohd T (2014) Potential of integrated membrane bioreactor in batik dye degradation-a review. Appl Mech Mat 575:50–54 Rani B, Kumar V, Singh J, Bisht S, Teotia P, Sharma S, Kela R (2014) Bioremediation of dyes by fungi isolated from contaminated dye effluent sites for bio-usability. Braz J Microbiol 45(3):1055–1063 Rashidi HR, Sulaiman NMN, Hashim NA (2012) Batik industry synthetic wastewater treatment using nanofiltration membrane. Procedia Eng 44:2010–2012 Rashidi HR, Sulaiman NMN, Hashim NA, Hassan CRC, Ramli MR (2015) Synthetic reactive dye wastewater treatment by using nano-membrane filtration. Desalination Water Treat 55:86–95 Ravichandran KR, Taguchi AT, Wei Y, Tommos C, Nocera DG, Stubbe J (2016) A >200 meV uphill thermodynamic landscape for radical transport in Escherichia coli ribonucleotide reductase determined using fluorotyrosine- substituted enzymes. J Am Chem Soc 138(41):13706–13716

102


Rodarte-Morales A, Feijoo G, Moreira M, Lema J (2012) Evaluation of two operational regimes: fed-batch and continuous for the removal of pharmaceuticals in a fungal stirred tank reactor. Chem Eng Trans 27:151–156 Rohilla SK, Salar RK, Kumar J (2012) Optimization of physiochemical parameters for decolorization of reactive black HFGR using soil fungus, Aspergillus allhabadii MTCC 9988. J Bioremed Biodegr 3(6):1–5 Romero S, Blánquez P, Caminal G, Font X, Sarrà M, Gabarrell X, Vicent T (2006) Different approaches to improving the textile dye degradation capacity of Trametes versicolor. Biochem Eng J 31:42–47 Ruiz-Dueñas FJ, Morales M, García E, Miki Y, Martínez MJ, Martínez A (2009) Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60:441–452 Saba M, Falandysz J, Nnorom IC (2016) Accumulation and distribution of mercury in fruiting bodies by fungus Suillusluteus foraged in Poland, Belarus and Sweden. Environ Sci Pollut Res 23:2749–2757 Sanghi R, Dixit A, Guha S (2006) Sequential batch culture studies for the decolorisation of reactive dye by Coriolus versicolor. Bioresour Technol 97:396–400 Sankaran S, Khanal SK, Jasti N, Jin B, Pometto AL, Van Leeuwen JH (2010) Use of filamentous fungi for wastewater treatment and production of high value fungal byproducts: a review. Crit Rev Environ Sci Technol 40:400–449 Saratale RG, Saratale GD, Chang JS, Govindwar S (2011) Bacterial dcolorization and degradation of azo dyes: a review. J Taiwan Inst Chem Eng 42:138–157 Sari FP, Budiyono (2014) Enhanced biogas production from rice straw with various pretreatment: a review. Waste Tech 2(1):17–25 Sathishkumar P, Balan K, Palvannan T, Kamala-Kannan S, BT O, Rodríguez-Couto S (2013) Efficiency of Pleurotus florida laccase on decolorization and detoxification of the reactive dye Remazol brilliant blue R (RBBR) under optimized conditions. Clean Soil Air Water 41:665–672 Saxena S, Raja ASM, Arputharaj A (2017) Challenges in sustainable wet processing of textiles. In: Muthu SS (ed) Textiles and clothing sustainability: sustainable textile chemical processes. Springer, Singapore, pp 43–79 Sen SK, Raut S, Bandyopadhyay P, Raut S (2016) Fungal decolouration and degradation of azo dyes: a review. Fungal Biol Rev 30:112–133 Shah M (2014) Effective treatment systems for azo dye degradation: a joint venture between physico-chemical & microbiological process. IJEBB 2(5):231–242 Shahvali M, Assadi MM, Rostami K (2000) Effect of environmental parameters on decolorization of textile wastewater using Phanerochaete chrysosporium. Bioprocess Eng 23(6):721–726 Shojnacka K (2010) Biosorption and bioaccumulation-the prospects for practial applications. Environ Int 36:229–307 Shree Nath S (2014) Microbial degradation of synthetic dyes in wastewaters. Springer International Publishing, Cham Siddiquia M, Wahida Z, Sakinaha M (2011) Bioremediation and biofouling perspective of real batik effluent by indigenous bacteria. IJCEE 2(5):302–308 Singh H (2006) Mycoremediation: fungal bioremediation. Wiley, New Jersey, p 592 Singh K, Arora S (2011) Removal of synthetic textile dyes from wastewaters: a critical review on present treatment technologies. Environ Sci Technol 41:807–878 Singh A, Gauba P (2014) Mycoremediation: a treatment for heavy metal pollution of soil. JCEET 1(4):59–61 Singh P, Sulaiman O, Hashim R, Rupani P, Peng LC (2010) Biopulping of lignocellulosic material using different fungal species: a review. Rev Environ Sci Biotechnol 9:141–151 Singh RL, Singh PK, Singh RP (2015) Enzymatic decolorization and degradation of azo dyes–a review. Int Biodeter Biodegr 104:21–31 Sousa AC, Martins LO, Robalo MP (2013) Laccase-catalysed homo-coupling of primary aromatic amines towards the biosynthesis of dyes. Adv Synth Catal 355:2908–2917 Spina F, Romagnolo A, Prigione V, Tigini V, Varese G (2014) A scaling-up issue: the optimal bioreactor configuration for effective fungal treatment of textile wastewaters. Chem Eng Trans 38:37–42


103

Srikanlayanukul M, Khanongnuch C, Lumyong S (2006) Decolorization of textile wastewater by immobilized Coriolus versicolor RC3 in repeated-batch system with the effect of sugar addition. CMUJ 5:301–306 Srinivasan A, Viraraghavan T (2010) Decolorization of dye wastewaters by biosorbents: a review. J Environ Manage 91:1915–1929 Suteu D, Zaharia C, Malutan T (2011) Removal of orange 16 reactive dye from aqueous solutions by waste sunflower seed shells. J Serb Chem Soc 76:607–624 Swamy J, Ramsay JA (1999) The evaluation of white rot fungi in the decoloration of textile dyes. Enz Microb Technol 24(3):130–137 Szalinska E, Dominik J, Vignati DAL, Bobrowski A, Bas B (2010) Seasonal transport pattern of chromium (III and VI) in a stream receiving wastewater from tanneries. Appl Geochem 25:116–122 Ten Have R, Hartmans S, Teunissen PJM, Field JA (1998) Purification and characterization of two lignin peroxidase isozymes produced by Bjerkandera sp. strain BOS55. FEBS Lett 422:391–394 Thakur M (2014) Mycoremediation- a potential tool to control soil pollution. AJES 9(1):24–31 Tien M, Kirk TK (1983) Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Sci (Washington) 221:661–662 Tien M, Tu C (1986) Cloning and sequencing of a cDNA for a ligninase from Phanerochaete chrysosporium. Nature 326:520–523 Tirado-Torres D, Gayaosso-Canales M, Marmolejo-Santillán Y, Romo-Gómez C, Acevedo- Sandoval O (2016) Removal of polycyclic aromatic hydrocarbons by Pleurotus ostreatus sp. ATCC38540 in liquid medium. AJSR 4(10):376–379 Toca-Herrera JL, Osma JF, Rodríguez Couto S (2007) Potential of solid-state fermentation for laccase production. In: Mendez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formatex, Badajoz, pp 391–400 Upadhye V, Joshi SS (2012) Advances in wastewater treatment–a review. Int J Chem Sci Appl 3:264–268 Vaithanomsat P, Apiwatanapiwat W, Petchoy O, Chedchant J (2010) Decolorization of reactive dye by white-rot fungus Datronia sp. KAPI0039. Kasetsart J Nat Sci 44:879–890 Vasmara C, Cianchetta S, Marchetti R, Galletti S (2015) Biogas production from wheat straw pre-treated with ligninolytic fungi and co-digestion with pig slurry. EEMJ 14(7):1751–1760 Vijayaraghavan J, Basha SS, Jegan J (2013) A review on efficacious methods to decolorize reactive azo dye. JUEE 7:30–47 Vinodha S, Thomas J, Varghese R, Jegathambal P (2013) Decolorization of red CLB dye using membrane bioreactor. Int J Environ Sci 3:1537 Vishwakarma SK, Singh MP, Srivastava AK, Pandey VK (2012) Azo dye (direct blue 14) decolorization by immobilized extracellular enzymes of Pleurotus species. Cell Mol Biol 58:21–25 Wang MX, Zhang QL, Yao SJ (2015) A novel biosorbent formed of marine-derived Penicillium janthinellum mycelial pellets for removing dyes from dye-containing wastewater. Chem Eng J 259:837–844 Waring DR, Hallas G (2013) The chemistry and application of dyes. Plenum Press/Springer US, New York/London, pp 17–47 Water and chemical use in the textile dyeing and finishing industry (1997) Guide produced by the environmental technology best practice programme (GG 62), (1997). UK. http://www.wrap. org.uk/sites/files/wrap/GG062.pdf Won SW, Vijayaraghavan K, Mao J, Kim S, Yun Y-S (2009) Reinforcement of carboxyl groups in the surface of Corynebacterium glutamicum biomass for effective removal of basic dyes. Bioresour Technol 100:6301–6306 Yang XQ, Zhao XX, Liu CY, Zheng Y, Qian SJ (2009) Decolorization of azo, triphenylmethane and anthraquinone dyes by a newly isolated Trametes sp. SQ01 and its laccase. Process Biochem 44(10):1185–1189 Yang S, Hai FI, Nghiem LD, Price WE, Roddick F, Moreira MT, Magram SF (2013) Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour Technol 141:97–108

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Yang J, Lin Q, Ng TB, Ye X, Lin J (2014) Purification and characterization of a novel laccase from Cerrena sp. HYB07 with dye decolorizing ability. PLoS One 9(10):1–13 Yao J, Jia R, Zheng L, Wang B (2013) Rapid decolorization of azo dyes by crude manganese peroxidase from Schizophyllum sp. F17 in solid-state fermentation. Biotechnol Bioproc E 18:868–877 Yaropolov A, Skorobogat’Ko O, Vartanov S, Varfolomeyev S (1994) Laccase. Appl Biochem Biotechnol 49:257–280 Yavuz M, Kaya G, Aytekin Ç (2014) Using Ceriporiopsis subvermispora CZ-3 laccase for indigo carmine decolourization and denim bleaching. Int Biodeter Biodegr 88:199–205 Zhang YZ, Reddy CA (1988) Use of synthetic oligonucleotide probes for identifying ligninase cDNA clones. Methods Enzymol 161:228–237 Zuraida SM, Nurhaslina C, Halim KK (2013) Influence of agitation, pH and temperature on growth and decolorization of batik wastewater by bacteria Lactobacillus delbruckii. IJRRAS 14(2):269–275

Chapter 6

Long-Time Corrosion of Metals and Profiles of Fungi on Their Surface in Outdoor Environments in Lithuania Elena Binkauskienė, Dalia Bučinskienė, and Albinas Lugauskas

6.1 Introduction: Outdoor Corrosion Outdoor corrosion of metals is affected by various environmental factors. The influence of microbial metabolism of the surface led to changes in its chemical and physical characteristics (Krätschmer et al. 2002; De la Fuente et al. 2007; Syed 2008; Videla and Herrera 2009; Lugauskas et al. 2009; Santana et al. 2012). It has recently been deduced, that approximately 40–50% of materials damage in the environment is connected with the activities of microorganisms, while in oil industry this index is up to 77% (Beech and Sunner 2004; Lugauskas et al. 2013). Such a value is determined by the environmental conditions such as temperature fluctuation and exposure to UV light, acidic rains, ozone, wind and the presence in the atmosphere of typical pollutants (SO2, Cl−, NO2, CO2, etc.). The corrosive impact of Lithuanian atmosphere corresponds to the “low” category (Ramanauskas et al. 2005). Growing mycobiota are detected on metals, and the variety of them determines the corrosion behaviour. The products of their activity (acids, alkalis, enzymes) and a variety of other aggressive chemical compounds soon start to contact with the components of the affected object; new chemical compounds are formed, which integrate into the further destruction processes (Lee et al. 2007; Beech and Sunner 2004). The surfaces of metallic constructions or equipment damaged by mycobiota get chapped and exfoliate. Their hardness and lifetime markedly diminish (Ramanauskas et al. 1998, 2000, 2005; Narkevičius et al. 2003). The last decade’s studies of microbial adherence to different substrata led to the conclusion that the survival of microorganisms in the natural habitats is dependent on their capacity to adhere to different surfaces/substrata and to form biofilm, consis ting of various macromolecules organic substances such as proteins, nucleic acids, polysaccharides and lipids. Its macromolecular components contain various anionic E. Binkauskienė (*) • D. Bučinskienė • A. Lugauskas State Research Institute Center for Physical Sciences and Technology, Vilnius, Lithuania e-mail: [email protected] © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_6

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Marine (M) environment Metals

Rural (R) environment Industrial (I) environment Reference (C) environment

Changes of surface of metals

Long-term(up 10 years) exposition Morphological investigations

Elemental analysis

Mass loss (∆m) measurements

Mycobiota identification

Fig. 6.1 Schematic of investigation of the long-term outdoor corrosion

functional groups including carboxyl, sulphate and phosphate groups environment and have extremely heterogeneous nature. The affinity of anionic ligands for multivalent cations, such as Ca2+, can be very strong (Beech and Sunner 2004). The study of effectiveness of selected airborne fungal species on corrosion of solid surface under modelling condition (Lugauskas et al. 2008) by using contemporary technical means was performed: the quartz crystal microbalance sensed microbiological corrosion in situ (Miečinskas et al. 2006), the electrochemical impedance spectroscopy measurements indicated the oxide layer interaction with products of metabolism of microorganisms (Juzeliūnas et al. 2005, 2007), and the difference in consumption and production of microelements has been determined by X-ray fluorescence spectroscopy and X-ray diffraction microscopy (Binkauskiene et al. 2014). We presented the studies about the use of polyaniline as useful coatings for biodegradation effect analysis on mycological treated surface. It was observed that on the biomodified polyaniline surface, biomineralization occur (Binkauskiene et al. 2009, 2013). Figure 6.1 shows schematic of investigations of the long-term outdoor corrosion, which has been systematically studied from 2002 to 2012.

6.1.1 The Total Metal Mass Loss The total metal mass loss (∆m) measurements provided the most reliable indicator of the corrosion behaviour of metals. As seen from Fig. 6.2, corrosion behaviour depends on the type of metals and environments. The highest ∆m values under natural exposure conditions were determined in the marine test site. This is apparently determined by the differences in meteorological factors and atmosphere pollution, especially a higher chlorine ion concentration. Taking into account the

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windiness, it may be stated that the surface of the samples is moistened and dried more often in the marine environment and the corrosion products are washed away more often too.

6.2 The Morphological Investigations 6.2.1 Scanning Electron Microscopy (SEM) Morphology of substrate by SEM method analysed the general appearance of the surface and its changes as a result of corrosion. The data of SEM morphological studies on zinc and copper after 10 years of exposure are given below (Fig. 6.3). SEM imaging has shown that there was no fungal growth detected on reference plate C (exposed to standard room condition HN 69:2003). On zinc exposed to the rural environment tangles of stretching fungi mycelium and a hoard of mineral substances around them were seen (Fig. 6.3a). On the surface exposed to the marine environment, threads of fungi mycelium interspersed into the deposits were observed. On zinc exposed to the industrial environment, Mycelia sterilia as well as Aureobasidium and Candida colonies were identified. In the rural environment, a rich biolayer and separate fragments of biota could be seen.

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Fig. 6.3 SEM images on the surface of (a) zinc and (b) copper after 10 years of exposure to rural (R), marine (M) and industrial (I) environments. Reference sample (C) (From Lugauskas et al. 2015)

Meanwhile a lot of mineralization products on copper exposed in marine and industrial environments could be observed (Fig. 6.3b). It has been reported in many studies that the accumulation of metal by mycobiota cultures is specific. Some mycobiota can also precipitate metals in amorphous and crystalline forms, such as secondary mycogenic minerals (Burford et al. 2006; Gadd et al. 2012; Binkauskienė et al. 2013).

6.2.2 Scanning Probe Microscopy (SPM) The SPM method is used for depths of corrosion measurements. The determined Rz is the maximum height of roughness profile. An evaluation of the corrosion process, variations on ∆m parameter after 1 and 10 years’ exposition and SPM data obtained for steel and aluminium surfaces after 10 years of exposure are presented in Table 6.1 (Lugauskas et al. 2016). The values

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Table 6.1 Variation on ∆m parameter after 1 and 10 years of exposure and SPM data obtained for steel and aluminium surfaces after 10 years of exposure to rural (R), marine (M) and industrial (I) environments Metals Steel

Aluminium

Environments (R) (M) (I) (R) (M) (I)

∆m10, g m−2 733.400 1100.000 569.500 2.207 5.261 2.284

∆m1, g m−2 91.100 189.800 85.700 0.304 0.628 0.300

∆m10/∆m 1 8.050 5.796 6.645 7.260 8.377 7.613

Rz, μm 30.80 >100 61.34 4.56 10.81 3.36

∆m10/Rz, g m−2/μm 23.812 Rhizopus sp. > Aspergillus terreus > Penicillium sp. (Lotfinasabasl et al. 2012). The enzymatic oxidation of petroleum hydrocarbons is the need of the hour as this will result in their degradation, producing nonhazardous products. Laccase oxidizes certain aromatic compounds. Laccase from the white- rot fungus Trametes hirsuta is employed for the oxidation of alkenes (Paavola et al. 1988; Palonen et al. 2003). The schematic representation of various fungi on different types of solid wastes from different sources is presented in Fig. 9.1.

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Fig. 9.1 Schematic representation of the bioremediation of solid wastes

9.10 Disadvantages of Mycoremediation A lot of research is still going on in the area of mycoremediation and thus mycoremediation can be considered to be in the testing phase. More proven techniques in the field of biodegradation by fungi are needed. The conventional remediation technologies are still capturing the faith of the treatment units. They can handle huge amounts of wastes at a time and are considered as fast processes. Mycoremediation in this case would be too slow, and the space required for treatment or storage of materials could be prohibitive. The end users are always in search of technologies which are 100% efficient, whereas the biological systems cannot promise that level of efficiency. Efficiency level of biological systems is never 100% efficient, which is difficult for some end users to understand. The natural systems always face problems with the competitive natural environment in particular area and are also affected by seasonal variations in extreme habitats. Though we are in the plan of commercialization of the technology by fungi, we very well know that the research is still in the experimental phase and also we are not sure of the time it will take. More effort is required in the field of fungal bioremediation to apply the technology to larger-scale projects. We need to improvise ways and means to eliminate the shortcomings that cause hindrances in the potential of mycoremediation. A big legal issue also prevails as many of the fungi and their products and various technologies involving them are patented by one or other scientists. Thus use of the fungi in bioremediation may pose certain legal problems.

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9.11 Conclusion As pollution is one of the burning concerns in the world, we are always in search of a technique to address this problem in a safer way. Mycoremediation is the bioremediation that uses fungi for degradation of the solid wastes from all the fronts of the society, be it industries, hospitals, houses, mines, agriculture, etc. Among the other techniques of waste disposal treatment like chemical, mechanical, biological, etc., we are more interested in the biological methods of treatment. Bioremediation is a treatment that uses naturally occurring organisms to break down hazardous substances into less toxic or nontoxic substances. Among mycoremediation, bacterial bioremediation, and phytoremediation, mycoremediation is attracting the interests of common man because the morphological and genetic qualities of filamentous fungi make them very robust to survive in a wide variety of restrictive conditions and allow them to degrade almost all possible classical and emerging pollutants. Fungi seem to be more efficient in tolerating the extreme environmental conditions like temperature, oxygen, substrate, pH, and the presence of other toxic compounds. Therefore exploration of more effective methods to use mycoremediation is the need of the hour. With the materialization of metagenomics, metatranscriptomics, and metabolomics approaches, bioremediation abilities of different fungi have been well explored and exploited for efficient treatment of wastes. Focusing on the different types of solid wastes in different areas, a huge plethora of fungi has been found to be efficient in the process of biodegradation of these wastes. There are various enzymes like cellulases, laccases, lignocellulases, etc., which are produced by these fungi proving to be an efficient technique to treat solid wastes and converting them to nontoxic substances. The various fungi used till date are immense. To pen down a few of them are as follows: Aspergillus versicolor, Bionectria ochroleuca, Penicillium chermesinum, Trichoderma virens, Aspergillus flavus, Coniophora puteana, Serpula lacrymans, Trametes hirsute, Phanerochaete chrysosporium, etc. The various types of solid waste where mycoremediation has played a vital role are in the area of biomedical, municipal, industrial, mines, electronics, agriculture, etc. Although the area of mycoremediation is proving to be a boon for the bioremediation of solid wastes, it is still in its youth stage and has a number of technical deficiencies to be worked on. An enormous amount of task is still required to make it a 100% efficient process of solid waste treatment.

References Adav SS, Li AA, Manavalan A, Punt P, Sze SK (2010) Quantitative iTRAQ secretome analysis of Aspergillus niger reveals novel hydrolytic enzymes. J Proteome Res 9:3932–3940 Adav SS, Ng CS, Sze SK (2011) iTRAQ-based quantitative proteomic analysis of Thermobifida fusca reveals metabolic pathways of cellulose utilization. J Proteomics 74:2112–2122 Alexandrino AM, Faria H, Souza C, Peralta R (2007) Reutilisation of orange waste for production of lignocellulolytic enzymes by Pleurotus ostreatus (Jack: Fr). Food Sci Technol (Campinas) 27(2):364–368

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Almagro VML, Moreno-Vivián C, Roldán MD (2016) Biodegradation of cyanide wastes from mining and jewellery industries. Curr Opin Biotechnol 38:9–13 Anastasi A, Coppola T, Prigione V, Varese GC (2009) Pyrene degradation and detoxification in soil by a consortium of basidiomycetes isolated from compost: role of laccases and peroxidases. J Hazard Mater 165:1229–1233 Anjum F, Shahid M, Bukhari SA, Potgieter JH (2014) Combined ultrasonic and bioleaching treatment of hospital waste (HW) incinerator bottom ash with simultaneous recovery of selected metals. Environ Technol 35:262–270 Arias J, Delira R, Alarcón A, López M, Barradas O, Sánchez J (2015) Bioleaching of gold, copper and nickel from waste cellular phone PCBs and computer gold finger motherboards by two Aspergillus niger strains. Braz J Microbiol 46(3):707–713 Aust SD (1995) Mechanisms of degradation by white rot fungi. Environ Health Perspect 103(Suppl 5):59–61 Behera SK, Panda PP, Singh S, Pradhan N, Sukla LB, Mishra BK (2011) Study on reaction mechanism of bioleaching of nickel and cobalt from lateritic chromite overburdens. Int Biodeterior Biodegrad 65(7):1035–1042 Casieri L, Anastasi A, Prigione V, Varese GC (2010) Survey of ectomycorrhizal, litter-degrading, and wood-degrading basidiomycetes for dye decolorization and ligninolytic enzyme activity. Antonie Leeuwenhoek 98:483–504 Chivukula M, Renganathan V (1995) Phenolic azo dye oxidation by laccase from Pyricularia oryzae. Appl Environ Microbiol 61:4347–4377 Christopher GJ, Kumar G, Tesema A, Thi N, Kobayashi T, Xu K (2016) Bioremediation for Tanning Industry: A Future Perspective for Zero Emission, Management of Hazardous Wastes. Prof. Hosam El-Din Saleh (ed), InTech, doi: 10.5772/63809. Chapter 6 Cwalina B (2008) Biodeterioration of concrete. Arch Civil Eng Environ 4:133–140 Daft MS, Nicholson TH (1974) Arbuscular mycorrhizas in plants colonizing coal wastes in Scotland. New Phytol 73:1129–1135 Dave SR, Shah MB, Tipre DR (2016) E-Waste: metal pollution threat or metal resource? SOJ Biotechnol 1(1):14 Durrant AJ, Wood DA, Cain RB (1991) Lignocellulose biodegradation by Agaricus bisporus during solid substrate fermentation. J Gen Microbiol 137(75):1–755 Erum S, Ahmed S (2011) Comparison of dye decolorization efficiencies of indigenous fungal isolates. Afr J Biotechnol 10(17):3399–3411 Field JA, Dejong E, Feijoocosta G, Debont JAM (1993) Screening for ligninolytic fungi applicable to the biodegradation of xenobiotics. Trends biotechnol 11:44–49 Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92 Garima T, Singh SP (2014) Application of bioremediation on solid waste management: a review. J Bioremed Biodeg 5:248 Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534 George RP, Ramya S, Ramachandran D, Mudali UK (2013) Studies on biodegradation of normal concrete surfaces by fungus Fusarium sp. Cem Concr Res 47:8–13 Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50:215–242 Inácio F, Ferreira R, Araujo C, Peralta R, Souza C (2015) Production of enzymes and biotransformation of orange waste by Oyster Mushroom, Pleurotus pulmonarius (Fr.) Quél. Adv Microbiol 5:1–8 Jenitta X, Gnanasalomi V, Gnanadoss J (2013) Treatment of leather effluents and waste using fungi. Int J Comput Algorithm 2:294–298 Jové P, Olivella MÀ, Camarero S, Caixach J, Planas C, Cano L, De Las Heras FX (2016) Fungal biodegradation of anthracene-polluted cork: a comparative study. J Environ Sci Health A Tox Hazard Subst Environ Eng 51(1):70–77

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Keri S, Bethan S, Adam GH (2008) Tire rubber recycling and bioremediation: a review. Biorem J 12:1–11 Khan AG (1978) Vesicular-arbuscular mycorrhizas in plants colonizing black wastes from bituminous coal mining in the Illawana Region of New South Wales. New Phytol 81:25–32 Khan R, Gupta AK (2015) Screening and optimization of organic acid producers from mine areas of Chhattisgarh region, India. Int J Curr Microbiol App Sci 4(2):103–111 Kinne M, Zeisig C, Ullrich R, Kayser G, Hammel KE, Hofrichter M (2010) Stepwise oxygenations of toluene and 4-nitrotoluene by a fungal peroxygenase. Biochem Biophys Res Commun 397:18–21 Kolenčík M, Urík M, Čerňanský S, Molnárová M, Matúš P (2013) Leaching of zinc, cadmium, lead and copper from electronic scrap using organic acids and the Aspergillus niger strain. Fresenius Environ Bull 22(12a):3673–3679 Kulshreshtha S, Mathur N, Bhatnagar P (2012) Mycoremediation of paper, pulp and cardboard industrial wastes and pollutants. Fungi Bioremediators 32:77–116 Kumar V, Dhall P, Kumar R, Prakash Singh Y, Kumar A (2012) Bioremediation of agro-based pulp mill effluent by microbial consortium comprising autochthonous bacteria. Scientific World Journal:Article ID127014. https://doi.org/10.1100/2012/127014 Lamar RT, Davis MW, Dietrich DM, Glaser JA (1994) Treatment of a pentachlorophenol- and creosote-contaminated soil using the lignin-degrading fungus Phanerochaete sordida: a field demonstration. Soil Bioil Biochem 26(12):1603–1611 Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH- contaminated samples. Chemosphere 52:1539–1546 Lokhande S, Musaddiq M (2014) Microflora degrading the municipal wastes by fungi. Indian. J Life Sci 4(1):13–16 Lotfinasabasl S, Gunale VR, Rajurkar NS (2012) Assessment of petroleum hydrocarbon degradation from soil and tarball by fungi. Biosci Discov 3(2):186–192 Magan N, Fragoeiro S, Bastos C (2010) Environmental factors and bioremediation of xenobiotics using white rot fungi. Mycobiology 38(4):238–248 Manavalan A, Adav SS, Sze SK (2011) iTRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J Proteomics 75:642–654 Mirizadeh S, Yaghmaei S, Nejad ZG (2014) Biodegradation of cyanide by a new isolated strain under alkaline conditions and optimization by response surface methodology (RSM). J Environ Health Sci Eng 12:85 Mitchell TK, Chilton WS, Daub ME (2002) Biodegradation of the polyketide toxin cercosporin. Appl Environ Microbiol 68(9):4173–4181 Murugesan K (2003) Bioremediation of paper and pulp mill effluents. Indian J Exp Biol. 41(11):1239–1248 Osono T, Takeda H (2002) Comparison of litter decomposing ability among diverse fungi in a cool temperate deciduous forest in Japan. Mycologia 94(3):421–427 Paavola ML, Karhunen E, Salola P, Raunio V (1988) Ligninolytic enzymes of the white-rot fungus Phlebia radiata. Biochem J 254(3):877–884 Palonen H, Saloheimo M, Viikari L, Kruus K (2003) Purification, characterization and sequence analysis of a laccase from the ascomycete Mauginiella sp. Enzyme Microb Technol 33(6):854–862 Pandey A, Gundevia HS (2008) Role of the fungus- Periconiella sp. in destruction of biomedical waste. J Environ Sci Eng 50(3):239–240 Parani K, Rani R, Selvarathi P (2012) Bioremediation of match industry waste by fungal isolates. J Biol Chem Res 29(2):151–158 Parani K, Rani R, Selvarathi P (2015) Bioremediation of match industry waste using fungal isolates and its impact on the growth of Vigna radiata Linn. World J Agr Sci 11(6):331–335 Perfettini JV, Revertegat E, Langomazino N (1991) Evaluation of cement degradation induced by the metabolic products of two fungal strains. Experientia 47:527–533 Pinedo-Rivilla C, Aleu J, Collado I (2009) Pollutants biodegradation by fungi. Curr Org Chem 13:1194–1214

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Raj DD, Mohan B, Shetty BMV (2011) Mushrooms in the remediation of heavy metals from soil. Int J Environ Pollut Control Manag 3(1):89–101 Russell JR, Huang J, Anand P, Kucera K, Sandoval AG, Dantzler KW, Hickman D, Jee J, Kimovec FM, Koppstein D, Marks DH, Mittermiller PA, Núñez SJ, Santiago M, Townes MA, Vishnevetsky M, Williams NE, Vargas MPN, Boulanger L-A, Slack CB, Strobel SA (2011) Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77(17):6076–6084 Sears ME, Volesky B, Neufeld RJ (1984) Ion exchange/complexation of uranyl ion by Rhizopus biosorbent. Biotechnol Bioeng 26:1323–1329 Shafy HI, Mansour M (2016) A review on polycyclic aromatic hydrocarbons: Source, environmental impact, effect on human health and remediation. Egypt J Pet 25(1):107–123 Singh A, Sharma R (2013) Mycoremediation an eco-friendly approach for the degradation of cellulosic wastes from paper industry with the help of cellulases and hemicellulase activity to minimize the industrial pollution. Int J Environ Eng Manag 4(3):199–206 Smith SE, Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Ann Rev Plant Physiol Mol Biol 39:221–244 Sowmya HV, Ramalingappa B, Nayanashree G, Thippeswamy B, Krishnappa M (2015) Polyethylene degradation by fungal consortium. Int J Environ Res 9(3):823–830 Thakur Y, Kumar M, Singh S (2015) Microbial biosorption as a green technology for bioremediation of heavy metals. Res J Pharm Biol Chem Sci 6(3):1717–1724 Verdin A, Sahraoui ALH, Durand R (2004) Degradation of benzo[a]pyrene by mitosporic fungi and extracellular oxidative enzymes. Int Biodeter Biodegr 53:65–70 Viswanath B, Chandra MS, Kumar KP, Pallavi H, Reddy BR (2008) Fungal laccases and their biotechnological applications with special reference to bioremediation dynamic biochemistry. Process Biotechnol Mol Biol 2(1):1–13 Xu TJ, Ramanathan T, Ting YP (2014) Bioleaching of incineration fly ash by Aspergillus niger – precipitation of metallic salt crystals and morphological alteration of the fungus. Biotechnol Rep 3:8–14 Yamada-Onodera K, Mukumoto H, Katsuyaya Y, Saiganji A, Tani Y (2001) Degradation of polyethylene by a fungus, Penicillium simplicissimum YK. Polym Degrad Stab 72:323–327 Yoshizawa S, Tanaka M, Shekdar AV (2004) Global trends in waste generation. In: Gaballah I, Mishar B, Solozabal R, Tanaka M (eds) Recycling, waste treatment and clean technology. TMS Mineral, Metals and Materials publishers, Madrid, pp 1541–52 (II) Zabaniotou AA, Stavropoulos G (2003) Pyrolysis of used automobile tires and residual char utilization. J Anal Appl Pyrolysis 70:711–722 Zafar U, Houlden A, Robson GD (2013) Fungal communities associated with the biodegradation of polyester polyurethane buried under compost at different temperature. Appl Environ Microbiol 79(23):7313–7324

Chapter 10

Mycoremediation: A Step Toward Cleaner Environment Vankayalapati Vijaya Kumar

10.1 Introduction Bioremediation is a waste management technique that uses the organisms to remove or neutralize the pollutants from contaminated sites. Bioremediation is defined as the process whereby organic wastes are biologically degraded under controlled conditions to an innocuous state or the levels below concentration limits established by regulatory authorities. By definition, bioremediation is the use of living organisms, primarily microorganisms, to degrade the environmental contaminants into less toxic forms. It uses naturally occurring microorganisms such as bacteria and fungi or plants to degrade or detoxify substances hazardous to human health and/or the environment. It is a cost-effective method to detoxify the pollutants present in soil. There are different types of bioremediation depending on the organisms used in remediation process. When fungi are used in remediation, it is called mycoremediation, phytoremediation when plants are used, and mycorrhizoremediation when mycorrhizal fungi are used. This chapter reviews mycoremediation, i.e., remediation of contaminated sites using fungi, types of mycoremediation, fungi involved, and advantages of mycoremediation. The environmental pollution is caused mainly by industries and the pesticides used in agriculture. The main soil contaminants belong to the following classes: (a) Polycyclic aromatic hydrocarbons (PAHs), residues arising from the processing of oil, tar, coal, and similar substances. (b) Polychlorinated biphenyls (PCBs). Due to their flame-hindering qualities and thermostability, these are used as transformer cooling agents. They are also V. Vijaya Kumar (*) Core Green Sugar and Fuels Private Limited, Tumkur Village, Shahapur Taluk, Yadgir District 585355, Karnataka, India e-mail: [email protected]; [email protected] © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_10

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present in pesticides and in plastics as a softener, paints, and many other products. (c) Dioxines. They are perhaps the most dangerous of all anthropogenic substance classes. They are by-products of chemical manufacturing and are found in fly ashes from combustion processes. Dioxins and PCBs are very recalcitrant substances for biodegradation due to their aromatic structures and high degree of chlorination (Loske et al. 1990).

10.2 Types of Mycoremediation (Bioremediation) Mycoremediation is of two types: in situ and ex situ remediation. In the first case, the remediation is done at the polluted site, whereas in the second case the soil from the polluted site is excavated and taken to another site for remediation purpose.

10.2.1 In Situ Remediation In situ remediation is done at the polluted site. It is an efficient and cost-effective method. The following are the in situ remediation strategies. 10.2.1.1 Biosparging It involves the injection of air under pressure below the water table to increase groundwater oxygen concentrations and enhance the rate of biological degradation of contaminants by naturally occurring bacteria. 10.2.1.2 Bioventing It uses low air flow rates to provide only enough oxygen to sustain the microbial activity. 10.2.1.3 Bioaugmentation It is the introduction of a group of natural microbial strains which treats contaminated soil or water. It is commonly used in municipal wastewater treatment to restart activated sludge bioreactors.

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10.2.2 Ex Situ Remediation It involves the excavation of contaminated soil from ground. Ex situ remediation is expensive and causes environmental pollution during the transport of pollutant from one site to another. The following are the strategies for ex situ remediation. 10.2.2.1 Land Farming It is a simple technique in which contaminated soil is excavated and spread over a prepared bed and periodically tilled until pollutants are degraded. The goal is to stimulate indigenous biodegradative microorganisms and facilitate their aerobic degradation of contaminants. 10.2.2.2 Composting It is a technique where the contaminated soil is amended with organic materials which support the rich growth of microorganisms and elevated temperature, which is a requisite for composting. 10.2.2.3 Biopiling It is a full-scale technology in which excavated soils are mixed with soil amendments, placed on a treatment area, and bioremediated using forced aeration. The contaminants are reduced to carbon dioxide and water. 10.2.2.4 Bioreactors Slurry reactors or aqueous reactors are used for ex situ treatment of contaminated soil and water pumped up from a contaminated plume. Bioremediation in reactors involves the processing of contaminated solid material (soil, sediment, sludge) or water through an engineered containment system. A slurry bioreactor may be defined as a containment vessel and apparatus used to create a three-phase (solid, liquid, and gas) mixing condition to increase the bioremediation rate of soil-bound and water-soluble pollutants as a water slurry of the contaminated soil and biomass (usually indigenous microorganisms) capable of degrading target contaminants.

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10.3 Fungi Used in Mycoremediation Fungi are unique organisms due to their morphological, physiological, and genetic features. They are omnipresent, able to colonize natural environments (soil, air, water), in which they help in maintaining the ecosystem’s equilibrium. Due to the adaptation to their environment, fungi developed unique bioremediation properties. Practically all natural organic compounds can be degraded by one or more fungal species by the production of enzymes such as amylases, lipases, and proteases that allow them to use substrates as starches, fats, and proteins. Other limited number of species can use pectin, cellulose, and hemicelluloses as carbon sources. Some fungi are the main degraders of natural complex polymers which are resistant to microbial attack, such as keratin, chitin, and lignin. Classification of fungi based on their involvement in remediation process of pollutants is given below: • Ligninolytic fungal degradation • Soil fungal biosorption • Mycorrhizal fungal degradation (Gupta and Srivatsava 2014)

10.3.1 Ligninolytic Fungal Degradation Lignocellulose is a renewable organic material and is the major structural component of all plants. Lignocellulosic wastes are produced in large amounts by many industries including those of forestry, pulp and paper, agriculture, and food. Such wastes are also present in municipal solid waste (MSW) and animal wastes. Lignocellulolytic fungi are classified into three groups: white rots, brown rots, and soft rots (Hickman and Perry 2011). 10.3.1.1 White Rot Fungi (WRF) They belong to Basidiomycota (Agaricomycotina) and in some of the Ascomycota (Xylaricaceae), White rots break down lignin and cellulose and commonly cause rotted wood to feel moist, soft, spongy, or stringy and appear white or yellow. Phanerochaete chrysosporium, Armillaria spp. (Honey mushroom), Pleurotus, and other oyster mushrooms are the examples of WRF. Other WRF include Trametes versicolor (turkey tail), Trametes hirsuta (hairy turkey tail), Ganoderma applanatum (artist’s conk), and Fomes fomentarius (tinder fungus).


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10.3.1.2 Brown Rot Fungi They exclusively belong to Basidiomycota, namely, Agaricomycetes. This class comprises the brown rot fungi belong to Agaricales, Hymenochaetales, Gloeophyllales, and Polyporales. Brown rots mainly decay the cellulose and hemicellulose (carbohydrates) in wood, leaving behind the lignin (brownish wood). Laetiporus sulphureus (sulfur fungus), Serpula lacrymans (True dry rot), Fibroporia vaillantii (mine fungus), Phaeolus schweinitzii, and Fomitopsis pinicola are the examples of BRF. 10.3.1.3 Soft Rot Fungi They belong to Ascomycetes and Fungi imperfecti. Both bacteria and fungi are the source for soft rots. They decay cellulose, hemicellulose, and lignin, in areas directly adjacent to their growth. Growth of soft rots is much slower than brown and white rots and usually do not cause huge structural damage to wood of living trees. Examples of soft rot fungi are Chaetomium, Ceratocystis, and Kretzschmaria deusta.

10.3.2 Soil Fungal Biosorption Extensive studies on the fungi living in soil Mucor sp., Aspergillus carbonarius, Aspergillus niger, Rhizopus sp., Saccharomyces cerevisiae, Botrytis cinerea, Neurospora crassa, Phanerochaete chrysosporium, and Lentinus sajor-caju have shown that they are useful in heavy metal biosorption. The mechanism of biosorption varied from species to species (Kumar et al. 2009).

10.3.3 Mycorrhizal Fungal Degradation Mycorrhizal fungi growing as symbionts with plant roots have the ability to degrade organic pollutants in soil. There are several types of mycorrhizae such as ecto mycorrhiza, ectendomycorrhiza, arbuscular mycorrhiza (AM), ericoid mycorrhiza, arbutoid mycorrhiza, monotropoid mycorrhiza, and orchid mycorrhiza. Ectomy corrhiza, (ECM), arbuscular mycorrhiza (AM), and ericoid mycorrhiza (ERM) can increase the tolerance to heavy metals.

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10.4 Mode of Action of Fungi in Degradation The biodegradation ability/mycoremediation ability of fungi is due to the secretion of extracellular lignocellulolytic enzymes. Lignocellulolytic enzymes are biocatalysts that are responsible for degradation of lignin and cellulosic materials.

10.4.1 Ligninolytic Enzymes They catalyze the breakdown of lignin model compounds; and they fall in two main groups: peroxidases and oxidases. 10.4.1.1 Peroxidases (EC 1.11.1.X) Peroxidases are microsomal or cytosolic secreted enzymes found in all kingdoms of life. They use hydrogen peroxide (H2O2) or organic hydroperoxides (R-OOH) as cosubstrates. Most of the peroxidases are heme proteins having excellent broad substrate spectrum that includes various organic and inorganic compounds (Dunford 1999). They catalyze oxidations resulting in the formation of free radicals (e.g., phenoxyl and aryl cation radicals), reactive cations (e.g., Mn3+), or anions (e.g., OCl–) which help in the destruction of lignin and humic substances, the oxidation of toxic compounds, and non-specific defense reactions (Hofrichter and Ullrich 2010). 10.4.1.2 Oxidases Phenol oxidases (EC 1.10.3) are well-known biocatalysts, which simply need dioxygen (O2) as cofactor (terminal electron acceptor). The important representatives, laccase and tyrosinase, have copper in their active sites and are produced by a variety of fungi such as yeast (e.g., Cryptococcus), molds (e.g., Penicillium), mushrooms (e.g., Agaricus), and white rot fungi (e.g., Pleurotus) (Mikolasch and Schauer 2009). White rot fungi produce lignin-degrading enzymes that catalyze the oxidation of xenobiotics in addition to the degradation of lignin. They consists of peroxidases, laccases, and other enzymes involved in the formation of free radicals, ROS, and H2O2 that cleave the carbon–carbon and carbon–oxygen bonds of the lignin/ xenobiotic by means of a free radical mechanism (Reddy and Mathew 2001). BRF degrade cellulose and hemicelluloses present in wood after only a partial modification of lignin (demethylation, partial oxidation, and depolymerization). Because of the preferential degradation of polymers, the decayed wood loses its inherent strength.


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Mushrooms belong to the family of Basidiomycetes commonly known as macro fungi. They have a characteristic fruiting body consist of a steam (stipe)-bearing cap (pileus) that have the potentiality to bioaccumulate most of heavy metals that are uptaken. Mushrooms can uptake heavy metals from the substrate (soil) by means of substrate mycelia. (Raj et al. 2011).

10.4.2 Cellulolytic Enzymes Cellulolytic enzymes are a group of hydrolytic enzymes responsible for cellulolytic and xylanolytic activities. They are mostly extracellular enzymes produced by various fungi. Fungal cellulolytic enzymes include cellulases (e.g., Trichoderma reesei, Trichoderma sp.), hemicellulases, pectinases (e.g., Rhizopus microsporus), chitinases (Fusarium sp., Lasiodiplodia sp., and Nigrospora sp.), amylases (e.g., Aspergillus niger, Penicillium sp., Chrysosporium sp.), proteases (Penicillium janthinellum), phytases (e.g., Aspergillus niger), mannases (e.g., Aspergillus niger, A. awamori, A. fumigatus, Sclerotium rolfsii, Trichoderma reesei), and xylanases (Trichoderma sp., Penicillium sp., Aspergillus sp., Thermomonospora sp.). By using agricultural wastes as substrate, fungi (e.g., Penicillium strains) produce various extracellular enzymes such as cellulases, mannanases, and pectinases which are useful in the degradation of cellulosic materials. Brown rot fungi produce extracellular compounds able to penetrate deep into the wood cell wall structure and participate in degradation reactions. These compounds break the bond between the fibril structures and depolymerize wood polysaccharides, causing only a limited weight loss at the initial stages of decay, and also they penetrate to cell wall structures along the micropores by breaking the glycosidic bonds of polysaccharides far from the hyphae (Koenigs 1972). The ability of brown rot fungi to produce hydrogen peroxide was demonstrated by Koenigs (1974). According to Fenton’s reaction, the hydrogen peroxide produced by fungi oxidized the two valance transition metals (Fe2+, Mn2+, Co2+). Koenigs (1974) observed that iron concentration in the wood is sufficient for this reaction. Soft rot fungi also degrade wood cell walls forming chains of diamond-shaped cavities that generally follow the orientation of the S2 elementary fibrils causing soft rot. They are known to produce cellulolytic enzymes. Their lignin-degrading ability is variable due to the limitation in the functioning of extracellular peroxidases and oxidases (Cragg et al. 2015).

10.4.3 Biosorption Soil fungi play a vital role in biosorption of heavy metals from aqueous solutions. Biosorption of metal ions primarily occurs by surface binding, including ion- exchange reactions and complexation with the functional groups present on the cell

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surface. Various functional groups believed to be involved in metal binding include carboxyl, amine, hydroxyl, phosphate, and sulfhydryl groups (Kapoor and Viraraghavan 1995).

10.4.4 Mycorrhizoremediation Mycorrhizal fungal degradation is also called as mycorrhizoremediation. This technology is employed for reclamation of soils and sediments that have been polluted by industries through phytoremediation. Arbuscular mycorrhizal fungus (AMF) improves the plant growth in a wide variety of soils by increased phosphorus and micronutrient uptake, makes the plants tolerate biotic and abiotic stresses, and improves the soil structure and aeration by the secretion of glomalin. Mycorrhizal colonization in roots plays a role in protecting the plant root from heavy metals, and the second, which is widely known as the mycorrhizal colonization of roots, increases root surface area for nutrient absorption. Mycorrhizal fungal ecotypes from heavy metal contaminated sites seem to be more tolerant to reference strains from non-contaminated soils. Abundant extrametrical mycelium was shown to be important for HM binding by the fungus. Most of the heavy metals were demonstrated to be bound to cell wall components such as chitin, cellulose, cellulose derivatives, and melanins. The high N and S concentrations associated with polyphosphate granules rather indicate the occurrence of HM-thiolate binding by metallothionein like peptides (Galli et al. 1994).The proteins in the cell walls of AM fungi appear to have the ability to absorb potentially toxic elements by sequestering them. There is evidence that AMF can withstand potentially toxic elements; AMF produce glomalin on hyphae can enhance HM sequester. The extraradical mycelium of AMF is adapted in polluted soil to help in the accumulation of heavy metals both within the plant roots (phytoaccumulation) and extramatrical fungal mycelium. Glomalin plays a vital part in sorption and sequestration of potentially toxic elements, reducing their bioavailability (Joner et al. 2000).

10.5 Degradation of Pollutants by Fungi 10.5.1 Hydrocarbon Degradation Mushrooms with their enzymes are having the ability to degrade a wide variety of environmentally persistent pollutants and transform industrial and agro-industrial wastes into products. Mushroom uses different methods to decontaminate polluted spots and stimulate the environment. These methods include (i) biodegradation, (ii) biosorption, and (iii) bioconversion. The term “biodegradation” is used to describe the ultimate degradation and recycling of complex molecule to its mineral


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constituents. It is the process which leads to complete mineralization of the starting compound to simpler ones like CO2, H2O, NO3, and other inorganic compounds by living organisms. Mushrooms can produce extracellular peroxidases, ligninase (lignin peroxidase, manganese-dependent peroxidase, and laccase), cellulases, pectinases, xylanases, and oxidases (Nyanhongo et al. 2007). These are able to oxidize recalcitrant pollutants in vitro. These enzymes are typically induced by their substrates. The uptake of pollutants/xenobiotics by mushrooms involves a combination of two processes: (i) bioaccumulation, i.e., active metabolism-dependent processes, which include both transport into the cell and partitioning into intracellular components, and (ii) biosorption, i.e., the binding of pollutants to the biomass without requiring metabolic energy. Several chemical processes may be involved in biosorption, including adsorption, ion-exchange processes, and covalent binding. According to Mar’in et al. (1997), the polar groups of proteins, amino acids, lipids, and structural polysaccharides (chitin, chitosan, glucans) may be involved in the process of biosorption. Mushroom varieties such as Armillaria mellea, Polyporus squamosus, and Polyporus sulphureus obtained from East Black Sea Region, are found to accumulate heavy metals like Hg, Pb, Cd, and Cu. Among them Armillaria mellea is shown to accumulate higher concentrations of Hg2+ as the concentration of mercury increases in the soil (Demirbas 2002). Moustafa (2016) conducted experiments for remediation of oil spills by isolating the fungi from oil spill in the Kingdom of Saudi Arabia. Out of the 17 isolates, 7 isolates showed the biodegradation ability. Aspergillus niger, Penicillium decumbens, Lichtheimia ramosa, and Fusarium oxysporum showed the highest degradation ability when screened for changing color of fungal isolates in presence of redox indicator. A moderate ability was observed by Fusarium solani, Penicillium chrysogenum, and Aspergillus flavus. The fungal isolate Lichtheimia ramosa was recorded as a new fungus in oil biodegradation ability. Al-Nasrawi (2012) reported, out of 16 fungal isolates isolated from sand contaminated with oil spill in Gulf of Mexico, 4 isolates have shown biodegradation ability of crude oil. Aspergillus niger has shown the highest degradation ability followed by Penicillium decumbens, Cochliobolus lutanus, and Fusarium solani. Aspergillus niger recorded the highest weight loss of 8.6%, compared to Penicillium decumbens (7.9%), Cochliobolus lunatus (4.7%), and Fusarium solani that strain 421,502 (1.9%). The highest crude oil biodegradation ability of Aspergillus sp. compared to Fusarium sp. and Penicillium sp. isolated from seawater contaminated with oil spill near industrial area was demonstrated by Fathima et al. (2014). Among the three isolates, Aspergillus sp. has shown the highest degradation capacity of 83.12% of hydrocarbons in water followed by Penicillium sp. (75.43%) and Fusarium sp. (69.89%). Decline in BOD was 41.64–49.99% at the end of 25 days. Similarly from the 16 isolates identified from used engine oil-contaminated soils in Tamilnadu, Aspergillus sp. and Rhizopus sp. were predominant. The isolates JJF3 (Aspergillus niger) and JJF9 (Aspergillus luchuensis) have degraded the used engine oil by 40.5% and 51.6%, respectively, in 30 days (Thenmozhi et al. 2013).

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A reduction in nutrient contents of contaminated soils after introduction of the white rot fungi (Pleurotus pulmonarius Fries (Quelet)) at higher levels of 20–40% crude oil and palm kernel sludge concentrations was observed compared to lower levels of the contaminant in a study conducted by Adenipekun and Lawal (2011) in crude oil-contaminated soil and palm kernel sludge in the soil. A decrease in the heavy metal contents was observed at all level of crude oil contamination except Pb which increased at 5% and 20% crude oil contamination. Agaricus campestris significantly reduced the total petroleum hydrocarbons from 2744.72 mg/l in control to 503.08 mg/l in the contaminated minimal salt solution (Adongbede and Sanni 2014). Washington State Department of Transportation invited different groups with bioremediation ideas to try them out on heavy oil-contaminated soil from a truck yard. While other treatments failed to yield impressive results, the berm inoculated with P. ostreatus was covered in mushrooms as large as 12 inch in diameter after 4 weeks. Ninety-five percent of the PAHs were removed in this time, and the mushrooms did not contain petroleum products. After the fungi used up the available food, a successional regrowth began as flies, then birds, and then seedlings of new plants recolonized the berm. The experimenters hypothesize that the fungi could be a keystone organism in restructuring PAH-contaminated areas. These same kinds of fungi were utilized again to help mop up oil washing up in San Francisco Bay after the tanker Cosco Busan spilled 60,000 gallons in 2007. The oil was soaked up from the shores using an innovative, highly absorbent mat made of human hair. Spores were introduced to the soaked mats and turned the entire product into carbon dioxide, water, and innocuous compost (Stamets 2010).

10.5.2 PAH Degradation Stropharia rugosoannulata was found to be the most efficient strain of basidiomycete for the removal of a variety of PAHs (anthracene, pyrene and benzo(a)pyrene), doing away with over 85% of them within 6 weeks in experimental culture. These results occurred with the addition of manganese (II) to the culture; without this addition, performance was much lower. This shows that manganese peroxidase, one of the extracellular ligninolytic enzymes, is an important component of the degradation that S. rugosoannulata performs (Steffen et al. 2002). Earthworms and spent fungal mycelia of Pleurotus sajor-caju has removed the PAHs (anthracene, phenanthrene, benzo α pyrene) by 99.99% in 30 days in a mycoremediation experiment conducted by Azizi et al. (2013) using PAH and sewage sludge mixture. A wide variety of fungi have evolved effective mechanisms to attack specific PAHs. One reason for this ability lies in the similarity between lignin, a long, aromatic family of molecules that is present in wood and PAHs. Lignin is one of the main components of woody tissue in all vascular plants along with cellulose and hemicellulose. It has been described as the cement in woody tissue that adds strength and flexibility to cellulose. This is the substance that gives trees the strength to grow


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taller toward the light and provides the crunchiness to vegetables (McCrady 1991). Fungi produce extracellular oxidative enzymes which completely mineralize lignin and carbohydtate components of wood to carbon dioxide and water. Since lignin is comprised of many different aromatic rings in long varied chains, the fungal enzymes for mineralization are non-specific and frequently can also mineralize PAHs (Mai et al. 2004).

10.5.3 Nitroaromatic Degradation Nitroaromatics have very few naturally occurring species. However, due to their increased synthesis and use over the past century, they have become a common contaminant in the environment. Among the synthetic nitroaromatics, trinitrotoluene (TNT) is the most widely spread contaminant, especially in areas surrounding current and former ammunitions and explosives production plants. 1-Hexahydro-1,3, 5- trinitro-1,3,5-triazine (RDX) and 2,4-dinitrotoluene (2,4-DNT) are also major environmental contaminants due to their use in explosives and polyurethane synthesis. Under ligninolytic conditions, the white rot basidiomycete Phanerochaete chrysosporium mineralizes 2,4-dinitrotoluene (I). The pathway for the degradation of I was elucidated by the characterization of fungal metabolites and oxidation products generated by lignin peroxidase (LiP), manganese peroxidase (MnP), and crude intracellular cell extracts (Valli et al. 1992). In different nutrient starvation conditions (carbon, nitrogen, or sulfur limitations), Phanerochaete chrysosporium favored TNT and other xenobiotic attacks. These reactions were carried out by secreted enzymes of the lignin-degrading system. This system contains lignin peroxidase, manganese peroxidase (MnP), oxidases, reductases, hydrogen peroxidase, veratryl alcohol, oxalate, and quinol oxidases. Stahl and Aust (1993a, b) provided evidence that TNT is reduced by a plasma membrane redox system in P. chrysosporium that requires live and intact mycelia. Any conditions that disrupt the integrity of the plasma membrane destroy the reductase activity. The presence of compounds known to inhibit the membrane redox systems also inhibits TNT reductase (Stahl and Aust 1993a, b).

10.5.4 Chlorinated Aromatic Compounds Degradation Chlorinated aromatic compound degradation includes chlorinated alkanes and alkenes (e.g., trichloroethylene, perchloroethylene), polychlorinated biphenyls, phenoxyalkanoic herbicides (e.g., 2,4-dichlorophenoxyacetic acid (2,4-D), 2,4,5-trichlorophenoxyacetic acid (2,4,5-T)), triazine herbicides (e.g., atrazine), chlorinated dioxins (e.g., polychlorinated dibenzodioxins), chlorobenzenes (e.g., monochlorobenzene, 1,2,3-trichlorobenzene, 1,2,4,-trichlorobenzene, etc.), and chlorinated insecticides (e.g., lindane, DDT).

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The fungi that degrade the above pollutants are Phanerochaete chrysosporium, T. versicolor, Irpex lacteus and Ganoderma lucidum (Marco-Urrea et al. (2008a), P. ostreatus (Kubatova et al. 2001), Dichomitus squalens (Reddy et al. 1997), Pleurotus pulmonarius (Masaphy et al.1996), Phlebia lindtneri (Kamei and Kondo 2005), Trametes versicolor (Marco-Urreaet al. 2008b), Gloeophyllum trabeum, Fomitopsis pinicola, and Daedalea dickinsii (Purnomo et al. 2008). Phanerochaete chrysosporium is demonstrated to degrade all the types of the above chlorinated aromatic compounds.

10.5.5 Dyes Degradation Coomassie Brilliant Blue (CBB), the dye used in textile industry, was degraded by the fungus Aspergillus sp. When the fungus was grown in the petri plates containing the medium supplemented with CBB, it has shown the blue color disappeared in the petri plate and observed the clear zone around mycelium. Initially the color around the mycelium turned yellow and later it became clear. The fungus adsorbed color in its mycelium as is evident from the blue color of the mycelium (Aditee et al. 2014). Muthezhilan et al. (2008) isolated and screened 13 fungal isolates under 17 genera and screened for their decolorization against methylene blue, gentian violet, crystal violet, cotton blue, sudan black, malachite green, methyl red, and carbol fuchin in mineral salt medium and Czapek-Dox broth. Aspergillus ochraceus, A. terreus, A. niger, Penicillium citrinum, and Fusarium moniliforme has decolorized maximum number of dyes in both solid and liquid media, whereas Mucor racemosus, Cladosporium cladosporioides, Penicillium oxalicum, and Trichoderma viride did not show any color reduction in solid medium and showed very little color reduction in liquid medium.

10.5.6 Herbicide Degradation The glyphosate degradation fungi were isolated from 11 cultivated soils (Riyadh and Karj area, KSA) after enriching with minimal salt media supplemented with Glyphosate. The glyphosate concentration was tested from 500 ppm to 10,000 ppm. Some fungal isolates tolerated glyphosate up to 10,000 ppm. Glyphosate disappeared rapidly in liquid Czapek-Dox medium containing 1% sucrose by Aspergillus flavus WDCZ2 (99.6%) and Penicillium spiculisporus ASP5 (95.7%) followed by P. verruculosum WGP1 (90.8%). However, glyphosate almost disappeared in Penicillium spinulosumASP3 (98.8%), Penicillium spiculisporus ASP5 (98.1%), and Aspergillus tamarii PDCZ1 (96.7%) followed by Aspergillus flavus WDCZ2 (90.6%) (Eman et al.2013). The degradation pathway of glyphosate produces the major metabolite aminomethylphosphonic acid (AMPA) and ultimately leads to the production of water, carbon dioxide, and phosphate (Forlani et al. 1999).


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10.5.7 Insecticide Degradation The biodegradation ability of the two fungi Trichoderma longibrachiatum and Aspergillus oryzae isolated from pesticide-contaminated soils were tested with insecticide imidacloprid (20 ppm) either singly or as a consortium by Gangola et al. 2015 by immobilized culture in alginate and agar disks and also amending organic wastes on biodegradation of imidacloprid in soil. In sodium alginate beads, after 15 days they observed that the maximum imidacloprid degradation was in consortium (95%) followed by FII (78%), FIII (76%), and control (15%). In agar disks after 15 days maximum degradation was observed in consortium (97%) followed by FII (84%), FIII (79%), and control (18%). Highest degradation was found in consortium amended with bagasse (99%) followed by consortium amended with hen manure (94%) and consortium amended with farmyard manure (91%). ITS regions of the two fungal isolates, i.e., FII and FIII, showed 100% similarity with Aspergillus oryzae and Trichoderma longibrachiatum, respectively.

10.5.8 Mycorrhizoremediation Inoculation of AM fungus (Rhizophagus fasciculatus) along with 25% mine spoil boosted the growth and development of Setaria italica (L.) Beauv. (foxtail millet) and grain yield per panicle when compared to remaining treatments (50%, 75%, 90%, 100% mine spoil). Shoot length, root length, fresh weight of shoot, root, percentage of mycorrhizal colonization, and mycorrhizal spore number/25 g were increased in 25% of mine spoil treatment compared to the other treatments (Lakshman 2013). When alfalfa inoculated with mycorrhiza in soils containing low and high levels of zinc and lead, the more accumulation of lead was observed in the roots of alfalfa, whereas more uptake of zinc was observed in the shoots also. This may be due to the high mobility of Zn compared to lead. These results indicate that mycorrhiza can effectively accumulate lead in the roots of alfalfa. The aerial parts of the plants can be used as a fodder, avoiding lead reaching into the food chain (Ebrahimi et al. 2014). By using radiolabeled atrazine, Donnelly et al. (1993) showed that ericoid mycorrhizal fungus, Hymenoscyphus ericae 1318, degraded atrazine, and relatively high levels of atrazine carbon were incorporated into its tissue. In general, as the nitrogen concentration increased, the extent of atrazine degradation increased.

10.6 Advantages of Bioremediation (Mycoremediation) Bioremediation is a natural and cost-effective method of remediation process. In many cases the pollutants are completely degraded to harmless products such as water, carbon dioxide, and cell biomass. Complete destruction of the target

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pollutant can be achieved. This can be performed onsite avoiding the need to transport the pollutant to other sites for remediation, thus avoiding risks during transportation and health hazards. This is a low-cost eco-friendly technology. The limitations of this technology are as follows: it is a slow process; this is effective only for biodegradable contaminants; not all the contaminants are biodegradable; sometimes the degradation products are more toxic and persistent than the parent compound; it is difficult to extrapolate from lab to pilot scale to field level; it may take longer time than other treatments such as incineration; and all the envi ronmental conditions are to be maintained and closely monitored. (Gnanasalomi et al. 2013; Sharma 2012; Vidali 2001).

10.7 Conclusion and Future Prospects Mycoremediation is the oldest technique in remediation of polluted soils. It is not practiced regularly due to the lack of awareness on mycoremediation methods. The enzymes secreted by mushrooms are non-specific to any substrate; due to this they have the ability to degrade a wide variety of pollutants. Mycorrhizal fungi (AMF) help in adoption of plants at polluted sites. Soil fungi show adoptability in a wide range of polluted soils and degrade pollutants. The availability of inoculum is another constraint in adapting mycoremediation at field level in large scale. By adapting fungi for remediation of various polluted environments, the contamination of water through runoff and entering of pollutants into the food chain can be prevented, and cleaner environment can be passed on to the future generation. Solid waste management program are being taken up in many municipalities and villages in India, generating compost, making the cities cleaner. There is a need to focus degradation of plastics which is the major pollutant in the environment. By using the consortia of different fungi, it is possible to reclaim soils contaminated with different pollutants at the same site, and cleaner and greener environment can be passed on to future generations. Acknowledgments The author is thankful to the management of Core Green Sugar and Fuels Pvt. Ltd., for giving an opportunity and encouragement in preparation of this chapter.

References Adenipekun CO, Lawal Y (2011) Mycoremediation of crude oil and palm kernel contaminated soils by Pleurotus pulmonarius Fries (Quelet). Nature and Science 9(9):125–131 Aditee J, Bharti D, Meenaxi P (2014) Mycoremediation of Coomassie brilliant blue by Aspergillus spp. Biotechnol 10(24):15567–15571


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Adongbede EM, Sanni RO (2014) Biodegradation of engine oil by Agaricus campestris (a white rot fungus). J Bioremed Biodegr 5:262. https://doi.org/10.4172/2155-6199.1000262 Al-Nasrawi H (2012) Biodegradation of crude oil by fungi isolated from Gulf of Mexico. J Bioremed Biodegr 3:147. https://doi.org/10.4172/2155-6199.1000147 Azizi AB, Liew KY, Noor ZM, Abdullah N (2013) Vermiremediation and mycoremediation of polycyclic aromatic hydrocarbons in soil and sewage sludge mixture: a comparative study. Int J Environ Sci Dev 4(5):565–568 Cragg SM, Beckham GT, Bruce NC, Bugg TDH, Distel DL, Dupree P, Etxabe AG, Goodell BS, Jellison J, McGeehan JE, McQueen-Mason SJ, Schnorr K, Walton PH, Watts JEM, Zimmer M (2015) Lignocellulose degradation mechanisms across the tree of life. Curr Opin Chem Biol 29:108–119 Demirbas A (2002) Metal ion uptake by mushrooms from natural and artificially enriched soils. Food Chem 78:89–93 Donnelly PK, Entry JA, Crawford DL (1993) Degradation of atrazine and 2, 4-dichlorophenoxyacetic acid by mycorrhizal fungi at three nitrogen concentrations in vitro. Appl Environ Microbiol 59:2642–2647 Dunford HB (1999) Heme peroxidases. John Wiley, New York Ebrahimi H, Moshiri F, Ardakani MR, Yeganeh M, Rejali F (2014) Agronomic properties of alfalfa as affected by Pb and Zn using rhizobox system and assessing its ability for phytoremediation purposes. Int J Agric Innov Res 2(6):1065–1070 Eman A, Abdel-Megeed A, Suliman AMA, Sadik MW, Sholkamy EN (2013) Biodegradation of glyphosate by fungal strains isolated from herbicides polluted -soils in Riyadh area. Int J Curr Microbiol App Sci 2(8):359–381 Fathima BS, Bardhan SK, Raj Mohan B (2014) Bioremediation of sea water contaminated with crude oil by fungi. Int J Renew Energy Environ Eng 2(04):301–303 Forlani G, Mangiagalli A, Nielsen E, Suardi CM (1999) Degradation of the phosphonate herbicide glyphosate in soil: evidence for a possible involvement of unculturable microorganisms. Soil Biol Biochem 31:991–997 Galli U, Schuepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92(2):364–368 Gangola S, Pankaj KP, Sharma A (2015) Mycoremediation of Imidaclopridin the presence of different soil amendments using Trichoderma longibrachiatum and Aspergillus oryzae isolated from pesticide contaminated agricultural fields of Uttarakhand. J Bioremed Biodegr 6:310. https://doi.org/10.4172/2155-6199.1000310 Gnanasalomi VDV, Jebapriya GR, Gnanadoss JJ (2013) Bioremediation of hazardous pollutants using fungi. Int J Comput Algorithm 2:273–278 Gupta M, Srivatsava S (2014) Mycoremediation: a management tool for removal of pollutants from environment. Indian. J Appl Res 4:289–291 Hickman GW, Perry EJ (2011) Wood decay fungi in landscape trees. University of California, p 4. UC ANR Publication 74109. http://www.ipm.ucdavis.edu/PMG/PESTNOTES/ Hofrichter M, Ullrich R (2010) New trends in fungal biooxidation. In: Hofrichter M (ed) The mycota X. Industrial applications. Springer, Berlin/Heidelberg, pp 425–449 Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234 Kamei I, Kondo R (2005) Biotransformation of dichloro-, trichloro-, and tetrachlorodibenzo-p- dioxin by the white rot fungus Phlebia lindtneri. Appl Microbiol Biotechnol 68:560–566 Kapoor A, Viraraghavan T (1995) Fungal biosorption- an alternative treatment option for heavy metal bearing wastewaters: a review. Bioresour Technol 53:195–206 Kishore Kumar K, Krishna Prasad M, Sarma GVS, Murthy CVR (2009) Removal of Cd (II) from aqueous solution using immobilized Rhizomucor tauricus. J Microbial Biochem Technol 01(01):015–021 Koenigs JW (1972) Effect of hydrogen peroxide on cellulose and its susceptibility to cellulase. Mater Org 7:133–147

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Koenigs JW (1974) Production of hydrogen peroxide by wood-rotting fungi in wood and its correlation with weight loss, depolymerization, and pH changes. Arch Microbiol 99:129–145. https://doi.org/10.1007/BF00696229 Kubatova A, Erbanova P, Eichlerova I, Homolka L, Nerud F, Sasek V (2001) PCB congener selective biodegradation by the white rot fungus Pleurotus ostreatus in contaminated soil. Chemosphere 43:207–215 Lakshman HC, Channabasava A (2013) Mycorrhizoremediation of mine spoil by using foxtail millet inoculated with Rhizophagus fasciculatus: an ex-situ solid waste management. Int J Curr Sci 8:E 85–E 92 Loske D, Huttermann A, Majcherczyk A, Zadrazil F, Lorsen H, Waldinger P (1990) Use of white-rot fungi for the clean-up of contaminated sites. In: Coughlan MP, Amaral Collaco MT (eds) Advances in biological treatment of lignocellulosic materials. Elsevier, London, pp 311–322 Mai C, Schormann W, Majcherczyk A, Hutterman A (2004) Degradation of acrylic copolymers by white-rot fungi. Appl Microbiol Biotechnol 65:479–487 Marco-Urrea E, Gabarrell X, Caminal G, Vicent T, Reddy CA (2008a) Aerobic degradation by white rot fungi of trichloroethylene (TCE) and mixtures of TCE and perchloroethylene (PCE). J Chem Technol Biotechnol 83:1190–1196 Marco-Urrea E, Parella T, Gabarrell X, Caminal G, Vicent T, Adinarayana Reddy C (2008b) Mechanistics of trichloroethylene mineralization by the white rot fungus Trametes versicolor. Chemosphere 70:404–410 Mar'in A, Conti C, Gobbi G (1997) Sorption of lead and caesium by mushrooms grown in natural conditions. Resour Environ Biotechnol 2:35–49 Masaphy S, Henis Y, Levanon D (1996) Manganese-enhanced biotransformation of atrazine by the white rot fungus Pleurotus pulmonarius and its correlation with oxidation activity. Appl Environ Microbiol 62(10):3587–3593 McCrady E (1991) The nature of lignin. At http://cool.conservation–us.org/byorg/abbey/ap/ ap04-4/ap04-402.html Mikolasch A, Schauer F (2009) Fungal laccases as tools for the synthesis of new hybrid molecules and biomaterials. Appl Microbiol Biotechnol 82:605–624 Moustafa AM (2016) Bioremediation of oil spill in Kingdom of Saudi Arabia by using fungi isolated from polluted soils. Int J Curr Microbiol App Sci 5(5):680–691 Muthezhilan R, Yogananth N, Vidhya S, Jayalakshmi S (2008) Dye degrading microflora from industrial effluents. Res J Microbiol 3:204–208 Nyanhongo GS, Gübitz G, Sukyai P, Leitner C, Haltrich D, Ludwig R (2007) Oxidoreductases from Trametes spp. in biotechnology: a wealth of catalytic activity. Food Technol Biotechnol 45:250–268 Purnomo AS, Kamei I, Kondo R (2008) Degradation of 1, 1, 1-trichloro-2, 2-bis (4-chlorophenyl) ethane (DDT) by brown-rot fungi. J Biosci Bioeng 105:614–621 Raj DD, Mohan B, Vidya Shetty BM (2011) Mushrooms in the remediation of heavy metals from soil. Int J Environ Pollut Control Manag 3:89–101 Reddy A, Mathew Z (2001) Bioremediation potential of white rot fungi. In: Gadd GM (ed) Fungi in bioremediation. Cambridge University Press, Cambridge, UK, pp 52–78 Reddy GVB, Joshi DK, Gold M (1997) Degradation of chlorophenoxyacetic acids by the lignin degrading fungus Dichomitus squalens. Microbiology 143:2353–2360 Sharma S (2012) Bioremediation: features, strategies and applications. Asian J Pharm Life Sci 2:202–213 Stahl JD, Aust SD (1993a) Plasma membrane dependent reduction of 2,4,6-trinitrotoluene by Phanerochaete chrysosporium. Biochem Biophys Res Commun 192:471–476 Stahl JD, Aust SD (1993b) Metabolism and detoxification of TNT by Phanerochaete chrysosporium. Biochem Biophys Res Commun 192(2):477–482 Stamets P (2010) The petroleum problem. http://www.fungi.com/mycotech/petroleum_problem


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Steffen KT, Hatakka A, Hofrichter M (2002) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60: 212–217 Thenmozhi R, Arumugam K, Nagasathya A, Thajuddin N, Paneerselvam A (2013) Studies on mycoremediation of used engine oil contaminated soil samples. Adv Appl Sci Res 4(2): 110–118 Valli K, Brock BJ, Joshi DK, Gold MH (1992) Degradation of 2,4-dinitrotoluene by the lignin- degrading fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58(1):221–228 Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73(7):1163–1172

Chapter 11

Arbuscular Mycorrhizal Fungi Provide Complementary Characteristics that Improve Plant Tolerance to Drought and Salinity: Date Palm as Model Ahmed Qaddoury

11.1 Introduction One of the main challenges for the sustainable management of agricultural lands is the combination of the proper use of plant biotechnologies and the management of soil microorganisms as providers of key ecological services that has been at the forefront of generating and promoting sustainable agricultural production. These organisms, often referred to as “ecosystem engineers,” “biocontrol agents,” “biofertilizers,” or “bioenhancers,” can participate in improving plant growth and nutrition, strengthening plant performance, restoring ecosystems, and combating pests and pollution. The most important providers of these ecological services are arbuscular mycorrhizal fungi (AMF) which can form symbiotic associations (mycorrhizas) with roots of 90% of terrestrial plant species including trees, shrubs, herbs, and crop plants (Smith and Read 2008). Mycorrhizas are highly evolved mutualistic associations formed between soilborne fungi and plant roots. Once established, AM symbiosis is known to benefit mineral nutrition and to provide enhanced water relations thereby enhancing host plant protection against the detrimental effects of environmental constraints (Davies et al. 1992). In exchange, the plants supply mycorrhizal fungi with carbon (20– 25%) fixed using photosynthetic process. Several studies have clearly highlighted the fundamental role that mycorrhizal fungi play at the interface between the soil and plant roots, enhancing thereby the multitrophic and protective interactions that affect productivity, competitiveness, and survival of the majority of plant species both in natural ecosystems and in managed fields. It’s now widely established that AM symbiosis significantly increases plant growth and water and nutrient uptake (Faghire et al. 2010; Baslam et al. 2014; Fouad et al. 2013; Fouad et al. 2014; Fouad A. Qaddoury (*) Plant Biotechnology & Agrophysiology of Symbiosis, Department of Biology, FST, University Cadi Ayyad, Marrakesh, Morocco e-mail: [email protected] © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_11

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2015; Benhiba et al. 2015; Essahibi et al. 2016), produces plant growth hormones, alters physiological and biochemical properties of the host, and strengthens root defense against soilborne pathogens (Dehne 1986; Smith and Read 1997). In addition, the integration of performing AMF in plantlet production cycles improved water-absorption capacity, osmotic balance, and composition of carbohydrates of the host plants (Ruiz-Lozano 2003; Fouad et al. 2014; Essahibi et al. 2016), reducing thereby the acclimatization period and improving the success of transplantation in several horticultural and forestry species (Fouad et al. 2014; Fouad 2015; Essahibi et al. 2016). Thus, inoculation with carefully selected AM fungi, having efficient adaptive tolerance to abiotic stresses, has resulted in conferring required growth and nutrition and physiological status to adapt in arid soils (Liddycoat et al. 2009). Moreover, AMF are key factors of the belowground network essential to safeguard soil agroecological performances, soil function, soil fertility, and soil stability. The fungal mycelium that extends from the mycorrhizal roots forms a three-dimensional network linking the roots and the soil environment beyond the nutrient depletion zone. It constitutes an efficient system for water and nutrient uptake (particularly P) and scavenging nutrient-poor conditions. The mycelium also contributes to the formation of water-stable aggregates necessary for good soil quality (Jeffries and Barea 2000). Regarding all of these benefits, AM symbiosis may provide an alternative strategy to increase crop stress tolerance and consequently promote sustainable food and feed production in extreme environmental conditions. However, occurrence and functionality and performance of AM fungal species have been reported dependent on soil properties, on host and fungi species, and on specific plant-soil- fungi combinations (Johnson et al. 1992). This chapter covers the occurrence of AM symbiosis and gives insight on their benefits to host plant and soil quality in agroecosystem context. It also examines the literature relating to the effectiveness of AMF in alleviating detrimental effects of water scarcity and salinity conferring efficient adaptive tolerance to abiotic stresses. Finally, an overview of most persuasive and effective applications of arbuscular mycorrhizal fungi in improving date palm performance in terms of growth, n utrition, and protection against adverse effects of environmental stresses is highlighted.

11.2 Occurrence of Mycorrhizal Fungi Soil fungi interact with plant root with different degrees of dependency. The most interesting, however, are specific beneficial symbiotic associations. More than 90% of terrestrial plants are associated with root-colonizing fungi, establishing a permanent and intimate mutual beneficial symbiosis, called mycorrhiza. The term “mycorrhiza” originates from the Greek “mycos” meaning fungus and “rhiza” meaning root. It was first used by Frank (1885) to describe the intimate mutual association between mycorrhizal fungi and plant roots, where the host plant receives mineral nutrients while the heterotrophic fungus obtains carbon compounds from the host.

11 Arbuscular Mycorrhizal Fungi Provide Complementary Characteristics that…

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Mycorrhizal fungi, which exist everywhere from tiny home gardens to large e cosystems (Wang and Qiu 2006; Helgason and Fitter 2009), are able to associate with about 90% of plant species, making this association the most ubiquitous and abundant terrestrial symbiosis. Several types of mycorrhizae exist, defined by plant/ fungus combination and symbiotic structure. The way the hyphae of the fungi are arranged within the cortical tissues of the root is the basis for grouping them into two major groups: ectomycorrhizae and endomycorrhizae. The term endomycorrhiza is generally used for all mycorrhizal types in which the fungus grows inside root cortical cells, but neither the fungal cell wall nor the host cell membrane are breached (Peterson et al. 2004). As the fungus grows, the host cell membrane invaginates and envelops the fungus, creating an apoplastic space that prevents direct contact between the plant and fungal cytoplasm and facilitates efficient transfer of nutrients between the symbionts. According to the characteristics of this latest structure, the endomycorrhizae group is further divided into ericoid, arbutoid, monotropoid, orchid, and the large group of arbuscular mycorrhizae (Peterson et al. 2004). Arbuscular mycorrhizae (AM) is the most common type, occurring in about 80% of plant species including agricultural crops such as cereals, vegetables, and horticultural plants. AM symbiosis can be found in almost all ecosystems. They have been described from deserts (Zhang et al. 2012), tropical rainforests (Zhao et al. 2001), contaminated soils (Khan 2005), as well as from ecosystems with strong saline soil (Carvalho et al. 2001). AM fungi have existed and supported plants since terrestrial plants evolved; fossil evidence (Remy et al. 1994) and DNA sequence analyses (Simon et al. 1993) suggest that this mutualism appeared 400–460 million years ago when first terrestrial plant started colonizing land (Prasad et al. 2017). The fact that the first land plants were already associated with fungi resembling the Glomeromycota (Remy et al. 1994; Redecker et al. 2000) is tempting to hypothesize that AMF assistance in water or mineral element acquisition was a prerequisite for plant colonization of land masses, since those early land plants did not have a true functional root system. Land plants have then evolved to organisms with highly diversified adaptations to almost all terrestrial habitats (Morton 1990; Pirozynski and Malloch 1975). The close relationship of AM fungi with their host plants is mirrored by their obligatory biotrophic status: they need a living host for carbon supply during their entire life cycle, having so far been unculturable in the absence of their host (Hepper 1985). As a result, AM fungi have evolved only with their plant hosts since they appeared on land. Most AMF produce spores able to germinate and grow in response to favorable edaphic and environmental conditions in the absence of host root, but are unable to complete their life cycle without establishing a functional symbiosis with a host plant (Mosse 1959; Hepper 1985). Their growth is therefore limited to a relatively short time (20–30 days) after which many modifications in fungal morphology point to a cessation of hyphal growth. During this asymbiotic phase, the fungus lives mainly on its triacylglyceride reserves. In the absence of signals from the plant root, spores germinate but show limited hyphal development (Requena et al. 2001). To overcome their obligate biotrophic status, AMF have developed

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multiple survival strategies allowing germinating spores to cope with the absence of growing host root (Mosse 1959; Koske 1992). The first survival strategy is represented by the ability of AMF to colonize a wide range (90%) of land plant species, increasing thereby the probability of germinated spores to come into contact and colonize host roots. The second evolutionary mechanism is the ability of the AMF spores to germinate several times (multiple germination ability) by producing successive germ tubes when those formed previously are severed from the parent spores because of the lack of growing root (Koske 1992). This capacity was described in spores of a Glomus sp. (Mosse 1959), and in G. gigantea, whose spores were able to germinate up to ten times over a period of 50 days (Koske 1992). The establishment of AM symbiosis begins with the colonization of a compatible root by the hyphae produced by AM fungal soil propagules, asexual spores, or mycorrhizal roots (Requena et al. 2001). The presence of growing plant root allows development of vegetative mycelium, which, under favorable conditions, can colonize 60–90% of the total length of the root system (Becard and Piche 1989; Bonfante and Bianciotto 1995). In the contact of plant root, AM fungi enter host tissues between the epidermal cells and form a hyphopodium in the first cell layers. This stage marks the autotrophic growth of the fungus. Then, hyphae grow first through the intercellular spaces and then enter the root tissues spreading between and through cells of the cortical root layers (Gianinazzi-Pearson and Gianinazzi 1989). Reaching the inner cortex, they penetrate the cell wall and grow into the apoplast between cell wall and plasma membrane; fungal hyphae extensively ramify to form treelike structures called “arbuscules.” These highly branched hyphae are closely surrounded by the host plasmalemma and represent a large surface of cellular contact facilitating the exchange of metabolites between both symbionts (Smith and Gianinazzi-Pearson 1988). Some AM fungi form other structure, vesicles, considered as storage organs (Walker 1995). As internal colonization spreads, the extraradical mycelium of the fungus ramifies and grows along the root surface forming more penetration points and into the surrounding soil developing an extensive tridimensional network of mycelium exploring the environment for mineral nutrients and roots of other plants (Smith and Read 2008). The length of the external hyphae growing in soil associated with mycorrhizal roots reaches an average of up to 10–14 m cm−1 root (Smith and Gianinazzi-Pearson 1988), increasing the root absorbing surface area 100- or even 1000-fold (Larcher 1995; Barea et al. 2011). This mycelial network can bridge over the zone of nutrient depletion around roots to absorb low-mobile ions from the bulk soil. In return host plant provides the fungus with sugars, amino acids, and vitamins essential for its growth (Harley and Smith 1983). The fungal life cycle is completed after formation of asexual chlamydospores on the external mycelium. Arbuscular mycorrhizal fungi are multifunctional microorganisms with myriads of ecosystem benefits. The extraradical hyphae network of the fungi permeates into the microsites of rocks and soils surrounding the plant roots, increasing the root absorbing surface area 100- or even 1000-fold (Larcher 1995; Barea et al. 2011). Therefore, AMF increase plants’ nutrient and water relations (Baslalm et al. 2014; Fouad et al. 2014) improve thereby plants’ field survival and establishment


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(Ouahmane et al. 2006; Manaut et al. 2015). Moreover, AMF improve soil agroecological characteristic including soil structure, soil water relation, soil fertility, and nutrient availability. As a result, plants’ tolerance to biotic and abiotic stresses, plants’ nutrient supply, and plants’ growth and yield are increased while fertilizer requirement and pesticide inputs are reduced (Al-Karaki 2013). Thus, in agriculture context, the increased uptake of water and soil minerals by AM-colonized plants would be an efficient alternative to substantially reduce the application of fertilizers and pesticides and at the same time obtaining equivalent or even higher crop yields.

11.3 A rbuscular Mycorrhiza Effects on Plant Performance and Soil Quality Together with root nodules, mycorrhiza is considered to be the most important symbiosis that helps feed the world. AM fungi supply the majority of land plants with nutrients, thus increasing biomass production and conferring resistance against biotic and abiotic stresses. The results of several meta-analysis, each dealing with hundreds of published papers, revealed the effectiveness of AMF in improving plant growth and productivity (Lin et al. 2015). With functional AM colonization in the roots, AMF afford host plant with a myriads of benefits: increased absorption surface area (100- or even 1000-fold), greater soil volume exploited, greater longevity of absorbing roots, better utilization of low-availability nutrients, and better retention of soluble nutrients, thus reducing reaction with soil colloids or leaching losses (Selvaraj and Chellappan 2006). AMF also provide plants with complementary characteristics and modify soil-plant-water relations, strengthening thereby better plant tolerance to adverse conditions, such as nutrient-poor soil, drought, and salinity. Hence, understanding the ecology and functioning of the AM symbiosis in the natural or agricultural ecosystem is essential for the improvement of plant growth and productivity. AMF have been shown to improve productivity in soils of low fertility and are particularly important for increasing the uptake of slowly diffusing ions such as PO43−, immobile nutrients such as P, Zn and Cu, and other nutrients such as ammonium and potassium (Rhodes and Gerdemann 1980; Ames et al. 1983; Liu et al. 2002). Under drought conditions, the uptake of highly mobile nutrients such as NO3− can also be enhanced by mycorrhizal associations (Subramanian and Charest 1999). The most established benefits from mycorrhizal fungus to the host plant is through the widespread mycelial network which penetrates deeper and wider in the soil in search of water and nutrients thereby widening the zone of activity. Nutrient acquisition begins with the uptake of free nutrients from soil by fungal extraradical hyphae that act as a bridge between the soil and plant roots (Bucher 2007). Nutrients are then transferred through the periarbuscular membrane to the plant cytosol. The majority of this nutrient exchange is believed to occur within root cortical cells containing highly branched hyphal structures termed arbuscules. The establishment

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of the mycorrhizal network offers a number of basic advantages for the acquisition of mineral nutrients: (1) fungal hyphae extend beyond the nutrient depletion zone that develops around the root. A nutrient depletion zone develops when nutrients are removed from the soil solution more rapidly than they can be replaced by diffusion. AMF hyphae can readily bridge this depletion zone and grow into soil with an adequate supply of nutrients. (2) Fungal hyphae network greatly increase the root absorbing surface area 100- or even 1000-fold compared to non-mycorrhizal roots. (3) Due to their narrow diameter relative to roots, hyphae are able to extend into soil pores that are inaccessible to roots or even root hairs. (4) Mycorrhizal fungi can access forms of N and P that are unavailable to non-mycorrhizal plants, particularly organic forms of these nutrients. One mechanism for this access is the production by plant roots and the associated mycorrhizal fungi of organic acids and hydrolytic enzymes (Smith and Smith 2011; Hodge and Storer 2015). On the other hand, the external (extraradical) mycelium of AMF establishes an underground tridimensional network that links different hosts allowing sequestration and transfer of carbon, nitrogen, and phosphorous among colonized plants. Furthermore, AMF are key component in governing plant nutrient cyclings, thus reducing significantly the need for further nutrient inputs (Al-Karaki 2013). In addition to supplying plants with nutrients, mycorrhizal fungi are clearly involved in increasing plant water availability particularly in limiting ecosystems (Auge 2001; Baslam et al. 2014; Fouad et al. 2014). These associations improve water uptake by increasing the hydraulic conductivity of the roots either by modifying root morphology and root anatomy or indirectly by hormonal and structural changes in the host plant. The survival of mycorrhizal plants in extremely dry condition is the result of a better colonized root performance and the ability to explore water in wider zones of soil by extension of the fungal mycelium into non- rhizospheric soil (Kehri and Chandra 1990). Contribution of the AM symbiosis to plant’s tolerance to drought is the result of their action on several plant functions including nutritional, physiological, and biochemical processes. This appears to be due, in many instances, to differences in tissue hydration between mycorrhizal and non-mycorrhizal plants (Baslam et al. 2014; Fouad et al. 2014). However, additional mechanisms by which AM symbiosis enhances drought tolerance of host plants have been proposed, such as increased water and nutrient absorption, high stomatal regulation by hormonal signals, enhanced osmotic adjustment, higher root hydraulic conductivity and leaf hydration, or reduced oxidative damage caused by the reactive oxygen species (ROS) generated during drought (Ruiz-Lozano 2003; Baslam et al. 2014; Fouad et al. 2014; Benhiba et al. 2015). In fact, it has been shown that mycorrhizal colonization and drought interact in modifying free amino acid and sugar pools in roots (Auge et al. 1992). A greater osmotic adjustment has also been reported in leaves of mycorrhizal plants than in non-mycorrhizal ones during drought period (Baslam et al. 2014; Fouad et al. 2014). In the same way, mycorrhizal plants had postponed declines in leaf water potential during drought stress (Davies et al. 1992; Baslam et al. 2014; Fouad et al. 2014; Benhiba et al. 2015). Furthermore, mycorrhizal plants have operated special biochemical mechanisms that prevent plant cell from oxidative damage through accumulation of some


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a ntioxidant compounds and enhancing antioxidant enzymes, superoxide dismutase (DOS), peroxidase (POX), and catalase (CAT) activities in leaves and roots of many water-stressed plants, and this was correlated to plant protection against drought (Ruiz-Lozano et al. 2003; Baslam et al. 2014; Fouad et al. 2014; Benhiba et al. 2015). On the other hand, root colonization by AM fungi may generally reduce the severity of diseases caused by soil-plant pathogens (Siddiqui et al. 1999). Such a significant effect on soil microorganisms has rapidly raised interest on the possible role of AMF in bioprotection. This has been clearly revealed by the meta-analysis of 144 published papers (Yang et al. 2014). Moreover, AMF have been described as “health insurance” of plants (Gianinazzi et al. 2010). Overall, results of most studies dealing with the interactions between AMF and soil pathogens showed that mycorrhizal colonization reduced pathogen damages confirming the potential role of AMF as biological control agent (Selim et al. 2005; Li et al. 2007). The main conclusions reported by these investigations are as follows: (1) AM associations reduce the damage caused by plant pathogens, particularly those caused by fungi and nematodes; (2) enhanced root resistance or tolerance by AM symbiosis is not equal in different plants; (3) the protection is not effective against all pathogens; and (4) protection is modulated by the host plant, soil properties, and environmental conditions (Azcon-Aguilar and Barea 1996; Siddiqui et al. 1999). Of the various mechanisms proposed for biocontrol of plant diseases, effective bioprotection is a cumulative result of multiple mechanisms working either separately or together to remind changes in root growth and morphology, physiological and biochemical changes within the plant, changes in host nutrition, competition for colonization sites, activation of defense mechanisms, and pathogen parasitism by AM fungi (Siddiqui et al. 1999). Other mechanism by which AMF increase plants’ pathogen tolerance could be the synergistic interaction AM fungi have with plant growthpromoting rhizobacteria (PGPR). On the other hand, the enhanced synthesis of secondary metabolites in mycorrhizal plants (Gianinazzi et al. 2010) may also explain why AMF are known to have a role in plants’ defense against herbivores (Larcher 1995). Arbuscular mycorrhizal fungi are the most effective soil organisms in stabilizing soil structure and key factors to soil quality characteristic and agroeconomic performances (Augé 2004). External hyphae network of AMF provides a physical structure that holds primary soil particles and leads to micro- then to macroaggregate production (Miller and Jastrow 1990; Augé 2004; Al-Karaki 2013). The efficiency of this process is enhanced by biochemical agents such as hydrophobins and glomalin (Bedini et al. 2009). Glomalin is an insoluble hydrophobic protein produced by AMF soil-based mycelium and is a major binding agent in soils that adds further weight to the importance of AMF in stabilizing soils and improving its quality (Bedini et al. 2009). AMF also indirectly improve soil aggregation by influencing bacterial communities and other soil microorganisms that can improve soil aggregate formation (Rilling 2004). According to Soka and Ritchie (2014), the soil stabilizing effects of AMF continue up to 5 months after their host’s death. Mycorrhizal symbiosis can also increase plant establishment and growth despite high levels of soil heavy metals resulting from mining activities, industrial processes,

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and agricultural activities. At elevated heavy metal concentrations in soils, mycorrhizal fungi have been shown to detoxify the environment for plant growth (Muchovej 2001). AM fungi can decrease the heavy metal concentration in shoot or in root or decrease translocation from root to shoot (Diaz et al. 1996). The latter could be due to the high metal sorption capacity of these fungi (Joner et al. 2000). In many cases AM fungi serve as a filtration barrier against transfer of heavy metal ions from roots to shoots. The protection and enhanced effect of AM fungi results in greater nutrients and water availability (Auge 2001) and best soil aggregation properties (Kabir and Koide 2000). Many factors contribute to differences in the effect of AMF on heavy metal sequestration. These include fungal genotype, metal uptake by plants via the AM symbiosis, association with soil microorganisms, soil properties, and soil heavy metal concentration. The successful integration of AMF in improving sustainable production of plants with increased adaptation potential is well documented (Douds et al. 1995; Scagel 2001, 2004; Scagel et al. 2003; Binet et al. 2007; Zai et al. 2007; Abbaspour et al. 2012; Singh et al. 2012; Yadav et al. 2013; Fatemeh and Zaynab 2014; Fouad et al. 2014; Ezekiel Amri, 2015; Fouad 2015; Essahibi et al. 2016). The benefits from AMF are thought to be highest when colonization occurs as early as possible in plant propagation cycles. The maximum benefit is obtained when inoculation is carried out during the first stage of root formation (Scagel 2001; Scagel et al. 2003; Fouad 2015; Essahibi et al. 2016). Furthermore, AMF played a critical role in adventitious root formation in many species (Scagel 2001; Scagel et al. 2003; Fouad 2015; Essahibi et al. 2016). The early inoculation provides the maximum benefits during plants’ acclimatization, thereby improving the survival and establishment of rooted cuttings (Fouad 2015; Essahibi et al. 2016). According to Essahibi et al. (2016), cuttings of carob, which is one of the most difficult-to-root species, were induced to root using AMF in the rooting substrate. In fact, inoculated cuttings rooted more frequently and produced considerably more roots than non-inoculated ones. The positive effects of AMF on adventitious root formation may be the results of a pre-colonization signal, liberation by cutting of CO2 or other metabolites able to activate AMF propagules, similar to those existing in the presence of host plant roots. The positive effect of AMF is more evident on plantlet survival to transplantation and hardening shocks. Mycorrhizal plants exhibited higher tissue hydration, higher stomatal conductance and transpiration fluxes, accompanied by improved CO2 fixation in mesophyll, and increased photosynthesis compared to non- mycorrhizal plants (Fouad 2015; Essahibi et al. 2016). Moreover, it’s well established that mycorrhizal tree seedlings tree seedlings are significantly more performant in terms of tolerance to acclimatization and post-acclimatization stresses (Fouad et al. 2014) and field survival and establishment (Ouahmane et al. 2006; Manaut et al. 2015). AMF nursery inoculation improved transplanted tree seedling growth and establishment in Acacia koa (Habte et al. 1999), Olea europaea L. (Fouad et al. 2014; Fouad 2015), and Ceratonia siliqua L. (Manaut et al. 2015; Essahibi et al. 2016). However, field mycorrhizal plant performances decreased with increasing seedling age (Karthikeyan and Krishnakumar 2012).


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11.4 M ycorrhizae Benefits in the Context of Agroecosystems Sustainability To ensure global food security, agriculture will face new major challenges: increasing future needs of a growing world human population that will reach about 10 billion by 2050 and climate changes in the context of minimizing negative environmental impact (Diouf 2011). Thus, rational and efficient use of agrosystem resources necessarily involves the use of sustainable agricultural practices. This includes better knowledge of the processes and factors that govern the bioavailability of soil nutrients and the rhizosphere functions including the root-soil-microorganism interaction understanding. The natural role of mycorrhizosphere organisms has been neglected in intensive agriculture, since microbial communities may have been modified due to tillage and high inputs of inorganic fertilizers and herbicides and pesticides (Sturz et al. 1997). Intensive agricultural practices contribute enormously in stepping up agricultural production regionally and globally, but at the same time its negative impact on soil fertility, ecosystem balance, environmental persistence, and soil biodiversity cannot be viewed superficially. Increased environmental awareness has progressively led to shift from conventional intensive management to low input crop production. Much has been written on the growing appreciation of the fundamental importance of the integration of soil microorganisms in agricultural sustainability and ecosystem management. Among these, the widespread AMF are prominent players with myriad of agroecosystem roles (Smith and Read 2008). AM symbiosis is regarded as a key component of sustainable agriculture and ecosystem management. AM fungi have beneficial effects on the two main aspects of sustainable agriculture including crop production and soil quality (Bethlenfalvay et al. 1994). They provide multiple benefits to their host plants (enhanced water and mineral uptake, increased tolerance to water stress, improved resistance to pathogens, and reduced sensitivity to toxic substances present in the soil) and myriads of ecosystem roles (assure nutrient cycling, contribute to soil structure and aggre gation of soil particles, influence microbial populations in soil, etc.). Hence, understanding of the ecology and functioning of the AM symbiosis in the natural or agricultural ecosystem is essential for the improvement of plant growth and productivity. Much of the data gained on AMF have been obtained in greenhouse experimentation using single species inoculants in sterilized soils on responsive host plants. Nevertheless, field-based studies have shown increases in early growth and development of crops when inoculated with effective AMF populations confirming the possible role of arbuscular mycorrhizae as suitable tools to improve plant performance under normal or limiting growth conditions. However, the costs of AM symbiosis can be high, with up to 20% of the host’s fixed carbon being delivered to the fungal symbiont. Nonetheless, under limiting conditions, mycorrhizal crop

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plants typically exhibit more performance over non-mycorrhizal crop plants. In high-input agricultural systems, the relative advantages are reduced while the carbon costs remain (Janos 2007). In this context, profitable application of AM symbiosis in agriculture is explained by the fact that the inevitable loss of carbon to the fungus is c ompensated by the reduction of inputs and consequently the reduction of the overall cost of production on a per unit yield basis. Moreover, by their interactions with soil particles and other organisms, AMF represent an important component of soil quality. Apart from agricultural systems, positive effect of the application of AM fungi has been reported for the rehabilitation of desert areas (Saito and Marumoto 2002) and for proper hardening and transplantation of plantlets obtained by softwood cuttings rooted under mist system or produced by tissue culture (Yano-Melo et al. 1999; Fouad et al. 2014; Fouad 2015). Indeed, higher rate of survival, improved biomass and overall growth, higher root system performance, higher photosynthetic efficiency, greater nutrient uptake, highest environmental stress tolerance, and better soilborne pathogen resistance were observed in colonized plantlets during hardening and post-hardening (Chittora et al. 2010; Fouad et al. 2014). In this context, plants not only require mycorrhizae for acclimatization but also for continuity of nutrient absorption and growth during the progress of the field establishment. Artificial mycorrhizae inoculum production using carefully selected efficient fungi is an alternative to soil chemical fertilizer administration in the context of soil fertility management. It can ensure the development of plants, which otherwise are not able to survive and produce on poor soils or in improper growing systems. AM species may be able to adapt themselves (and their host) with different ecological and environmental conditions. Moreover, resource availability and prevailing environmental conditions generate more performing AM symbiosis among plant and soil organism associations. So, origin of AM fungi should be considered when managing for their benefits in sustainable agriculture and ecosystem restoration. Appropriate management of mycorrhizae, including careful selection of performing host/fungus combinations, would allow substantial reduction in the amount of inputs without losses in productivity while at the same time permitting a more sustainable production management.

11.5 Application of AMF to Date Palm Production Date palm (Phoenix dactylifera L.) has long been one of the most important fruit crops in the arid regions of the Arabian Peninsula, North Africa, and the Middle East. During the past three centuries, it was also introduced to new production areas in Australia, India, Pakistan, Mexico, southern Africa, South America, and the United States (Chao and Krueger 2007). Dates are a main income source and staple food for local populations in many countries in which they are cultivated and have played significant roles in the economy, society, and environment. Moreover, date palm is the principal component of the oasis ecosystem where it provides


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a dequate microclimate allowing development of the understory crops and protection of the surrounding production system against desert influences. Palm grove, and consequently oasis ecosystem, is often subjected to severe environmental constraints such as nutrient-poor and moisture-deficient soil, long-term drought and high temperature, saline soil, and desertification causing considerable economic, ecological, and social damage. During the last decades, the detrimental effects of these constraints have been exacerbated as a result of the global climate changes that are more pronounced in these desert areas. These constraints cause not only reduction in the production of dates, the principal food of humans and animals in the desert, but also an imbalance of the oasis ecosystem causing a serious threat to plant resources and long-term agricultural production (Haddouch 1997). On the other hand, the increasing spread of new palm groves based on intensive agricultural practices (large amounts of fertilizers and irrigation are added annually to achieve high yields and superior fruit quality) contributes enormously in stepping up agricultural production regionally and globally, but at the same time its negative impacts soil fertility, ecosystem balance, environmental persistence, and soil biodiversity cannot be viewed superficially. This may lead to salinization of soil and leaching of nutrients to deep soils that might affect groundwater. Being a monocot, date palm produces a fasciculated and mostly fibrous root system. Seeds give birth to the primary roots from where secondary roots originated. The secondary roots produce lateral roots (tertiary roots and so on) of the same type and with approximately the same diameter throughout their length (Zaid and de Wet 2002). The date palm root system is adventitious in nature and composed of numerous, relatively small nonwoody, roots of which all primary roots are of a more or less constant diameter and arise independently and periodically from an area at or near the base of the stem called the root initiation zone (RIZ). It is this adventitious constantly or periodically renewing root system that largely makes it possible to transplant large specimens with a relatively small root ball. Full or nearly full development of the RIZ enhances transplant success. A substantial portion of the root system, almost 85%, is located in the upper 2 m of the soil surface and extends only about 2 m laterally (Munier 1973). The entire root system can be divided into four zones (Oihabi 1991; Zaid and de Wet, 2002). Regarding the harsh environmental conditions prevailing in the area of date palm distribution, it can be assumed that date palm has evolved highly mycotrophic as a strategy to allow more efficient adaptation to adverse environment conditions. Moreover, due to the shallow and coarse root system of date palm, AM symbiosis is a key factor for its survival and production under such extreme conditions. Nowadays, the mycotrophic status of date palm is well documented (Bouamri et al. 2006; Dreyer et al. 2006; Bouamri et al. 2014; Baslam et al. 2014; Benhiba et al. 2015; Sghir et al. 2015). Moreover, the roots of date palm have shown receptive not only to arbuscular mycorrhizal fungi (Khaliel and Abu Heilah 1985; Oihabi 1991; Al-Whaibi and Khaliel 1994; Dreyer 2004; Al-Yahya’ei et al. 2011) but also to ectomycorrhizal fungi (Zegaye et al. 2012) and to other endophytes: septate hyphae and sclerotia (Peterson et al. 2004).

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Arbuscular mycorrhizal colonization in date palm is restricted to the inner cortex of higher-order roots (the third-order roots) being more susceptible to AM colonization, except for the pneumatorhizas and the short thick roots (Dreyer et al. 2010). Based on the AMF structures developed in the root tissues and the on the root thickness, two types of third-order roots could be distinguished: on the one hand, mycorrhizal thickened roots containing arbuscules and, on the other hand, mycorrhizal fine roots with only intraradical hyphae and spores, but without arbuscules, and pseudomantles of spores anchored in the pneumatorings of the second-order roots. The first-order and almost all the second-order roots were not colonized by AM fungi. Bouamri et al. (2006) mentioned that the root colonization pattern of Phoenix dactylifera was Arum type. However, according to Dreyer et al. (2010) date palm mycorrhiza is intermediate between the Arum and the Paris types and is characterized by intercalary arbusculate coils and by an intracellular and intercellular fungal growth. Because of the low number of AM fungal spores in the soil conditions of palm groves, the main source of inocula is extraradical mycelium (Dreyer, 2004). The development of different root types and structures, such as the pseudomantle, is a notable example of adaptation between host and fungal partner to increase propagule numbers in response to such conditions (Dreyer et al. 2010). Several surveys on the AM status of adult date palm trees, spore density, and species richness in the rhizosphere of date palm were carried out in the main palm groves of the southeastern of Morocco (Bouamri et al. 2006, 2014; Benhiba et al. 2014; Sghir et al. 2015), as well as in Iraq (Khudairi 1969), Saudi Arabia (Khaliel and Abou-Hailah 1985), Bahrain (Al-Karaki et al. 2007), Jordan (Mohammad et al. 2003), and Sultanate of Oman, southern Arabia (Al-Yahya’ei et al. 2011), and revealed controversial results with larger variation of reported frequency and intensity of root colonization and spore density. A total of ten AMF species, including Glomus (Funneliformis) mosseae, G. fasciculatum, G. constrictum, G. aggregatum, G. macrocarpum, three undescribed species of Acaulospora, and two of Scutellospora genera, were isolated from ten palm groves in the arid part of southwestern Morocco (Bouamri et al. 2006). Nine phylogenetic taxa of AMF were found to be associated with date palm roots in Omane, eight of which could be attributed to the Glomus group A and one to the Scutellospora group (Al-Yahya’ei et al. 2011). These observations could be a general case of occurrence of mycorrhizal associations with date palms in other areas as well. More recent studies have shown that well-established date palms are naturally colonized by AMF, and natural root colonization frequency varied according to the physicochemical characteristics of the soils, particularly the P content (Benhiba et al. 2014; Bouamri et al. 2014). Moreover, large variation in spore density (13–135 spores/g of soil) and MPN (more than 1600 propagules/cm3 in Tinejdad, Ain Meski, and Aoufous and between 49 and 920 propagules/cm3 for the rest of the sites) were reported (Benhiba et al. 2014). Results of AMF identification based on spore morphology showed the existence of 12 morphotypes in the Tafilalet and Draa palm groves with a population of four to seven species per site. The isolated species include Funneliformis mosseae, F. geosporum, Rhizophagus fasciculatus, R. manihotis, R. aggregatus, Acaulospora scrobiculata, Pacispora scintillans, and three undescribed species of the genus Acaulospora


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and Scutellospora. Molecular methods identified other strains including G. claroideum and other Glomus: Glomus sp. (personal data). Seasonal variations of AMF colonization and community diversity were recently assessed in the Tafilalet date palm groves (Bouamri et al. 2014). Root colonization levels were highest during the wet season coinciding respectively with the period of active vegetative growth that requires higher nutrient allocations. However, root colonization decreased during summer and autumn coinciding respectively with the period of fruit maturation and dormant stage when need for actively functioning AM symbiosis is not as essential as during plant vegetative growth period. The outcome of these observations in regard to the occurrence of AMF in date palm is the predominance of the Glomus genus in date palm groves, confirming its world distribution and its strong adaptation to a wide range of physical, chemical, biological, and environmental soil conditions (Stutz et al. 2000; Tao and Zhiwei 2005).The natural root colonization and the diversity of AMF species associated with date palm suggest the applicability of mycorrhizal symbiosis in the management of date palm nurseries and grove establishment.

11.6 U tilization of Mycorrhizal Fungi for Date Palm Propagation Most land plant species form mycorrhizal symbioses; however, plants vary greatly in the degree to which they potentially benefit from the myriad of positive effects AMF symbiosis could provide. This ranges from those that benefit little to those that are strongly mycorrhizal dependent (Janos 2007). In the case of date palm trees, the limited development of the root system, along with field observations of high levels of mycorrhizal colonization, suggests that they benefit greatly from the AM symbiosis. The dependency of date palm on the mycorrhizal symbiosis is expected to be higher or at least similar to that of other fruit tree species since it’s a long-lived perennial species with a high demand for nutrients to sustain a large aboveground biomass and fruit production. Moreover, the coarse root systems with a low degree of branching and root hair formation as well as the arid habitats in which date palms are grown both contribute to mycorrhizal dependency. AMF could have the potential to improve sustainability of date palm production systems in various ways, for instance, by enhancing soil aggregate stability, fixing mobile sand, and improving physical and chemical soil conditions (Bearden and Petersen 2000), as well as by enhancing water uptake and nutrient availability in the desert soils under drought and saline conditions (Al-Karaki et al. 2007). However, date palm is commonly grown in deserts, which tend to be unstable ecosystems often subject to frequent disturbance, resulting in the loss or reduction of indigenous AMF density and diversity (Jeffries and Barea 1994). This can be detrimental because mycorrhizas are regarded as key components of desert ecosystems. The low density of mycorrhizal propagules in semiarid ecosystems may limit the successful establishment of native

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plants, including date palms. Alternatively, date palm seedlings can be inoculated at the propagation stage and then transplanted to the field. Inoculation of date palm seedlings with AMF in nursery condition has been reported to increase the water and nutrient uptake and enhance growth over the non- inoculated seedlings (Al-Whaibi and Khaleil 1994; Baslam et al. 2014; Benhiba et al. 2015). In addition, inoculation with AM increased the growth of tissue culture date palm seedlings at low fertilizer rate (Benhiba et al. 2014). Blal et al. (1990) reported a four- to fivefold increase in the coefficient of P utilization in micropropagated oil palms after inoculation with mycorrhizae. Date palm seedlings grown under normal nursery conditions grow more slowly and have lower survival rates when transplanted to the field, especially into disturbed soils. The innovative technique of artificial inoculation of date palm during propagation at the nursery stage and field planting might reverse these effects and result in improved plant establishment, growth rate, and yield, with complementary reductions in water and fertilizer use. The demand for high-quality date palm cultivars has increased during the last three decades, which has been encouraged by the use of micropropagation and tissue culture techniques for mass production of the transplants (Awad 2008). In spite of this great potential, transplantation success to the field has been rather low and, in some cases, cultivars have shown only a 40–50% survival rate (Zaid and de Wet 2002). Under such conditions, inoculation with AMF could be an important step to enhance the establishment and survival of the transplanted seedlings. Schultz (2001) reported that post vitro survival rate and growth of oil palm ranged between 83% and 100% after 3 months of in vitro inoculation with AMF, compared to only 55% of the non-inoculated plants. From an economic perspective, the high potential of enhancing growth characteristics and improving the survival rate may reduce costs. These findings could lead to enormous savings for nurseries given the high costs associated with the loss of nursery plants as well as high mortality and slow growth rate at the outplanting stage. The effectiveness of native AMF strains isolated from the Southwest of Morocco, compared to Rhizophagus intraradices (reference strain), in improving acclimati zation and tolerance to post-acclimatization abiotic stresses in date palm in vitro plantlets has been recently reported (Benhiba et al. 2014). Compared to non- inoculated plantlets, plantlets of Nejda and Boufeguous varieties inoculated by the native and reference AMF strains showed better acclimatization performances in terms of survival rate, growth and biomass production (aerial and root’s fresh and dry weights), water status (relative water content), and nutrient status (leaf content of sugars, proteins, and mineral elements P, K, Mg, N, and Mn). Similarly, these mycorrhizal associations have shown a better ability to overcome water stress and phosphorus deficiency in post-acclimatization through their positive effects on growth (plant height and leaf area), biomass production (root and shoot weight), metabolism (phosphatase, polyphenol oxidase, peroxidase, and superoxide dismutase activities), and physiology (stomatal conductance, electrolyte loss, relative water content) in both varieties (Benhiba et al. 2014a, b, c). The local strains Acaulospora scrobiculata, Rhizophagus manihotis, and Glomus versiforme were as


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effective as the reference strain Rhizophagus intraradices known for providing highly significant benefits to plants especially in adverse conditions.

11.7 Response of Mycorrhizal Date Palm to Water Stress Water deficit is one of the most environmental stresses affecting agricultural productivity around the world and may result in considerable yield reduction. Drought affects nearly all the plant functions; however, the plants’ response to water stress depends upon the intensity, rate, and duration of exposure and the stage of crop growth. In this context, the importance of the date palm tree has increased as it’s a drought-tolerant species in addition to its impact in combating desertification. Moreover, date palm assumes importance because production of other fruit trees is limited in the harsh environment. Although date palm can withstand long periods of drought, large amount of water are required for vigorous growth and high yields (Chao and Krueger 2007). Cultural areas of date palm depend on groundwater, the main source of water for agriculture in these regions. The limited precipitation and the increase in the area of agricultural land have put pressure on groundwater usage, since the agricultural demand for freshwater in this region is growing. Therefore, drought stress can cause significant yield losses in date palm and negatively affect their productivity. Indeed, among abiotic stresses, water scarcity is the most severe environmental stress impairing crop development in arid and semiarid areas where long dry seasons with low water availability adversely affect all plant functions. To adapt and survive periods of drought stress, higher plants are endowed with evolved defense mechanisms that include, among other strategies, a battery of enzymatic (e.g., SOD, CAT, APX, G-POD, and GR) and nonenzymatic antioxidants, e.g., ascorbate and glutathione (Kar 2011; Sharma et al. 2014). However, long-term drought stress inevitably results in overproduction of reactive oxygen species (ROS) that can pose a threat to cells by causing oxidization of lipids, DNA, RNA, and proteins, leading ultimately to cell death (Smirnoff 1995; Mittler 2002; Kar 2011; Sharma et al. 2014). In this context, the ability of the root systems to establish beneficial symbiotic relationships with soil microorganisms represents one of the most successful strategies that land plants have developed to cope with abiotic stresses. AM symbiosis is widely believed to provide complementary characteristics that improve host plant performance due to the capacity of AM fungi to alleviate the deleterious effects of drought (Wu and Xia 2006; Faghire et al. 2010; Abbaspour et al. 2012; Fouad et al. 2014). The contribution of AM symbiosis to the host plant’s drought tolerance results from a combination of physiological and metabolic effects. This appears to be due to improved water uptake and/or reduced transpiration leading to differences in tissue hydration between mycorrhizal and non-mycorrhizal plants (Ruiz-Lozano 2003; Faghire et al. 2010; Baslam et al. 2014; Benhiba et al. 2015). However, additional mechanisms have been proposed such as enhanced osmotic adjustment or reduced oxidative damage caused by ROS (Ruiz-Lozano 2003; Abbaspour et al. 2012; Fouad et al. 2014; Baslam et al. 2014).

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Recently several experimentations had been carried out to investigate the influence of different AMF species, Rhizophagus intraradices, Funneliformis mosseae, and Complex Aoufous (Moroccan native AMF), on date palm plantlets grown under two water regimes, well water (75% of field capacity) or water deficit (25% of field capacity) (Faghire et al. 2010; Baslam et al. 2014; Benhiba et al. 2015). Obtained results demonstrated that the beneficial effect of mycorrhizal symbiosis depended on fungal species and water regime. While native AMF (CA) were most effective in increasing growth and biomass production under well water conditions, R. intraradices was most beneficial under restricted water supply. In this study, mycorrhizal date palm seedlings suffered less water stress imposed by short-term water scarcity (Baslam et al. 2014). Performance of mycorrhizal date palm seedlings, attributed to a primary drought avoidance by mycorrhizal symbiosis, was related to difference in tissue hydration and nutrient status between mycorrhizal and non-mycorrhizal plants, as well as to increased cell wall elasticity, and maintained leaf water potential and osmotic potential, but not related to changes in antioxidant activities (Faghire et al. 2010; Baslam et al. 2014). However, under long-term drought (LTD), activity of antioxidant enzymes SOD, CAT, G-POD, and APX was higher in mycorrhizal plants than in non-inoculated plants, showing a consistent effect of AM colonization on oxidative stress alleviation induced by LTD (Benhiba et al. 2015). Indeed, H2O2 and MDA were less accumulated in water-stressed mycorrhizal plants compared to their relative non-inoculated plants. Mycorrhizal date palm tolerance to LTD involves several plant functions including (1) increased soluble sugars, proteins, proline, and K accumulation, (2) improved plant water relations, (3) enhanced antioxidants enzymes activities, and (3) alleviation of ROS accumulation and oxidative damage. R. intraradices was the most efficient in improving date palm plants’ tolerance to drought. Thus contribution of AM fungi to date palm protection against short-term water stress involves enhanced mechanisms associated with water status and nutrient acquisition (Baslam et al. 2014). However, under persistent drought, the complex system related to protection against oxidative stress involving antioxidant enzyme activities and ROS alleviation has been substantially triggered off (Benhiba et al. 2015).

11.8 Response of Mycorrhizal Date Palm to Saline Soil Soil salinity negatively affects the establishment, growth, and development of plants (Evelin et al. 2009). Salt stress can induce both ionic and osmotic stress. Toxic effects of specific ions (sodium and chloride) inhibit the protein synthesis, damage the cell organelles, disrupt structure of enzymes, and uncouple photosynthesis as well as respiration (Ruiz-Lozano et al. 2012). Salt accumulation in the soil depresses the soil osmotic potential and virtually impedes water uptake by roots, subsequently leading to drought stress (Ruiz-Lozano et al. 2012). In addition, the saline rhizosphere environment reduces nutrient uptake and/or transport to the shoot, leading eventually to nutrient deficiency or imbalanced plant nutrition (Evelin et al. 2009).


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Plant cells have three different strategies to cope with ionic and osmotic stresses: osmotic adjustment through accumulations of compatible solutes such as betaine and proline (Tang and Newton 2005), salt extrusion from the cell across the plasma membrane using ion transporters such as the Na+/H+ antiporter (Parvin et al. 2014), and salt accumulation in the vacuoles using tonoplast transporters (Zhu et al. 2005). In date palm, detrimental effect of salt stress impacts growth, development, survival, and the productivity by affecting mechanisms related to ROS production and oxidative damage (Parvin et al. 2014). Helaly and El-Hosieny (2011) found that under stress conditions, the lipid peroxidation increased in plant tissues caused by a high degree of membrane deterioration (Pottosin and Shabala 2014). Hence, alternatives to enhance constitutive and/or induced activity of SOD and other antioxidants such as APX, CAT, and GR are essential. Soil organisms mutually cooperating with plant roots have seen increased consideration in recent years. Inoculation with beneficial microorganisms has resulted in increased plant performance in terms of growth, nutrition, and tolerance to abiotic stresses, conferring better plant survival, establishment, and development in arid soils (Liddycoat et al. 2009). Thus proper management of the soil biological potential is the keystone to agricultural success in semiarid and arid areas (Zarea 2010; 2013). Biofertilizers and polyamines (Put and others) have been reported to be involved in the plant response to salt and osmotic stress by playing an important role in the ROS-mediated damage caused by salt stress (Rasmia and Darwesh 2013) and act as antioxidants in the protective mechanisms (Tang and Newton 2005; Salama et al. 2014). Similarly, the application of effective microorganisms at the rate of 90 ml/ palm/year (with about 104 cells/ml) increased leaf chlorophyll and mineral contents as well as fruit quantity and quality in date palm (Salama et al. 2014). According to Helaly et al. (2016), selected PGPR allow date palm to increase its adaptation to saline areas. Furthermore, the interaction between PGPR and Put under salt and osmotic stress conditions could affect not only the productivity of date palm but also the properties of the soil. Thus, selection of efficient microorganisms from stressed ecosystems can be used as a biotechnology tools to sustainable agriculture management. AM fungi are ubiquitous and are known to exist in saline environment (Giri et al. 2003; Yamato et al. 2008; Estrada et al. 2013). In this context, there is evidence that saline-stress-specific AMF could help their host plants to overcome the detrimental effect of salt stress (Evelin et al. 2009). In addition to its effect on the host plant, salinity affects also directly or indirectly their symbionts (AMF). Indeed, salinity negatively impacts colonization capacities, spore germination abilities, and fungal hyphal growth (Juniper and Abbott 2006). Moreover, under conditions of high salinity, plants might not be able to supply the necessary carbon for the fungus because of the need for additional energy to pump out Na+ and Cl−. In addition, photosynthesis may be impaired due to chloroplast disintegration. However, being less sensitive to salt stress, AM fungi may provide multiple advantages to their hosts under saline conditions (Ruiz-Lozano et al. 2012): (1) nutrient uptake via the mycelium may compensate for decreased nutrient uptake via the root surface; (2) the fungal

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mycelium might protect the host roots from uptake of toxic levels of Na+ and Cl−; (3) colonized roots grow and function better under salinity; and (4) extraradical mycelium of AM fungi can extend beyond the salt accumulation area and access the less saline bulk soil. On the other hand, the outcome from several investigations aiming to mitigate salt stress effect is that AMF provide complementary characters to strengthen plant tolerance to salt stress. This results from the action of AMF on various mechanisms, such as improving water and phosphorus uptake (Ruiz-Lozano 2003), production of phytohormone (Fortin et al. 2016), changes in physiological and biochemical properties of the host plant (Smith and Read 2008), and root protection against toxic ions (Hammer et al. 2010). Moreover, nitrogen assimilation is substantially increased by the host plant under salt stress (Evelin et al. 2009). Date palms are known to be salinity-tolerant (Maas 1990, 1993). Physiological mechanisms underlying salinity tolerance in date palms are not completely understood, but salt exclusion rather than inclusion seems to be related to the extent by which salinity is tolerated. In their natural habitat, date palm may encounter salinity either in all parts of their root system or restricted to the topsoil or subsoil. In many places where date palms are grown under surface irrigation, water supplied to the plants is brackish, and salts may accumulate to a greater extent in the topsoil compared with the subsoil. Moreover, date palm is more sensitive to nutrient deficiencies and large amounts of mineral fertilizers and irrigation are added annually, especially in newer plantations, to achieve high yields and superior fruit quality. This may lead to salinization of soil and leaching of nutrients to deep soils that might affect groundwater which is used for irrigation purposes resulting in accumulation of salts in the root zone. Even though drip irrigation is often used in newer plantations, flood irrigation is still highly practiced by farmers in many countries (e.g., Arabian Peninsula), which result in high water consumption and hence high accumulation of salts in the root zone of date palm. In addition, slightly saline water is often used for irrigation. This might lead to soil degradation and may negatively affect date palm production. In recent experimentation, response of young mycorrhizal clone of date palms to partial root zone salinity and drought (with either topsoil or subsoil roots exposed to salinity or drought) has been investigated (Asha Christopher 2015). Obtained results suggest that percentage of root colonization was not affected by the soil dryness; however, a drastic decline in root colonization was noticed with the increased salinity. Mycorrhizal date palm exposed to subsoil salinity grows better and shows higher water use efficiency, unlikely due to water saving mechanisms induced upon exposure of roots to a low osmotic potential. It can be noticed from the present experiment that mycorrhiza had not influenced mineral nutrient uptake since leaf concentrations of almost all nutrients (Ca, Mg, Cu, and Fe) were below the optimum levels needed for the better growth of the date palm (Asha Christopher 2015). Other experiment dealing with the impact of mycorrhizal inoculation on date palm response to salt stress was carried out by Diatta et al. (2014). Seedlings of two date palm cultivars, Nakhla hamra (NHH) and Tijib, were inoculated with five Glomus species (G. aggregatum, G. intraradices, G. verriculosum,


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G. mosseae, G. fasciculatum) and subjected to increasing levels of NaCl (0, 1, 2, 4, 6, 8, and 16 g∙L−1). Obtained results showed that upon reaching the threshold of tolerance to salt, NaCl had a significantly depressive effect on the growth parameters of both date palm cultivars, NHH and Tijib, as previously reported by Sané et al. (2005). However, Tijib was less sensitive to salt stress than NHH when salt concentrations exceed 8 g∙L−1. Inoculation with AMF significantly improved the growth of date palm seedlings under conditions of salt stress in both cultivars. Highest NHH’s plant tolerance to salt was recorded in the presence of R. intraradices that exhibited not only the highest mycorrhizal intensity (28%) but also the longest stems (32.16 cm) and roots (77 cm) and the strongest root production (50 roots/plant). However, in Tijib, mycorrhizal intensity (8.10%) and stem (33.26 cm) and root (51.62 cm) growth and the average production of roots (45 roots/plant) were highest in the presence of G. fasciculatum. Moreover, mycorrhizal seedlings of date palm subjected to salt stress accumulate high concentration of proline, thereof, varied according to the date palm cultivar, AMF strain, and NaCl concentration. Indeed, seedlings of NHH quickly accumulate proline (1.75 to 4 times higher than control) when inoculated with Glomus intraradices, respectively, under 8 and 16 g∙L−1 of salt. In contrast, Tijib seedlings accumulated more proline when colonized by G. fasciculatum. The fewer studies dealing with the role of AM fungi in date palm survival, maintenance, and productivity in saline lands and the encompassed knowledge gaps would continue to stimulate a more effective dialogue between mycorrhizal researchers and agronomists in the continued quest for sustainable productivity improvements, especially in the context of abiotic harsh conditions.

11.9 Conclusion One of the main challenges for agricultural success in arid land is the efficient exploitation of soil, not only as an agricultural resource base but also as a living and fragile system, to guarantee its long-term stability and productivity. The soil biological component is a key component of the soil quality since the agronomic potentialities of a soil depend on it. The management of soil microorganisms as providers of key ecological services is at the forefront of governing sustainable soil fertility. These organisms can participate in improving plant growth and nutrition, strengthening plant performance, restoring ecosystems, and combating pests and pollution. A greater understanding of how plants and soil microbes live together and benefit each other can provide new strategies to improve plant productivity while helping to protect the environment and maintain global biodiversity. Modern agriculture has gone through three evolution phases in recent history: (1) agricultural revolution in the eighteenth century introduced crop rotation to take advantage of and manipulate microbial populations in the soil, although at that time it was not known why this benefited plant health and growth. (2) The second revolution, referred to as the “green revolution” was based on the improvement of

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plant-breeding techniques, including genetic engineering of plants, but also and especially on heavy use of chemical inputs. (3) We may now be at the dawn of a third revolution, which will combine the two approaches in a more complete and global strategy including application of new knowledge about beneficial plant-soil microbe interactions to plant-breeding and genetic-engineering technologies. Nowadays, the management of rhizospheric microorganism biodiversity mainly the AMF is at the root of the sustainable development of agroecosystems. These organisms, often referred to as “ecosystem engineers,” “biocontrol agents,” “biofertilizers,” or “bioenhancers,” are biotechnological tools of undeniable practical interest especially when they are developed from the natural soil microflora. Today, reviewing plant production cycles and agricultural practices considering beneficial effects of mycorrhizal fungi needs support from legislators, politicians, and society in general to develop sustainable agricultural strategies to achieve acceptable levels of productivity and food quality while minimizing adverse environmental impacts. There is substantial evidence that mycorrhiza can improve date palm productivity in established plantations, especially if growers could rethink fertilizer and pesticide inputs. Indeed, the proper management of the date palm groves and the surrounding agrosystem can enhance native AMF levels in the soil which can help plants to tolerate stresses and grow better under extreme adverse conditions. In addition, efficient integration of innovative mycorrhizal technology during propagation and transplanting phase in date palm production may help in (1) increasing survival and establishment of tissue-cultured plants in addition to complementary reductions in fertilizer inputs leading to colossal reduction of the overall production costs, (2) promoting more sustainable date palm production system, and alleviating problems associated with high chemical inputs.

References Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169(7):704–709 Al-Karaki GN (2013) Application of mycorrhizae in sustainable date palm cultivation. Emir J Food Agric 25(11):854–862 Al-Karaki GN, Othman Y, Al-Ajmi A (2007) Effects of mycorrhizal fungi inoculation on landscape turf establishment under Arabian Gulf region conditions. Arab Gulf J Sci Res 25(3):147–152 Al-Whaibi MH, Khaleil AS (1994) The effect of Mg on Ca, K and P content of date palm seedlings under mycorrhizal and non-mycorrhizal conditions. Mycoscience 35:213–217 Al-Yahya’ei MN, Oehl F, Vallino M, Lumini E, Redecker D, Wiemken A, Bonfante P (2011) Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia. Mycorrhiza 21(3):195–209 Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two N-labelled sources by Glomus mosseae. New Phytol 95:381–396 Amri E (2015) Influence of Arbuscular mycorrhizal fungi on rooting ability of auxin treated stem cuttings of Dalbergia melanoxylon (Guill and Perr.) Res J Bot 10:88–97 Auge RM, Foster JG, Loescher WH, Stodola AJ (1992) Symplastic molality of free amino acids and sugars in Rosa roots with regard to VA mycorrhizae and drought. Symbiosis 12:1–17


209

Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42 Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84(4):373–381 Awad MA (2008) Promotive effects of a 5-aminolevulinic acid-based fertilizer on growth of tissue culture-derived date palm plants (Phoenix dactylifera L.) during acclimatization. Sci Hortic 118:48–52 Azcon-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soilborne plant pathogens-an overview of the mechanisms involved. Mycorrhiza 6:457–464 Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz- García A et al (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301 Baslam M, Qaddoury A, Goicoechea N (2014) Role of native and exotic mycorrhizal symbiosis to develop morphological, physiological and biochemical responses coping with water drought of date palm, Phoenix dactylifera. Trees 28(1):161–172 Bearden BN, Petersen L (2000) Influence of arbuscular mycorrhizal fungi on soil structure and aggregate stability of a vertisol. Plant Soil 218:173–183 Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular- arbuscular mycorrhizal symbiosis. Appl Environ Microbiol 55:2320–2325 Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41(7):1491–1496 Benhiba L, Essahibi A, Fouad MO, Qaddoury A (2014) Effet des champignons mycorrhiziens arbusculaires, sous conditions semi contrôlées sur la croissance des vitro-plants de palmier dattier sous stress en phosphore. In: International congress on mycorrhizae, October 15–17 Marrakech–Morocco Benhiba L, Fouad MO, Essahibi A, Gholam C, Qaddoury A (2015) Arbuscular mycorrhizal symbiosis enhanced growth and antioxidants metabolism in date palm seedlings subjected to long- term drought. Trees 29:1725–1733 Bethlenfalvay GJ, Schüepp H (1994) Arbuscular mycorrhizas and agrosystem stability. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser Verlag, Basel, pp 117–131 Binet MN, Lemoine MC, Martin C, Chambon C, Gianinazzi S (2007) Micropropagation of olive (Olea europaea L.) and application of mycorrhiza to improve plantlet establishment. In Vitro Cell Dev Biol Plant 43(5):473–478 Blal B, Gianinazzi-Pearson V (1990) Interest of endomycorrhizae for the production of micropropagated oil palm clones. Agric Ecosyst Environ 29:39–43 Bonfante P, Bianciotto V (1995) Presymbiotic versus symbiotic phase in arbuscular endomycorrhizal fungi: morphology and cytology. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer-Verlag, Berlin, pp 229–247 Bouamri R, Dalpe Y, Serrhini MN, Bennani A (2006) Arbuscular mycorrhizal fungi species associated with rhizosphere of Phoenix dactylifera L. (date palm) in Morocco. Afr J Biotechnol 5(6):510–516 Bouamri R, Dalpé Y, Serrhini MN (2014) Effect of seasonal variation on arbuscular mycorrhizal fungi associated with date palm. Emir J Food Agric 26(11):977–986 Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26 Carvalho LM, Correia PM, Martins-Loucao MA (2001) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170 Chao CCT, Krueger RR (2007) The date palm: overview of biology, uses and cultivation. Hortic Sci 42(5):1077–1082 Chittora M, Suthar RK, Purohit SD (2010) Root colonization and improved growth performance of micropropagated Terminalia bellerica Roxb. plantlets inoculated with Piriformospora indica during ex.vitro acclimatization. Acta Hort (ISHS) 865:193–198

210

A. Qaddoury

Christopher A (2015) Development and functioning of mycorrhizal roots systems under non- uniform rootzone salinity, PhD thesis 2015, p 243, University College of Food and Agriculture, United Arab Emirates Davies FT, Potter JR, Linderman RG (1992) Mycorrhiza and repeated drought exposure affect drought resistance and extraradical hyphae development of pepper plants independent of plant size and nutrient content. J Plant Physiol 139:289–294 Dehne HW, Backhaus GF (1986) The use of vesicular-arbuscular mycorrhizal fungi in plant production. I. Inoculum production, A. Pflanzenkranheiten Pflanzenschutz 93:415–424 Diatta ILD, Kane A, Agbangba CE, Sagna M, Diouf D, Aberlenc-Bertossi F, Duval Y, Borgel A, Sane D (2014) Inoculation with arbuscular mycorrhizal fungi improves seedlings growth of two sahelian date palm cultivars (Phoenix dactylifera L., cv. Nakhla hamra and cv. Tijib) under salinity stresses. Adv Biosci Biotechnol 5:64–72 Diaz G, Azcon-Aguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum Spartum and Anthyllis Cytisoides. Plant Soil 180:241–249 Diouf J (2011) Biotechologies for agricultural development. Food Agriculture Organization of the United Nations, Rome Douds DD, Bécard G, Pfeffer PE, Doner LW (1995) Effect of vesicular–arbuscular mycorrhizal fungi on rooting of Sciadopitys verticillata Sieb & Zucc. Cuttings. Hortscience 30(1):133–134 Dreyer B (2004) Estudios de caracterización y eficiencia de las micorrizas arbusculares de las palmeras Brahea armata S Watson, Chamaerops humilis L, Phoenix canariensis Chabaud y P Dactylifera L Ph.D. thesis, Universidad de Murcia, Spain Dreyer B, Morte A, Pérez-Gilabert M, Honrubia M (2006) Autofluorescence detection of arbuscular mycorrhizal fungal structures in palm roots: an underestimated experimental method. Mycol Res 110:887–897 Dreyer B, Morte A, Ángel Lopez J, Honrubia M (2010) Comparative study of mycorrhizal susceptibility and anatomy of four palm species. Mycorrhiza 20:103–115 Essahibi A, Benhiba L, Fouad MO, Ait Babram M, Ghoulam C, Qaddoury A (2016) Improved rooting capacity and hardening efficiency of carob (Ceratonia siliqua L.) cuttings using arbuscular mycorrhizal fungi. Arch Biol Sci https://doi.org/10.2298/ABS160307100E Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201:42–51 Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280 Faghire M, Baslam M, Samri S, Meddich A, Goicoechea N, Qaddoury A (2010) Effect of arbuscular mycorrhizal colonization on nutrient statut, water relations and growth of date palm seedlings under water stress. Acta Hortic 882:833–838 Fatemeh B, Zaynab M (2014) Enhanced rooting of leaf bud cuttings of Schefflera arboricola using mycorrhizal fungi. Annual Res Rev Bio 4(18):2892–2900 Fortin JA, Plenchette C, Piché Y (2016) Les mycorhizes, l’essor de la nouvelle révolution verte. Editions Quae, Feb 1, 2016 – Mycorhizes – p 184 Fouad MO (2015) Determinants of performances of olive cuttings to overcome the acclimatization and transplantation shocks: role of arbuscular mycorrhizal fungi, Dissertation University Cadi Ayyad of Marrakech, p 157 Fouad MO, Essahibi A, Qaddoury A (2013) Arbuscular mycorrhizal fungi enhanced hardening and post hardening water stress tolerance of Semi-herbaceous olive cuttings. In: 7th International Conference on Mycorrhiza (ICOM7) New Delhi, January, 6–11 Fouad MO, Essahibi A, Benhiba L, Qaddoury A (2014) Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought. Span J Agric Res 12(3):763–771 Frank AB (1885) Über die auf Wurzelsymbiose berhende Ernährung gewiser Bäume durch unterirdische Pilze. Berichte der Deutschen Botanishen Gesellschaft 3:128–145.


211

Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530 Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255 Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175 Habte MY, Zhang C, Schmitt DP (1999) Effectiveness of Glomus species in protecting white clover against nematode damage. Can J Bot 77:135–139 Haddouch M (1997) Situation actuelle et perspective de développement du palmier Dattier au Maroc. Bulletin de liaison du programme Nationale de Transfert de technologie en agriculture No. 31 Hammer EC Nasr H Pallon J Olsson PA, Wallander H (2010) Elemental composition of arbuscular mycorrhizal fungi from with excessive salinity. In: Tryckeriet I E-hyset, Lund. Nutriment Balance and Salinity Stress in Arbuscular Mycorrhizal Fungi, pp 105–122 Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, London Helaly MN, El-Hosieny H (2011) Combined effects between genotypes and salinity on sweet orange during the developmental stages of its micropropagation. Res J Bot 6:38–57 Helaly MN, El-Hosieny H, Elsheery NI, Hazem Kalaji M (2016) Effect of biofertilizers and putrescine amine on the physiological features and productivity of date palm (Phoenix dactylifera, L.) grown on reclaimed-salinized soil. Trees 30:1149–1161 Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (phylum Glomeromycota). J Exp Bot 60:2465–2480 Hepper C (1985) Isolation and culture of VA mycorrhizal (AM) fungi. In: Powell CL, Bagyaraj DJ (eds) VA mycorrhizal. CRC Press, Boca Raton, pp 95–112 Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19 Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91 Jeffries P, Barea JM (1994) Biogeochemical cycling and arbuscular mycorrhizas in the sustainability of plant–soil systems. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser Verlag, Basel, pp 101–115 Jeffries P, Barea JM (2000) Arbuscular mycorrhiza-a key component of sustainable plant-soil ecosystems. In: Hock B (ed), The mycota, vol. IX, Fungal associations. Springer-Verlag, New York, pp 95–113 Johnson NC, Tilman D, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042 Joner EJ, Aarle IM, Vosatka M (2000) Phosphatase activity of extra-radical arbuscular mycorrhizal hyphae a review. Plant Soil 226:199–210 Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379 Kabir Z, Koide RT (2000) The effect of dandelion or a cover crop on mycorrhiza inoculum potential, soil aggregation and yield of maize. Agric Ecosyst Environ 78:167–174 Kar RK (2011) Plant responses to water stress role of reactive oxygen species. Plant Signal Behav 6:1741–1745 Karthikeyan A, Krishnakumar N (2012) Reforestation of bauxite mine spoils with Eucalyptus tereticornis Sm. seedlings inoculated with arbuscular mycorrhizal fungi. Ann For Res 55:207–216 Kehri HK, Chandra S (1990) Mycorrhizal association in crops under sewage farming. J Indian Bot Soc 69:267–270 Khaliel AS, Abou-Heilah AN (1985) Formation of vesicular-arbuscular mycorrhizae in Phoenix dactylifera L., cultivated in Qassim region, Saudi Arabia. Pak J Bot 17:267–270 Khan AG (2005) Role of soil microbes in the rhizospheres of plant growing on trace metal contaminated soils. J Trace Elem Med Biol 18:355–364 Khudairi AK (1969) Mycorrhiza in desert soils. Bioscience 19(7):598–599

212

A. Qaddoury

Koske RE, Gemma JN (1992) Fungal reactions to plants prior to mycorrhizal formation. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman & Hall, New York Larcher W (1995) Physiological plant ecology, 3rd edn. Springer Verlag, New York Li B, Ravnskov S, Xie GL, Larsen J (2007) Biocontrol of Pythium damping-off in cucumber by arbuscular mycorrhiza-associated bacteria. BioControl 52:863–875 Liddycoat SM, Greenberg BM, Wolyn DJ (2009) The effect of plant growth promoting rhizobacteria an asparagus seedling and germinating seeds subjected to water stress under greenhouse conditions. Can J Microbiol 55:388–394 Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232 Liu A, Hamel C, Elmi A, Costa, Ma B, Smith DL (2002) Concentrations of K, Ca and Mg in maize colonized by arbuscular mycorrhizal fungi under field conditions. Can J Soil Sci 82:271–278 Maas EV (1990) Crop salt tolerance. In: Tanji KK (ed) Agricultural salinity assessment and management ASCE manuals and reports on engineering, no. 71. ASCE, New York, pp 262–304 Maas EV (1993) Testing crops for salinity tolerance. In: Maranville JW, BaIigar BV, Duncan RR, Yohe JM (eds) Proc. workshop on adaptation of plants to soil stresses. INTSORMIL Pub No. 94–2. Univ of NE, Lincoln, pp 234–247 Manaut N, Sanguin H, Ouahmane L, Bressan M, Thioulouse J, Baudoin E et al (2015) Potentialities of ecological engineering strategy based on native arbuscular mycorrhizal community for improving afforestation programs with carob trees in degraded environments. Ecol Eng 79:113–119 Miller RM, Jastrow JD (1990) Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol Biochem 22:579–584 Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410 Mohammad MJ, Hamad SR, Malkawi HI (2003) Population of arbuscular mycorrhizal fungi in semiarid environment of Jordan as influenced by biotic and abiotic factors. J Arid Environ 53:409–417 Morton JB (1990) Species and clones of arbuscular mycorrhizal fungi (Glomales, Zygomycetes): their role in macro- and microevolutionary processes. Mycotaxon 37:493–515 Mosse B (1959) The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Trans Br Mycol Soc 42:273–286 Muchovej RM (2001) Importance of mycorrhiza for agricultural crops, institute of reduced by drought. Aust J Exp Agric 36:563–569 Munier P (1973) Le palmier dattier. Maisonneuve & Larose, Paris Oihabi A (1991) Doctorat d’Etat, Universite Cadi Ayyad, Faculte des Sciences Semlalia-Marrakech, Maroc, p 110 Ouahmane L, Duponnois R, Hafidi M et al (2006) Plant Ecol 185:123. https://doi.org/10.1007/ s11258-005-9089-9 Parvin S, Lee OR, Sathiyaraj G, Khorolragcha A, Kim Y, Yang DC (2014) Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defence system. Gene 537:70–78 Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa Pirozynski KA, Malloch DW (1975) The origin of land plants: a matter of mycotropism. Biosystems 6:153–164 Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signalling. Front Plant Sci 5:1–16 Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza. Springer International Publishing, Cham, pp 1–7 Rasmia SS, Darwesh (2013) Improving growth of date palm plantlets grown under salt. Ann Agric Sci 58:247–256


213

Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the ordovician. Science 289:1920–1921 Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91:11841–11843 Requena N, Perez-Solis E, Azcon-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498 Rhodes LH, Gerdemann (1980) Nutrient translocations in VA mycorrhizae. In: Pappas CW, Rudolph ED (eds) Cellular interactions in symbiosis and parasitim. The Ohio State University Press, Colombus, p 173 Rilling MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754 Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress new perspectives for molecular studies. Mycorrhiza 13:309–317 Ruiz-Lozano JM, Porcel R, Azcn C, Areca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044 Saito M, Marumoto T (2002) Inoculation with arbuscular mycorrhizal fungi: the status quo in Japan and the future prospects. Plant Soil 244:273–279 Salama I, Messedi D, Ghnaya T, Abdely C (2014) Effet du déficit hydrique sur la croissance et l’accumulation de la proline chez Sesuvium portulacastrum. Revue des Régions Arides 1:234–241 Sané D, Ould Kneyta M, Diouf D, Badiane FA, Sagna M, Borgel A (2005) Growth and development of date palm (Phoenix dactylifera L.) seedlings under drought and salinity stresses. Afr J Biotechnol 4:968–972 Scagel CF (2001) Cultivar specific effects of mycorrhizal fungi on the rooting of miniature rose cuttings. J Environ Hortic 19(1):15–20 Scagel CF (2004) Enhanced rooting of kinnikinnick cuttings using mycorrhizal fungi in rooting substrate. Hort Technol 14(3):355–363 Scagel CF, Reddy K, Armstrong JM (2003) Mycorrhizal fungi in rooting substrate influences the quantity and quality of roots on stem cuttings of Hick’s yew. Hort. Technology 13(1):62–66 Schultz C (2001) Effect of (vesicular-) arbuscular mycorrhiza on survival and post vitro development of micropropagated oil palms (Elaeis guineensis Jacq.), Ph.D. thesis. Universität Gö ttingen, Germany Selim S, Negrel J, Govaerts C, Gianinazzi S, van Tuinen D (2005) Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the sorghum mycorrhizosphere. Appl Enivron Microbiol 71:6501–6507 Selvaraj T, Chelleppan P (2006) Arbuscular mycorrhizae: a diverse personality. Centrail Eur J Agr 7:349–358 Sghir F, Touati J, Chliyeh M, Ouazzani Touhami A, Filali-Maltouf A, El Modafar C, Moukhli A, Oukabl A, Benkirane R, Douira A (2015) Diversity of arbuscular mycorrhizal fungi in the rhizosphere of date palm tree (Phoenix dactylifera) in Tafilalt and Zagora regions (Morocco). Ame J Sci Med Res 1(1):1–11 Sharma A, Batra NG, Sharma H (2014) Physical chemical analysis of the rhizospheric soil of Phoenix dactylifera L. in semi arid regions of Jaipur district. Int Res J Pharm App Sci 4(1):9–15 Siddiqui ZA, Mahmood I, Khan MW (1999) VAM fungi as prospective biocontrol agents for plant parasitic nematodes. In: Bagyaraj DJ, Varma A, Khanna KK, Kehri HK (eds) Modern approaches and innovations in soil management. Rastogi, Meerut, pp 47–58 Simon L, Levesque RC, Lalonde M (1993) Identification of endomycorrhizal fungi colonizing roots by fluorescent single-strand conformation polymorphism polymerase chain reaction. Appl Environ Microbiol 59:4211–4215 Singh NV, Singh SK, Singh AK, Meshram DT, Suroshe SS, Mishra DC (2012) Arbuscular mycorrhizal fungi (AMF) induced hardening of micropropagated pomegranate (Punica granatum L.) plantlets. Sci Hortic 136:122–127

214

A. Qaddoury

Smirnoff N (1995) Antioxidant systems and plant response to the environment. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific Publishers, Oxford, UK, pp 217–243 Smith SE, Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular- arbuscular mycorrhizal plants. Annu Rev Plant Physiol Plant Mol Biol 39:221–244 Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Waltham Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250 Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis and ecosystem processes: prospects for future research tropical soils. OJE 4:11–22 Sturz AV, Carter MR, Johnston HW (1997) A review of plant disease, pathogen interactions and microbial antagonism under conservation tillage in temperate humid agriculture. Soil Tillage Res 41:169–189 Stutz JC, Copeman R, Martin CA, Morton JB (2000) Patterns of species composition and distribution of arbuscular mycorrhizal fungi in arid regions of southwestern North America and Namibia, Africa. Can J Bot 78:237–245 Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75 Tang W, Newton RJ (2005) Polyamines reduced salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43 Tao L, Zhiwei Z (2005) Arbuscular mycorrhizas in a hot and arid ecosystem in southwest China. Appl Soil Ecol 29:135–141 Walker C (1995) In: Verma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, New York, pp 25–29 Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363 Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425 Yadav K, Aggarwal A, Singh N (2013) Arbuscular mycorrhizal fungi (AMF) induced acclimatization, growth enhancement and colchicine content of micropropagated Gloriosa superba L. plantlets. Ind Crop Prod 45:88–93 Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in coastal vegetation on Okinawa Island and effect of the isolated fungi on growt of sorghum under salt-treated conditions. Mycorrhiza 18:241–249 Yang H, Dai Y, Wang X, Zhang Q, Zhu L, Bian X (2014) Meta-analysis of interactions between arbuscular mycorrhizal fungi and biotic stressors of plants. Sci World J 2014:7. https://doi. org/10.1155/2014/746506 Yano-Melo AM, Saggin OJ, Lima-Filho JM, Melo LC, Maia LC (1999) Effect of arbuscular mycorrhizal fungi on the acclimatization of micropropagated banana plantlets. Mycorrhiza 9:119–123 Zai X, Qin P, Wan S, Zhao F, Wang G, Yan D, Zhou J (2007) Effects of arbuscular mycorrhizal fungi on the rooting and growth of beach plum (Prunus maritima) cuttings. J Hortic Sci Biotechnol 82(6):863–866 Zaid A, de Wet PF, Oihabi A (2002) Diseases and pests of date palm. In: Zaid A (ed) Date palm cultivation FAO paper No. 156, Rome, Italy, pp 227–281 Zarea MJ (2010) Conservation tillage and sustainable agriculture in semi-arid dryland farming. In: Lichtfouse E (ed) Biodiversity, biofuels, agroforestry and conservation agriculture. Springer, Dordrecht, pp 195–232


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Zarea MJ, Goltapeh EM, Karimi N, Varma A (2013) Sustainable agriculture in saline-arid and semiarid by use potential of AM fungi on mitigates NaCl effects. In: Goltapeh EM et al (eds) Fungi as bioremediators. Springer-Verlag, Berlin/Heidelberg, pp 347–369 Zegaye F, Khalid A, Hasnaoui A, Serghini HC, El Amrani A (2012) Ectomycorrhization of date palm and carob plants. Global J Sci Front Res Bio Sci 12(8):13–20 Zhang T, Tian CY, Sun Y, Bai DS, Feng G (2012) Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut. Desert. J Arid Land 4(1):43–51 Zhao ZW, Qin XZ, Li XW, Cheng LZ, Sha T, Wang GH (2001) Arbuscular mycorrhizal status of plants and the spore density of arbuscular mycorrhizal fungi in the tropical rain forest of Xishuangbanna, southwest China. Mycorrhiza 11:159–162 Zhu JK, Chinnusamy V, Jagendorf A (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

Chapter 12

Applications of Haloalkaliphilic Fungi in Mycoremediation of Saline-Alkali Soil Shi-Hong Zhang and Yi Wei

12.1 Introduction Plants, the primary producers on land, are the main food sources and raw materials for feed and industry. However, for plants, soil has special significant meanings. In other words, plants are not only rooted in the soil but also absorb essential nutrients and water from the soil for growth, development, and reproduction. Unfortunately, due to the presence of harmful substances such as the redundant salt or alkali contained in soil, some types of soils are not so effective and suitable for plant growth. High salt accumulation in soils imposes multiple negative effects on soil organic matter decomposition and available nutrient uptake (Rietz and Haynes 2003; Karlen et al. 2008) and then on plant growth and development and crop yield and quality (Rady 2011). Soil salinization is an increasingly serious environmental problem on a global scale. It is estimated that 6.5% of the total land has been salinized, and this area continues to expand (Wang et al. 2003; Yadav et al. 2011). Soda saline-alkaline soils are significantly harmful to agriculture due to the accumulation of solutes that induces a primary soil alkalization process, with Na2CO3 and NaHCO3 being the major sources for soil alkalization, and the coexistence of salinity and alkalinity and difficulties for management. Soda saline-alkaline soils occur within the boundaries of at least 75 countries (Szabolcs 1994), and the severity is increased steadily in several major irrigation schemes throughout the world (Ghassemi et al. 1995). Nowhere in China is the issue more serious than in the Songnen Plain of Northeast China which is largely a basin surrounded by mountains and has very poor drainage (Fig. 12.1). Soil alkali is the major ecological gradient and the main limiting factor for food security in the area (Gao et al. 1996). Therefore, efficacy strategies to remediate such soil are urgent. S.-H. Zhang (*) • Y. Wei College of Plant Sciences, Jilin University, Changchun, China e-mail: [email protected] © Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9_12

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Fig. 12.1 Songyuan soda saline-alkaline soil in Songnen Plain of Northeast China (Photos taken in 2015). The white snow-like layer of land is soda salt that returns to the surface of the soil (In a soil level of 0–20 cm: the maximum concentration of NaCl = 21 g/kg, the maximum pH = 10.4)

In general, several remediation measures, involving physical tillage operations, chemical amendments, leaching with water, and plant-associated phytoremediation, have been used to ameliorate saline soils (Qadir et al. 2007). Among these methods, phytoremediation has been considered as one of the most prospective methods on the account of its significant ecological, environmental, and economic effects (Ghaly 2002; Ilyas et al. 1993; Robbins 1986). So far, the core technique for the success of the phytoremediation has relied on the selection and application of appropriate plants such as salt-resistant or salt-tolerant species and their cropping sequence. However, the upper limit of plant resistance limits the application range of this method. Above all, in severe saline soils, ecosystems are rather simple and fragile: microbes such as fungal flora are rare, let alone plants. An alternative but available technique is the application of organic matter conditioners, which can both ameliorate and increase the fertility of saline soils (Melero et al. 2007). Salt-affected soils generally exhibit poor structural stability due to low organic matter content. Actually, many researchers have suggested that the structural stability of soil can be improved by the addition of organic materials (Tejada et al. 2006; Oo et al. 2013). The addition of maize straw to a saline soil, for example, could decrease the negative effects of salinity on the microbial community and mineralization (Wichern et al. 2006). Compared to a non-amended control, the amendments, which were applied at 4.5 kg organic matter m-3, dramatically promoted plant growth; improved soil structure; increased the cation exchange capacity, organic carbon, and available nutrients; and reduced the salt content, electrical conductivity, and exchangeable

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sodium percentage; in addition, combination of green waste compost, sedge peat and furfural residue has substantial potential for ameliorating saline soils in the coastal areas of northern China, and it works better than each amendment alone (Wang et al. 2014). During the natural process of soil formation, the maturation and health of soil are mainly influenced by microbes in addition to plants and related organisms. Soil microorganisms have the ability to adapt to or tolerate salinity, especially when regularly confronted with high salt environment (Sparling et al. 1989). There are examples of microbes thriving in high concentration of salt ponds (Casamayor et al. 2002), reflecting the evolutionary potential of microorganisms. However, fungi tend to be sensitive to salt stress, indicated by decreasing ergosterol contents in the soil (Sardinha et al. 2003). In addition, fungal diversity has been verified to be declined in a long-term stress (Van Bruggen and Semenov 2000). In general, elevated salinity leads to a stronger decline of fungi than bacteria, then decreases soil microbial biomass and activity, and further affects the turnover of organic matter. This creates a vicious cycle that finally causes a more infertile and desolation soil. Thereby it is not difficult for us to understand why the ecosystem of saline-alkaline land is simple and fragile. Soil-inhabitant fungi play potential roles in buffering salinity and alkalinity stress through absorbing and/or constraining salt ions, secreting organic acids and/ or macromolecular degradation enzymes, and other benefits of biomasses for soil health (Fig. 12.2); thus, haloalkaliphilic fungi are excellent biological resources for soil mycoremediation. Microbial application for amelioration of saline soils is gaining popularity due to its better amelioration and reduction in economic and

Fig. 12.2 Mechanism model of mycoremediation of saline-alkali soil through adding haloalkaliphilic fungi and crop straw in soil

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environmental costs. A study by Sahin et al. (2011) on irrigated land in the Igdir plain, Northeast Turkey, was designed to determine the effects of microbial inoculation (fungi and bacteria) on saturated hydraulic conductivities of four saline-sodic soils ameliorated with gypsum. The results suggested that microbial mixtures played a key role in increasing the saturated hydraulic conductivities under saline soils. Within the last few decades, a series of halophilic and alkaliphilic fungi that are capable to live in high salt and high alkaline or both environments, for example, Eurotium herbariorum, which lives at 340 g/L total dissolved salts (the Dead Sea) (Kis-Papo et al. 2001a; Yan et al. 2005), have been isolated and characterized and further studied. Some halo- and/or alkaliphilic fungi are potential agents for bioremediation in saline and alkaline soils. On the other hand, they are at least genetic pools for saline- and alkaline-resistant (or tolerant) and organic matter degradation gene cloning, which will be used to improve or create high activity fungi for soil remediation. In this chapter, we highlight the abiotic stress resistance mechanisms and resistant genes in extremophilic fungi. In addition, application strategies for anti-abiostress genetic engineering are also discussed.

12.2 Haloalkaliphilic Fungi: Isolation and Characterizations Halophilic fungi that require at least 0.3 M concentrations of salt (e.g., sodium salts) to grow optimally are capable of thriving in high salt environments (Madigan et al. 2012). Similar to halophilic fungi, halotolerant fungi are another species which tend to live in saline areas but do not require elevated concentrations of salt. However, it is actually difficult to define the boundaries between halotolerant and halophile. The establishment of the difference is harder in fungi; even up to date, the limits between halotolerant and halophilic strains are not outspoken (Arakaki et al. 2013). Therefore, in this chapter, we consider halophilic fungi as a general designation. Alkaliphilic fungi are a class of extremophilic microbes capable of surviving in alkaline (pH roughly 8.5–11.5) environments, growing optimally around a pH of 10. Halophilic fungi growing in alkaline environments are adapted to high levels of pH value as well as high levels of ions and are described as haloalkaliphilic, rather than merely halophilic or alkaliphilic, and thus haloalkaliphilic fungi are those alkaliphilic fungi that at the same time require high salt content to survive (Horikoshi 1999). Halophilic fungi have been isolated mainly from oceans or related places with a high concentration of salt, such as the famous Dead Sea, Qinghai Salt Lake in Qing- Tibet Plateau, the Great Salt Lake in Utah, and Owens Lake in California, although some reports demonstrate that halophilic fungi are not restricted to saline habitats and can be found in normal environments (Abdel-Fafez 1981; Moubasher et al. 1990; Nielsen et al. 1995; Castillo and Demoulin 1997; Arahal et al. 1999; Pinar et al. 2001; Santos et al. 2004; Echigo et al. 2005; Abrahao et al. 2008; Arakaki et al. 2013). Till now, many studies on biodiversity and physiology have focused on the characterization of halophilic fungi present in saline and hypersaline ecosystems;


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and many species of ascomycetes, and some basidiomycetes, have been described with the ability to grow in these environments (Butinar et al. 2005; Gunde-Cimerman et al. 2005). The Dead Sea is one of the most typical salt habitats for microorganisms, in which 340 g/L total salt is dissolved, and a variety of filamentous fungi have been isolated by Nevo and colleagues. Gymnascella marismortui is a remarkable salt- tolerant fungi isolated from surface water to 300 m down in the Dead Sea (Buchalo et al. 1998). This isolate can grow optimally at NaCl concentrations between 0.5 and 2 M without being affected by ionic composition (Buchalo et al. 1998, 1999, 2000; Molitoris et al. 2000), suggesting its adaption to the high salt conditions and requirement for high salt concentrations. Among the 476 fungal isolates from the Dead Sea, the species Aspergillus terreus, A. sydowii, A. versicolor, Eurotium herbariorum, Penicillium westlingii, Cladosporium cladosporioides, and C. sphaerospermum were isolated consistently and probably from a stable core of the community; in addition, approximately 43% of the isolates belongs to the genera Eurotium and Aspergillus (Kis-Papo et al. 2001b). Recently, Nazareth and Gonsalves (2014) confirmed a true halophilic fungus Aspergillus penicillioides through characterizing 39 strains of A. penicillioides isolated from the different saline habitats. The fungus can only grow on the media supplemented with at least 10% solar salt. It cannot grow without extra salt added in media. The results demonstrated that most of the isolates tested had a minimum salt requirement of 5% for growth, suggesting the true halophilic nature in A. penicillioides. A. penicillioides was common in saline habitats, which implies the ubiquitous distribution and extensive adaptability of the fungus in varied environments. Given that A. penicillioides species have no sexual life cycle (Tamura et al. 1999; Gostincar et al. 2010), which consequently inhibits gene flow, this species will have a great value in use. In addition to A. penicillioides, Gymnascella marismortui (Buchalo et al. 1998), Wallemia ichthyophaga (Zalar et al. 2005; Gunde-Cimerman et al. 2009), (Elmeleigy et al. 2010), and Aspergillus unguis (Nazareth et al. 2012) have also been reported to be obligate halophiles. Some halophilic fungi, such as Aspergillus niger and Cladosporium cladosporioides, were also isolated from sand and mud on the surrounding shore or from inflowing freshwater of floods and springs (Kis-Papo et al. 2001a, b). Previously, we isolated the halophilic fungus Aspergillus glaucus CCHA from air-dried wild vegetation at the surface periphery of a solar salt field (Liu et al. 2011). This species shows an extreme salt tolerance, with a salinity range for growth from 5% to 32% (saturation, NaCl) (Liu et al. 2011). Above all, to our surprise, the species survives in a broad pH value range of 2–11.5, indicating A. glaucus CCHA belongs to a haloalkaliphilic fungus. Further investigation indicated that A. glaucus CCHA can be induced by enhancing pH value (> 8.0) to produce a variety of organic acids, such as citric acid, oxalic acid, and malic acid, as well as possess multiple resistance to aridity, heavy metal ions, and high temperatures (Fig. 12.3). All these properties suppose that the species is rather valuable in soil remediation practice. In comparison with the isolated halophilic fungi, alkaliphilic fungi reported are relatively less. Hozzein et al. (2013) isolated 117 alkaliphilic and alkaline-resistant

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Fig. 12.3 Extreme salt and alkali resistance of Aspergillus flavus CCHA grown on PDA medium (pH = 7.0, 35 °C) supplemented with 30% NaCl for 6 days (A) or grown on PDA medium (pH = 11.5, 35 °C) for 9 days (B)

microorganisms from 30 soil samples, which were collected from different six localities representing Wadi Araba, Egypt. The soil samples from the different six localities were slightly saline, and the pH values of the tested soil samples fall in the alkaline range. Through adjusting the pH value to 10 after sterilization by addition of sterilized 10% Na2CO3 solution, they only screened 4 fungal isolates among 117 alkaliphilic and alkaline-resistant microorganisms. Unfortunately, the authors did not detail what species the four isolates are. Alkaliphilic fungi were also isolated from industrial effluents. Aspergillus nidulans KK-99 that has been isolated from the industrial effluents of Shreyans Paper Industry Limited, Ahmedgarh, Punjab, India, for example, is adapted to grow in alkalescent environment (pH 10.0) (Taneja et al. 2002 ), and the alkaliphilic fungus Myrothecium sp.IMER1 was isolated from China (Zhang et al. 2007). In recent years, the isolation and characterization researches of halophilic fungi have been developed rapidly in China. In addition to A. glaucus CCHA, other promising halophilic fungi have been isolated and characterized as well. The new halotolerant species of Alternaria, A. xiaochaidanensis, is described and illustrated for instance. The specimen was collected from a salt lake in Qinghai-Tibet Plateau. China has plentiful biodiversities, and particularly has many typical hypersaline environments, such as Chaka Salt Lake and Qarhan Salt Lake in Qinghai, Barkol Salt Lake in Xinjiang, Yuncheng Salt Lake in Shanxi, and Baicheng soda saline- alkali land in Jilin. All these environments are suitable for extremophilic fungi and other microorganism colonization. It is a significant task to carry out isolation and identification of extremophilic fungi in China.

12.3 S aline and/or Alkaline Resistance Genes in Extremophilic Fungi As described above, most of the isolated extremophilic fungi are characterized only by one distinctive extreme factor (saline or alkaline), despite the accelerated description of novel species. Aspergillus glaucus CCHA as an extreme fungus is the few detailed haloalkaliphiles, which with no doubt will limit the applications of


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haloalkaliphilic fungi. Thus, genetic improvement of normal soil fungi is necessary, and surely, the premise is that we must have the relevant genes that are resistant to salt, alkali, or both. The yeast fungus Saccharomyces cerevisiae is with moderate levels of tolerance. It presents a rather poor performance in the presence of salt, alkali, drought, extreme temperature, and other stressors (Prista et al. 2002, 2005; Serrano and Gaxiola 1994). Thus, S. cerevisiae is not the best model organism, neither for salt tolerance nor for sensitivity to salt. However, S. cerevisiae has been actually extensively applied in resistance field as a model for being manipulated conveniently due to fast growth rate and easy transformation. The high-osmolarity glycerol (HOG1) pathway, which is an essential stress-signaling module, has been extensively studied in fungi from the yeast S. cerevisiae to the filamentous fungus Trichoderma harzianum (Brewster et al. 1993; Delgado-Jarana et al. 2006). HOG1 functions also in extremophilic fungi. Nevo group testified that E. herbariorum HOG1 is highly similar to homologs from no-extreme fungi like Aspergillus nidulans, S. cerevisiae, and Schizosaccharomyces pombe (Yan et al. 2005). Like S. cerevisiae, the yeast Debaryomyces hansenii that is usually found in salty environments has been extensively investigated in recent years. The salt-loving fungus is able to accumulate high concentrations of sodium without having any damages and also grow well under additional stress factors such as high temperature and extreme pH in the presence of 0.25 M NaCl (Almagro et al. 2000). Through screening S. cerevisiae transformants that contain the genomic library prepared from D. hansenii (Prista et al. 2002), a series of genes associated with salt tolerance were identified and characterized. For example, the DhGZF3 gene, which encodes GATA transcription factor homologs to Dal80 and Gzf3 in S. cerevisiae, has been functionally analyzed in D. hansenii, but the gene was verified to be a negative transcription factor when it was expressed in S. cerevisiae (García-Salcedo et al. 2006). Using the cDNA library from the stress-tolerant basidiomycete yeast Rhodotorula mucilaginosa, more than 100 S. cerevisiae transformants that are tolerant to concentrations of various osmolites have been screened by Gostinčar and Turk (2012). Among the sequenced clones, 12 genes mediated increased stress tolerance in the R. mucilaginosa transformants. Recently, from the D. hansenii genome database, Pereira et al. (2014) analyzed nine candidates of polyol/H(+) symporters by heterologous expression in S. cerevisiae. Five distinct polyol/H(+) symporters were confirmed, among which two symporters were tested to be specific for uncommon substrates as galactitol and D-(+)-chiro-inositol. Interestingly, the stress tolerance genes in extremophilic fungi are scarcely reported and their functions need more researches. These genes could be of significantly importance in transgenic biotechnology. Above all, the abiotic stress resistance genes isolated from extremophilic fungi appear to be more resistant than homologs from no extremophiles. EhHOG, as mentioned above, is the E. herbariorum MAPK kinase gene similar to HOG1 homologs from A. nidulans, S. cerevisiae, Schizosaccharomyces pombe, and most other fungi; but hog1 mutant complemented with EhHOG outperformed the wild type under high salt and

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freezing-thawing conditions (Yan et al. 2005), indicating the higher genetic fitness of EhHOG in comparison with the corresponding HOG from S. cerevisiae. Some genes isolated from the halophilic fungus A. glaucus were also found to be more resistant to osmotic stress than the common fungi such as S. cerevisiae and Magnaporthe oryzae. A yeast expression library containing full-length cDNAs of A. glaucus was constructed and used to screen salt resistance transformants in our lab at Jilin University (Liu et al. 2011; Fang et al. 2014). The ribosomal protein L44 (RPL44), one of the proteins of the large ribosomal subunit 60S, was obtained according to its association with salt resistance. In comparison with the homologous sequence from M. oryzae, MoRPL44 in a yeast expression system, the results indicated that yeast cells with overexpressed AgRPL44 were more resistant to salt, drought, and heavy metals than yeast cells expressing MoRPL44 at a similar level of stress. In addition, when AgRPL44 was introduced into M. oryzae, the transformants also displayed significantly enhanced tolerance to salt and drought, indicating the unique osmosis resistance ability from the halophilic fungus (Liu et al. 2014). Similar results were also obtained in the studies of another ribosomal protein subunit of AgRPS3aE (Liang et al. 2015), the AgglpF (Liu et al. 2015), a 60S protease subunit, and 14 other unknown or predicted genes including the cell wall degrading enzymes such as chitinase, cellulase, and glucanase (Zhang and Chen, unpublished). The citric acid cycle is a key metabolic pathway that connects carbohydrate, fat, and protein metabolism. Through catabolism of sugars, fats, and proteins, the two- carbon organic product acetyl-CoA is produced which enters the citric acid cycle. In the citric acid cycle, seven organic acids as the intermediates such as citrate, isocitrate, succinate, fumarate, malate, and oxaloacetate are regenerated during each cycle turn. The reactions of the cycle are carried out by eight enzymes that completely oxidize acetate, in the form of acetyl-CoA, into two molecules each of carbon dioxide and water. The high pH enduring ability of A. glaucus makes it an organic production strain (Barnes and Weitzman 1986). When A. glaucus was cultured in alkaline medium, the key enzymes (e.g., citrate synthase, aconitase, isocitrate dehydrogenase, succinyl-CoA synthetase, fumarase, malate dehydrogenase) of the three carboxylic acid cycle were significantly upregulated (Zhang and Liu, unpublished), suggesting these genes contribute to the high pH enduring ability of A. glaucus. Therefore, alkali resistance will be improved in A. glaucus or other fungi with the same characteristics through overexpressing one of these genes in fungal candidates. Two Thermomyces lanuginosus ATP-dependent Lon proteases that are highly conserved with multiple roles in diverse species were genetically studied recently (Cui et al. 2017). The results demonstrated that both mitochondrial and peroxisomal Lons exhibit synergistic effects on resistance to multiple stressors, such as salt and alkali in T. lanuginosus. As we know, the thermophilic fungus T. lanuginosus is sensitive to salt and alkali, but the salt resistance activity provided by both Lons is very useful in practice. Actually, the MAP1/Lon in the rice blast fungus Magnaporthe oryzae is also with the same activity (Li et al. 2014; Cui et al. 2015). The common features of all these genes are highly conserved, at least not specific to extremo-


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philic fungi, but they obviously support transgenic cells or organisms surviving under stress conditions, suggesting special mechanisms to be uncovered in the future and potential values for genetic engineering.

12.4 G ene Cloning of Cellulase with Stable Activity in Saline-Alkali Soil Cellulose is the most abundant biomass on Earth. From the viewpoint of carbon cycle, the available organic matters in soil are mainly derived from the degradation of various crop remains such as fallen leaves and stalks. However, as mentioned above, the microbe community of saline-alkaline land is simple and fragile, and elevated salinity leads to a stronger decline of fungi than bacteria, then decreases soil microbial biomass and activity, and further affects the turnover of organic matter. Therefore, fungi with not only both salt- and alkali-resistant properties but also the ability of producing and secreting cellulose-degrading enzyme are badly needed. Salt and alkali resistance genes are capable of improving genetically soil fungi and enhancing their resistance to extreme environments. On the other hand, in order to be beneficial to the soil, fungi must possess the ability to produce and secrete a large number of hydrolytic enzymes that function to degrade plant organic matter (e.g., maize, wheat, or rice straw), such as cellulose, semi-cellulose, or lignin enzymes, because soil enzyme activities are closely related to soil properties, soil types, and environmental conditions and are now widely used as important indicators of soil quality and soil biological activities (Rietz and Haynes 2003; Yuan et al. 2007). Of course, these enzymes are not ordinary enzymes; in other words, after being secreted into the extracellular ambient, these enzymes must maintain enough activities under high salt or alkali conditions. The cellulase complex includes endoglucanases (EC 3.2.1.4), exoglucanases (EC 3.2.1.91), and β-glucosidases (EC 3.2.1.21). Endoglucanases randomly attack the internal chain of cellulose to produce cellooligosaccharides. Exoglucanases catalyze the hydrolysis of crystalline cellulose from the ends of the cellulose chain to produce cellobiose, which is ultimately hydrolyzed to glucose by β-glucosidases (Béguin and Aubert 1994; Tomme et al. 1995). Trichoderma reesei and Penicillium janthinellum are known to be excellent cellulase producers, but the studied cellulases are acidic and neutral, respectively (Wang et al. 2005; Qin et al. 2008; Mernitz et al. 1996). Aspergillus niger is recognized as one of the more efficient cellulose- degrading microorganisms, which can secrete large amounts of different cellulases for the fermentation (Schuster et al. 2002). The endoglucanase B (EGLB), encoded by the endoglucanase gene (GenBank GQ292753) of Aspergillus niger BCRC31494, has been used in the fermentation industry because of its alkaline and thermal tolerance (Li et al. 2012). The open reading frame length of the EGLB gene is 1217 bp with five introns. The EGLB was assigned to glycosyl hydrolase family 5 of the cellulase superfamily. When the recombinant cDNA was expressed in Pichia

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pastoris, a purified protein with a molecular weight of 51 kDa in size was obtained. The enzyme was specific for substrates with β-1,3 and β-1,4 linkages, and it exhibited optimal activity at 70 °C and pH 4. Interestingly, the relative activity of the recombinant EGLB at pH 5–9 was significantly higher than that of the wild type. Even better, the recombinant enzyme displayed broad pH stability; when incubated at 70 °C in the pH value range of 4.0 to 8.0, the enzyme activity remained higher than 50%. All these advantages, particularly the broad pH value range, make the endoglucanase EGLB gene applicable in genetic improvement of fungi for haloalkaline soil remediation. Based on the genome sequence and the CAZy annotation of the haloalkaliphilic fungus A. glaucus CCHA that can grow on media with a salinity range from 5% to 32% and a broad pH value range from 2.0 to 11.5, we recently found that there is only one gene belonging to GH5 family (data unpublished), implying the low ability of cellulase degradation of the species or the high degradation activity of the single GH5 member. The A. glaucus CCHA glycoside hydrolase family 5 member (GH5), termed as AgCel5A, was cloned and heterologously expressed in Pichia pastoris GS115. The open reading frame of Agcel5A consists of 1509 base pairs, which encode a polypeptide of 502 amino acids (involving a signal peptide of 18 residuals at the N-terminus). The theoretical molecular mass and isoelectric point (pI) of the protein are 52.8 kDa and 5.2, respectively. AgCel5A has four potential N-glycosylation sites and three O-glycosylation sites, which shows high similarity to the characterized GH5 β-glucosidases from Aspergillus niger (65%) and Trichoderma reesei (31%). The recombinant enzyme exhibited maximal activity at pH 5.0, which is similar as PdCel5C from Penicillium decumbens (Liu et al. 2013). However, the enzyme is much more stable; at pH 8.0–10.0, it retains more than 70% of its maximum activity. Meanwhile, AgCel5A as well exhibits a stable degradation activity under conditions of high salt (NaCl). In the presence of 4 M NaCl, AgCel5A still retains 90% activity even after 4-h preincubation. Interestingly, along with the increase of NaCl concentration, the activity of AgCel5A increases as well and reaches the peak value (approximately 220%) at 0.5 M NaCl, suggesting the activator action of the enzyme. Overall, the double resistances to salt and alkali make the endoglucanase AgCel5A an ideal candidate for genetic improvement of soil fungi and industrial applications. So far, less cellulase genes with multiple resistances to salt and alkali have been cloned from fungi (Henrissat et al. 1985). In contrast, such genes cloned are mainly from bacteria (e.g., Paenibacillus sp., Thermomonospora sp.) (Kanchanadumkerng et al. 2017; Zarafeta et al. 2016) and guts of animals such as higher termites. For example, CelDZ1, the novel thermotolerant and exceptionally halostable GH5 cellulase from an Icelandic Thermoanaerobacterium hot spring isolate, is a glycoside hydrolase with optimal activity at 70 °C and pH 5.0 that exhibits good thermostability, high halotolerance at near-saturating salt concentrations, and resistance toward metal ions and other denaturing agents. In terms of the genetic improvement for fungal resistance to salt and alkali, these cellulases are also appropriate candidates to be considered.


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12.5 S trategies for Genetically Improving Haloalkaliphilic Fungi Soil fungi that play important roles in degrading the insoluble organic matter such as crop straw into soluble and easily absorbed nutrients for crop plants; therefore, application of organic matter supplemented with fermentation fungi in saline-alkali soil is a practical and feasible strategy for soil remediation. Surely, these fungi suitable for soil remediation must first have the ability to survive and then function. Generally speaking, according to the different biological characteristics between fungi from fertile soil and saline-alkali soil, the fungi from saline-alkali soil are rich in salt- and/or alkali-resistant system but poor in cellulose degradation system; on the contrary, the fungi from fertile soil are just the opposite. To solve these problems, we propose the following genetic strategies to improve haloalkaliphilic fungi with high activity of cellulases: based on the naturally isolated haloalkaliphilic fungus as transformational receptor and the cloned high activity cellulase gene from fertile soil fungi, the cellulase gene will be transferred into the haloalkaliphilic fungus. Candidate strains of the transgenic fungus will not only possess salt and alkali resistance but also possess high degradation activity of cellulase; taking salt- and alkali-resistant genes as transgenes, the fertile soil fungi as transformational target will be endowed with multiple resistance to saline-alkali soil environment and then play roles in remediating saline-alkali soil. Beyond above strategies, inducible promoters are available in creating genetically modified haloalkaliphilic fungi. The salt- and/or alkali-resistant gene or genes driven by a salt or alkali inducible promoter from an extremophilic fungus or high activity cellulase genes driven by cellulose inducible promoter from fertile fungi constitute the so-called two-component sensor systems (de Wit 1992). This strategy will reduce energy ATP waste and other negative physiological effects on the genetically modified fungi.

12.6 Concluding Remarks Saline-alkaline soils happen within the boundaries of at least 75 countries (Szabolcs 1994), and the severity is increased steadily in several major irrigation schemes throughout the world (Ghassemi et al. 1995). Phytoremediation is one of the most prospective methods on the account of its significant ecological, environmental, and economic effects. (Ghaly 2002; Ilyas et al. 1993; Robbins 1986), but it takes more than 8 years to see results. Soil structural stability can be improved by the addition of organic materials (Tejada et al. 2006; Oo et al. 2013; Wang et al. 2014); therefore, an alternative technique is the application of organic matter conditioners, which can both ameliorate and increase the fertility of saline soils (Horikoshi 1999; Melero et al. 2007).

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Fig. 12.4 The three - year - mycoremediation of soda saline-alkali soil by using amendments supplemented with the mixed strains of Aspergillus glaucus CCHA, Aspergillus terreus, Aspergillus penicillioides, Aspergillus oryzae, Aspergillus candidus, Aspergillus erythrocephalus, and Aspergillus itaconicus (right) or not (left). The experimental location is in Northeast Flower Village, Songyuan soda saline-alkaline soil in Songnen Plain of Northeast China (the position has been mentioned in Fig. 12.1). Properties of the saline soil before organic amendments were applied belong to heavy soda saline-alkali soil

Soil-inhabitant fungi play irreplaceable roles in maintaining soil healthy; they build a solid bridge between insoluble organic matter and soil nutrients through producing cellulose degradation enzymes such as cellulase and other bioprocesses. Thus, haloalkaliphilic fungi are excellent biological resources for soil mycoremediation. Many researchers have focused on the characterization of halophilic fungi present in saline and hypersaline ecosystems; and many species, such as most Aspergillus fungi, have been described with the ability to grow in these environments. Most Aspergillus strains like the halophilic fungus Aspergillus glaucus CCHA behave in an extreme salt and alkali tolerance, implying the valuable haloalkaliphilic fungi, and actually we have been trying to test their applications in the bioremediation of the severe saline-alkali soil in the northeast of China (Fig. 12.4). Few haloalkaliphilic fungi have been isolated so far, and there are many fungi to be isolated and developed urgently. According to the molecular genetics of fungi, fungi can be improved through transferring functional gene/genes. A series of salt and/or alkali resistance genes have been isolated and functionally analyzed, which provides candidates for genetic improvement of soil fungi; on the other hand, in order to enhance the ability of cellulose degradation of haloalkaliphilic fungi, more genes of cellulases with salt and


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alkali stability are in need. Through using these genes, two strategies can be employed to obtain multiple resistant and better degradation strains. Surely, natural ideal strains are still the first choice; therefore, it is a long-term task to isolate and screen suitable strains from natural environments. Acknowledgments This work was partially supported by two grants of the National Natural Science Foundation of China (grant nos. 31671972 and 31670141) and a project of the Ministry of Science and Technology of China (grant no. 2016YFD0300703). The authors would like to thank the members of Zhang laboratory at Jilin University, and the collaborators Hon-Ming LAM, Zhen- Dong CHEN, Run-Zhi TAO, and Chi ZHU, who gave us a lot of encouragement and assist in promoting the transformation of the scientific and technological achievements about saline-alkali soil mycoremediation.

References Abdel-Fafez S (1981) Halophilic fungi of desert soils in Saudi Arabia. Mycopathologia 75:75–80 Abrahao MC, Gugliotta AM, Da Silva R, Fujieda RJ, Boscolo M, Gomes E (2008) Ligninolytic activity from newly isolated basidiomycete strains and effect of these enzymes on the azo dye orange II decolourisation. Ann Microbiol 58:427–432 Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J, Loureiro-Dias MC (2000) Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int J Food Microbiol 56:191–197 Arahal DR, Marquez MC, Volcani BE, Schleifer KH, Ventosa A (1999) Bacillus marismortui sp. nov., a new moderately halophilic species from the Dead Sea. Int J Syst Bacteriol 49:521–530 Arakaki R, Monteiro D, Boscolo R, Gomes E (2013) Halotolerance, ligninase production and herbicide degradation ability of basidiomycetes strains. Braz J Microbiol 44:1207–1214 Barnes SJ, Weitzman PD (1986) Organization of citric acid cycle enzymes into a multienzyme cluster. FEBS Lett 201(2):267–270 Béguin P, Aubert JP (1994) The biological degradation of cellulose. FEMS Microbiol Rev 13:25–58 Brewster JL, de Valoir T, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259:1760–1763 Buchalo AS, Nevo E, Wasser SP, Oren A, Molitoris HP (1998) Fungal life in the extremely hypersaline water of the Dead Sea: first records. Proc R Soc Lond B 265:1461–1465 Buchalo AS, Nevo E, Wasser SP, Oren A, Molitoris HP, Volz PA (2000) Fungi discovered in the Dead Sea. Mycol Res News 104:132–133 Buchalo AS, Wasser SP, Molitoris HP, Volz PA, Kurchenko I, Lauer I, Rawal B (1999) Species diversity and biology of fungal life in the extremely hypersaline water of the Dead Sea. In: Wasser SP (ed) Evolutionary theory and processes: modern perspectives. papers in honour of Eviatar Nevo. Kluwer Academic Publishers, Dordrecht, pp 293–300 Butinar L, Zalar P, Frisvad JC, Gunde-Cimerman N (2005) The genus Eurotium-members of indigenous fungal community in hypersaline waters of salterns. FEMS Microbiol Ecol 51:155–166 Casamayor EO, Massana R, Benlloch S, Øvreås L, Díez B, Goddard VJ, Gasol JM, Joint I, Rodríguez-Valera F, Pedrós-Alió C (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 4:338–348 Castillo G, Demoulin V (1997) NaCl salinity and temperature effects on growth of three wood- rotting basidiomycetes from a Papua New Guinea coastal forest. Mycol Res 101:341–344 Cui X, Wei Y, Wang Y, Zheng Y, Li J, Wong F, Liu S, Yan H, Jia B, Liu J, Zhang S (2015) Proteins interacting with mitochondrial ATP-dependent Lon protease (MAP1) in Magnaporthe oryzae are involved in rice blast disease. Mol Plant Pathol 16(8):847–859

230


Cui X, Wei Y, Xie XL, Chen LN, Zhang SH (2017) Mitochondrial and peroxisomal Lon proteases play opposing roles in reproduction and growth but co-function in the normal development, stress resistance and longevity of Thermomyces lanuginosus. Fungal Genet Biol 103:42–54 de Wit PJ (1992) Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu Rev Phytopathol 30:391–418 Delgado-Jarana J, Sousa S, González F, Rey M, Llobell A (2006) ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152(Pt 6):1687–1700 Echigo A, Hino M, Fukushima T, Mizuki T, Kamekura M, Usami R (2005) Endospore of halophilic bacteria of the family Bacillaceae isolated from nonsaline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Syst 1:1–13 Elmeleigy MA, Hoseiny EN, Ahmed SA, Alhoseiny AM (2010) Isolation, identification, morphogenesis and ultrastructure of obligate halophilic fungi. J Appl Sci Environ Sanit 5:201–202 Fang J, Han X, Xie L, Liu M, Qiao G, Jiang J, Zhuo R (2014) Isolation of salt stress-related genes from Aspergillus glaucus CCHA by random overexpression in Escherichia coli. ScientificWorldJournal 2014:620959. https://doi.org/10.1155/2014/620959 Gao Q, Yang XS, Yun R, Li CP (1996) MAGE, a dynamic model of alkaline grassland ecosystems with variable soil characteristics. Ecol Model 93:19–32 García-Salcedo R, Casamayor A, Ruiz A, González A, Prista C, Loureiro-Dias MC, Ramos J, Ariño J (2006) Heterologous expression implicates a GATA factor in regulation of nitrogen metabolic genes and ion homeostasis in the halotolerant yeast Debaryomyces hansenii. Eukaryot Cell 5(8):1388–1398 Ghaly FM (2002) Role of natural vegetation in improving salt affected soil in northern Egypt. Soil Tillage Res 64:173–178 Ghassemi F, Jakeman AJ, Nix HA (1995) Salinisation of land and water resources: human causes, extent, management and case studies. CABI Publishing, Wallingford Gostinčar C, Grube M, De Hoog S, Zalar P, Gunde-Cimerman N (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11 Gostinčar C, Turk M (2012) Extremotolerant fungi as genetic resources for biotechnology. Bioengineered 3(5):293–297. https://doi.org/10.4161/bioe.20713 Gunde-Cimerman N, Butinar L, Sonjak S, Turk M, Ursic V, Zalar P, Plemenitaš A (2005) Halotolerant and halophilic fungi from coastal environments in the Arctics. In: Gunde- Cimerman N, Oren A, Plemenitas A (eds) Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya. Springer, Dordrecht, pp 397–423 Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241 Henrissat B, Driguez H, Viet C, Schulein M (1985) Synergism of cellulases from Trichoderma reesei in the degradation of cellulose. Nat Biotechnol 3:722–726 Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750 Hozzein WN, Ali MIA, Ahmed MS (2013) Antimicrobial activities of some alkaliphilic and alkaline-resistant microorganisms isolated from Wadi Araba, the eastern desert of Egypt. Life Sci J 10(4):1823–1828 Ilyas M, Miller RW, Qureshi RH (1993) Hydraulic conductivity of saline-sodic soil after gypsum application and cropping. Soil Sci Soc Am J 57:1580–1585 Kanchanadumkerng P, Sakka M, Sakka K, Wiwat C (2017) Characterization of endoglucanase from Paenibacillus sp. M33, a novel isolate from a freshwater swamp forest. J Basic Microbiol 57(2):121–131. https://doi.org/10.1002/jobm.201600225 Karlen DL, Andrews SS, Wienhold BJ, Zobeck TM (2008) Soil quality assessment: past, present and future. Electr J Integr Biosci 6(1):3–14 Kis-Papo T, Grishkan I, Oren A, Nevo E (2001a) Comparison of fungal diversity in the Dead Sea and the Jordan River. Israel J Plant Sci 49:160 Kis-Papo T, Grishkan I, Oren A, Wasser SP, Nevo E (2001b) Spatiotemporal diversity of filamentous fungi in the hypersaline Dead Sea. Mycol Res 105:749–756


231

Li CH, Wang HR, Yan TR (2012) Cloning, purification, and characterization of a heat- and alkaline- stable endoglucanase B from Aspergillus niger BCRC31494. Molecules 17:9774–9789 Li J, Liang X, Wei Y, Liu J, Lin F, Zhang S (2014) An ATP-dependent protease homolog ensures basic standards of survival and pathogenicity for Magnaporthe oryzae. Eur J Plant Pathol 141(4):703–716 Liang X, Liu Y, Xie L, Liu X, Wei Y, Zhou X, Zhang S (2015) A ribosomal protein AgRPS3aE from halophilic Aspergillus glaucus confers salt tolerance in heterologous organisms. Int J Mol Sci 16(2):3058–3070. https://doi.org/10.3390/ijms16023058 Liu G, Qin Y, Hu Y, Gao M, Peng S, Qu Y (2013) An endo-1,4-β-glucanase PdCel5C from cellulolytic fungus Penicillium decumbens with distinctive domain composition and hydrolysis product profile. Enzym Microb Technol 52:190–195 Liu XD, Liu JL, Wei Y, Tian YP, Fan FF, Pan HY, Zhang SH (2011) Isolation, identification and biologic characteristics of an extreme halotolerant Aspergillus sp. J Jilin Univ. (In Chinese; abstract in English) 49:548–552 Liu XD, Wei Y, Zhou XY, Pei X, Zhang SH (2015) Aspergillus glaucus aquaglyceroporin gene glpF confers high osmosis tolerance in heterologous organisms. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02127-15 Liu XD, Xie L, Wei Y, Zhou XY, Jia B, Liu J, Zhang SH (2014) Abiotic stress resistance, a novel moonlighting function of ribosomal protein RPL44 in the halophilic fungus Aspergillus glaucus. Appl Environ Microbiol 80(14):4294–4300. https://doi.org/10.1128/AEM.00292-14 Madigan M, Martinko J, Stahl D, Clark D (2012) Brock biology of microorganisms, 13th edn. Pearson Education, San Francisco Melero S, Madejo’n E, Ruiz JC, Herencia JF (2007) Chemical and biochemical properties of a clay soil under dryland agriculture system as affected by organic fertilization. Eur J Agron 26:327–334 Mernitz G, Koch A, Henrissat B, Schulz G (1996) Endoglucanase II (EGII) of Penicillium janthinellum: cDNA sequence, heterologous expression and promoter analysis. Curr Genet 29:490–495 Molitoris HP, Buchalo AS, Kurchenko I, Nevo E, Rawal BS, Wasser SP, Oren A (2000) Physiological diversity of the first filamentous fungi isolated from the hypersaline Dead Sea. In: Hyde KD, Ho WH, Pointing SB (eds) Aquatic mycology across the millennium, vol 5. Fungal Diversity, Hong Kong, pp 55–70 Moubasher AH, Abdel-Hafez SII, Bagy MMK, Abdel-Satar MA (1990) Halophilic and halotolerant fungi in cultivated desert and salt marsh soils from Egypt. Acta Mycol 26(2):65–81 Nazareth S, Gonsalves V, Nayak S (2012) A first record of obligate halophilic aspergilli from the Dead Sea. Indian J Microbiol 52:22–27 Nazareth S, Gonsalves V (2014) Aspergillus penicillioides – a true halophile existing in hypersaline and polyhaline econiches. Ann Microbiol 64:397–402 Nielsen P, Fritze D, Priest FG (1995) Phenetic diversity of alkaliphilic Bacillus strains: proposal for nine new species. Microbiology 141:1745–1761 Oo AN, Iwai CB, Saenjan P (2013) Soil properties and maize growth in saline and nonsaline soils using cassava-industrial waste compost and vermicompost with or without earthworms. Land Degrad Dev. https://doi.org/10.1002/ldr2208 Pereira I, Madeira A, Prista C, Loureiro-Dias MC, Leandro MJ (2014) Characterization of new polyol/H+ symporters in Debaryomyces hansenii. PLoS One 9(2):e88180. https://doi. org/10.1371/journal.pone.0088180 Pinar G, Ramos C, Rolleke S, Schabereiter-Gurtner C, Vybiral D, Lubitz W, Denner EB (2001) Detection of indigenous Halobacillus populations in damaged ancient wall paintings and building materials: molecular monitoring and cultivation. Appl Environ Microbiol 67:4891–4895 Prista C, Loureiro-Dias MC, Montiel V, García R, Ramos J (2005) Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res 5(8):693–701 Prista C, Soeiro A, Vesely P, Almagro A, Ramos J, Loureiro-Dias MC (2002) Genes from Debaryomyces hansenii increase salt tolerance in Saccharomyces cerevisiae W303. FEMS Yeast Res 2:151–157

232


Qadir M, Oster JD, Schubert S, Noble AD, Sahrawat KL (2007) Phytoremediation of sodic and saline-sodic soils. Adv Agron 96:197–247 Qin Y, Wei X, Song X, Qu Y (2008) Engineering endoglucanase II from Trichoderma reesei to improve the catalytic efficiency at a higher pH optimum. J Biotechnol 135:190–195 Rady MM (2011) Effects on growth, yield, and fruit quality in tomato (Lycopersicon esculentum Mill.) using a mixture of potassium humate and farmyard manure as an alternative to mineral-N fertilizer. J Hortic Sci Biotechnol 86(3):249–254 Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854 Robbins CW (1986) Sodic calcareous soil reclamation as affected by different amendments and crops. Agron J 78:916–920 Sahin U, Eroğlu S, Sahin F (2011) Microbial application with gypsum increases the saturated hydraulic conductivity of saline-sodic soils. Appl Soil Ecol 48(2):247–250 Santos SX, Carvalho CC, Bonfa MR, Silva R, Gomes E (2004) Screening for pectinolytic activity of wood-rotting basidiomycetes and characterization of the enzymes. Folia Microbiol 49:46–52 Sardinha M, Müller T, Schmeisky H, Joergensen RG (2003) Microbial performance in soils along a salinity gradient under acidic conditions. Appl Soil Ecol 23:237–244 Schuster E, Dunn-Coleman N, Frisvad JC, van Dijck PW (2002) On the safety of Aspergillus niger- A review. Appl Microbiol Biotechnol 59:426–435 Serrano R, Gaxiola R (1994) Microbial models and salt stress tolerance in plants. Crit Rev Plant Sci 13:121–138 Sparling GP, West AW, Reynolds J (1989) Influence of soil moisture regime on the respiration response of soils subjected to osmotic stress. Aust J Soil Res 27:161–168 Szabolcs I (1994) Soils and salinization. In: Pessarakli M (ed) Handbook of Plant and Crop Stress. Marcel Dekker, New York, pp 3–11 Tamura M, Kawasaki H, Sugiyama J (1999) Identity of the xerophilic species Aspergillus penicillioides: integrated analysis of the genotypic and phenotypic. J Gen Appl Microbiol 45:29–37 Taneja K, Gupta S, Kuhad RC (2002) Properties and application of a partially purified alkaline xylanase from an alkalophilic fungus Aspergillus nidulans KK-99. Bioresour Technol 85(1):39–42 Tejada M, Garcia C, Gonzalez JL, Hernandez MT (2006) Use of organic amendment as a strategy for saline soil remediation: influence on the physical, chemical and biological properties of soil. Soil Biol Biochem 38:1413–1421 Tomme P, Warren RAJ, Gilkes NR (1995) Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol 37:1–81 Van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24 Wang T, Liu X, Yu Q, Zhang X, Qu Y, Gao P, Wang T (2005) Directed evolution for engineering pH profile of endoglucanase III from Trichoderma reesei. Biomol Eng 22:89–94 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14 Wang L, Sun X, Li S, Zhang T, Zhang W, Zhai P (2014) Application of Organic Amendments to a Coastal Saline Soil in North China: Effects on Soil Physical and Chemical Properties and Tree Growth. PLoS One 9(2):e89185 Wichern J, Wichern F, Joergensen RG (2006) Impact of salinity on soil microbial communities and the decomposition of maize in acidic soils. Geoderma 137:100–108 Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685 Yan J, Song WN, Nevo E (2005) A MAPK gene from Dead Sea fungus confers stress tolerance to lithium salt and freezing-thawing: prospects for saline agriculture. Proc Natl Acad Sci U S A 102(52):18992–18997 Yuan BC, Li ZZ, Liu H, Gao M, Zhang YY (2007) Microbial biomass and activity in salt affected soils under arid conditions. Appl Soil Ecol 35(2):319–328


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Zalar P, Kocuvan MA, Plemenitas A, Gunde-Cimerman N (2005) Halophilic black yeasts colonize wood immersed in hypersaline water. Bot Mar 48:323–326 Zarafeta D, Kissas D, Sayer C, Gudbergsdottir SR, Ladoukakis E, Isupov MN, Chatziioannou A, Peng X, Littlechild JA, Skretas G, Kolisis FN (2016) Discovery and characterization of a thermostable and highly halotolerant GH5 cellulase from an icelandic hot spring isolate. PloS One 11:e0146454 Zhang X, Liu Y, Yan K, Wu H (2007) Decolorization of an anthraquinone-type dye by a bilirubin oxidase-producing nonligninolytic fungus Myrothecium sp IMER1. J Biosci Bioeng 104:104–114

Index

A Agriculture BFBF, 48 solid wastes, 164 Agroecosystems sustainability, 197, 198 AgRPL44, 224 Air pollutants, 56 Alkaliphilic fungi, 221 American Association of Textile Chemists and Colourists (AATC), 70 Arbuscular mycorrhiza (AM) AMF spores, 192 benefit, 196 external mycelium, 192 extraradical hyphae network, 192 fossil evidence and DNA sequence, 191 heavy metal, 195 host plant, 191 hydraulic conductivity, 194 hyphae network, 195 mineral nutrients, 194 osmotic adjustment, 194 PGPR, 195 plant growth and productivity, 193 root colonization, 195 vegetative mycelium, 192 Arbuscular mycorrhizal fungi (AMF), 189 Arbuscules, 192 Arsenic (As) Aspergillus niger, 29, 31 Aspergillus sydowii, 30, 31 mangrove ecosystem, 28 methylation, 28 removal, 28 Rhizopus sp., 30 yeasts, 31

Artificial mycorrhizae inoculum, 198 Aspergillus niger, 225 Aspergillus penicillioides, 221 Azo dyes, 79, 87, 89 Azoreductases, 82 B Batik painting, 90 reactive dyes, 90 wastewater, 91 wastewater treatment, 90 water use, 91 Beauveria bassiana (Bals.) Vuill., 8, 9 Bioaccumulation, 78 Biodegradation demolition solid waste, 165 petroleum hydrocarbons, 165 Biofertilizers, 48, 189, 205 Biofilm affecting factors horizontal gene transfer, 43 hydrodynamics, 42 physicochemical properties, 41, 42 quorum sensing, 43 topography of surface, 41 and biocontrol, 46 cells, 39 definition, 39 developmental steps, 41, 42 ecological advantage agriculture, 46 colonization, 46 defense, 45 genetic traits, 46

© Springer International Publishing AG 2017 R. Prasad (ed.), Mycoremediation and Environmental Sustainability, Fungal Biology, https://doi.org/10.1007/978-3-319-68957-9

235

Index

236 Biofilm (cont.) metabolic cooperation, 45 nutrient availability, 45 PGPR, 40 quorum sensing, 46 regulation architectural structure, 45 Bacillus subtilis, 44 EPS, 44 maturation, 44 osmolarity, 43 Biofilm biofertilizer (BFBF), 48 Biogas production, 94 Biomedical solid wastes, 158 Biopulping, 93 Bioreactor and operation mode, 88, 89 Bioremediation advantages, 183, 184 coal wastes, 163, 164 definition, 137, 171 fruit and food industry (see Fungal bioremediation) solid wastes, 166 Biosorption, 8, 9, 22, 27, 30, 78, 140, 141, 177, 178 Brown rot fungi, 175 C Cadmium, 136 Carbon dioxide emissions, 3 CCHA, 226 Cellulases, 163, 164, 167 Cellulolytic enzymes, 177 Cellulose, 225, 226 Chemical time bombs (CTBs), 134 Chlorinated aromatic compound degradation, 181 Chlorinated insecticides DDT, 121 endosulfan, 121, 122 LDS, 122 NADPH, 121 PCP, 123 Chromium biological removal, 25 Doehlert experimental design, 27 EPA, 25 FTIR analysis, 26 fungi, 26 pseudo-second-order model, 26 removal techniques, 25 Yarrowia lipolytica, 27

Citric acid cycle, 224 Cleaner environment, 184 Climate change, 3 Common effluent treatment plant (CETP), 23 Contamination environment, 137 of groundwater, 4 PAH, 142 soil degradation, 4 soil resources heavy metals, 5 soil biota, 5 Crude oil, 133, 141, 144 Crude oil biodegradation, 179, 180 D Date palm production AM colonization, 200 AMF species, 200 mycorrhizal fungi artificial inoculation, 202 desert ecosystems, 201 post-acclimatization, 202 root systems, 201 saline soil, 204–207 water stress, 203, 204 oasis ecosystem, 198, 199 pseudomantle, 200 RIZ, 199 root colonization, 201 seeds, 199 DDT, 121 Dead Sea, 221 Decolorization and degradation azoreductases, 82 enzymes, 95 fungal biofactories aeration and agitation, 86 carbon sources, 84 dye concentration, 86 dye effluents, 83 inoculum, 87 mineral salts, 85 nitrogen sources, 84 pH, 85 temperature, 85 fungi, 79 haem peroxidases, 78 home-made textile industry, 90, 91 laccases, 83 peroxidases, 79, 81, 82 white-rot fungi, 79–81

Index Degradation atrazine, 127 butachlor, 126 chlorinated aromatic, 181 chlorpyrifos, 125 DDT, 121 dye, 182 glyphosate, 127 herbicide, 182 insecticide, 183 malathion, 125 nitroaromatics, 181 PAHs, 180 PCP, 124 Dioxines, 172 Doehlert experimental design, 27 Domestic effluent pollution, 55 Dry and wet processing, 74, 75 Dye classification, 70, 72, 73 concentration, 86 decolorization, microbial enzymology, 77 degradation, 21, 182 organic colours, 70 removal, 22, 70 wastewater treatment, 73–77 E Effluents decolorization and detoxification, 20 mass spectrometric scan analysis, 20 Endoglucanases, 225 Endomycorrhiza, 191 Endophytes fungi-aided phytoremediation airborne spores, 139 AM, 139 biosorption, 140 Microsphaeropsis sp. LSE10, 141 REMI, 140 phytotoxicity, 138 rhizosphere, 138 Endophytic fungi biosorption, 140 heavy metals, 139 PAH, 143 Energy-dispersive X-ray spectroscopic (EDX), 28 Environment, agriculture effect carbon dioxide emissions, 3 climate change, 3

237 eutrophication, 2 pollution groundwater, 4 soil degradation, 4 soil resources, 5 water pollution, 1 Environmental pollution air pollutants, 56 definition, 54 organic and inorganic, 53 removal process, 53 risk factors, 54 soil pollutants, 58 types, 55 water pollutants, 57 Environmentally sound technologies (ESTs), 137 EnvZ/OmpR signaling system, 43 Eutrophication, 2 E-Wastes, 163 Ex situ remediation, 173 Exoglucanases, 225 Extracellular polymeric substances (EPS), 39 Extremophilic fungi, 223 F Fourier-transform infrared (FTIR), 112 Fungal biomasses, 7 Fungal bioremediation Beauveria bassiana (Bals.) Vuill., 8, 9 Paecilomyces lilacinus (Thom) Samson, 9, 10 pollution, soil degradation, 10 recalcitrant toxic compounds, 17, 18 Trichoderma sp., 7, 8 Fungal classification ascomycetes, 55 basidiomycetes, 57 deuteromycetes, 58 zygomycetes, 57 Fungal communities, 112–114 Fungal dye decolorization, 78 Fungi environmental indicator (see Fungal bioremediation) pollutants remediation, 60 white-rot and brown-rot, 61 G Genetically engineered microorganisms (GEM), 7, 145

Index

238 H Haloalkaliphilic fungi, 220–222 Halophilic fungi, 220, 221 Heavy metal pollution, 92 Heavy metals arsenic, 135, 136 (see also Arsenic (As)) cadmium, 136 (see also Chromium) contamination, 134 lead (Pb), 135 mercury, 135 Herbicide degradation, 182 Herbicides atrazine degradation, 127 glyphosate degradation, 127 phenylamide compounds, 125 High-osmolarity glycerol (HOG1), 223 Hydrocarbon contamination, 165 Hydrocarbon degradation crude oil biodegradation, 179, 180 mushrooms bioconversion, 179 biodegradation, 178 biosorption, 178–179 Hydrocarbon pollution, 133, 141, 142 Hydrothermal As biosequestration, 31 Hyperaccumulators, 137, 138 I Incineration, 120 Industrial pollutants, 154 Industrial solid wastes bioremediation, 161, 163 E-waste, 163 leather waste treatment, 162 mycoremediation, 161–163 Inoculum, 61, 87 Insecticides chlorinated compounds, 121–123 degradation, 183 organophosphorus, 123, 125 In situ remediation, 172 L Laccases, 83, 160, 167 Lead (Pb), 135 Lignin degrading system (LDS), 122 Lignin peroxidase (LiP), 23 Lignin-degrading enzymes (LDEs), 19 Lignin-modifying enzymes (LMEs), 19 Ligninolytic enzymes oxidases, 176 peroxidases, 176

Ligninolytic fungal degradation brown rot fungi, 175 soft rot fungi, 175 WRF, 174 Lignocellulases, 167 Long-term drought (LTD), 204 M Magnaporthe oryzae, 224 Marasmiellus troyanus, 10 Marine-derived fungi Aspergillus niger, 22 Bhavnagar coast, 29 (see also Mycoremediation) Mercury, 135 Microbes endophytic bacteria, 144 PAH, 143 petroleum-polluted soils, 144 rhizospheric interaction, 143 Microbial bioremediation, 154 Microbial enzymology, 77–78 Microbial treatment, 6 Microorganisms, 59, 61, 62, 73, 189 Mineralization, 63 Mining solid wastes, 159 Morphological investigations SEM, 107, 108 SPM, 108, 109 MoRPL44, 224 Municipal solid waste, 160 Mycobiota, 112 Mycofiltration, 62 Mycoremediation advantages, 154 arsenic, 27–30, 32 biogas production, 94 biopulping, 93 chromium, 25–27 definition, 171 disadvantages, 166 dye degradation, 21 effluents, 19, 20 ex situ remediation, 173 fungal biodegradation, 155 heavy metal pollution, 92 in situ remediation, 172 inoculum, 61 LDEs, 19 match industry, 161 mycofiltration, 62 mycorrhizal fungi, 59, 61 nutrient capture, 157

Index PAHs, 63, 64, 93 paper and pulp industrial waste, 162, 163 polyethylene, 59, 155 saline-alkali soil, 219, 228 synthetic dyes decolorization, 19 health risks, 18 textile dyes, 19 toxicity testing, 21 Mycorrhizal fungal degradation, 175 Mycorrhizal symbiosis, 195 Mycorrhizas AM (see Arbuscular mycorrhiza (AM)) AMF, 190 endomycorrhiza, 191 mycelium, 190 plant/fungus combination, 191 symbiotic structure, 191 Mycorrhizoremediation, 178, 183 N Nakhla hamra (NHH) and Tijib, 206 Nicotinamide adenine dinucleotide phosphate (NADPH), 121 Nitroaromatics, 181 O Organophosphorus insecticides, 123, 125 Osmolality, 44 Outdoor corrosion environmental conditions, 105 metals, 107 mycobiota, 105 polyaniline, 106 total metal mass loss, 106, 107 P Paecilomyces lilacinus (Thom) Samson, 9, 10 PAH degradation, 180, 181 Peroxidases LiP, 81 manganese, 81 VP, 82 Pesticides applications, 119 biodegradation, 128 bioremediation, 120 chemical treatment and volatilization, 120 contamination, 119 incineration, 120

239 Petroleum biodegradation, 143, 144 Phenol oxidases, 176 Phytoremediation, 7, 75, 137, 142, 218 Phytotoxicity, 138 Plant growth-promoting rhizobacteria (PGPR), 40, 195 Pollutants, 74, 75, 174 See also Degradation Pollution defined (see Environmental pollution) solid wastes (see Solid wastes management) Polyamines, 205 Polyaromatic hydrocarbons (PAHs) aqueous phase, 63 biodegradation, 63 mineralization, 63 PVA, 64 Polychlorinated biphenyls (PCBs), 171 Polycyclic aromatic hydrocarbons (PAHs), 93, 142, 143, 171 Polyvinyl alcohol (PVA), 64 R Reactive Blue 4 (RB4), 20 Remazol brilliant blue R (RBBR), 21 Response surface methodology (RSM), 20 Restriction enzyme-mediated integration (REMI), 140 Ribosomal protein L44 (RPL44), 224 Risk factors, 114 Root initiation zone (RIZ), 199 Rubber solid waste, 159 S Saline-alkali soil A. glaucus, 224 cellulose, 225, 226 citric acid cycle, 224 D. hansenii, 223 EhHOG, 223 extremophilic fungi, 223 microbial application, 219, 222 MoRPL44, 224 mycoremediation, 219 S. cerevisiae, 223 soil-inhabitant fungi, 219 T. lanuginosus, 224 Salinity-tolerant, 206 Scanning electron microscopy (SEM), 107, 108

Index

240 Scanning probe microscopy (SPM), 108–109 Soft rot fungi, 175 Soil biota, 5 Soil degradation, 4 Soil fungal biosorption, 175 Soil-plant pathogens, 195 Soil pollutants, 58 Soil salinity AM fungi, 205, 206 date palm, 206 microorganisms, 205 osmotic stress, 205 PGPR, 205 salt stress, 204 Soil salinization, 217 Solid waste management agriculture, 164 biodegradation, 165 biomedical, 158 bioremediation, 154 fungal biodegradation mining, 158 rubber, 159 fungi and pollutants, 155–157 garbage and rubbish, 160 industrial wastes (see Industrial solid wastes) recyclable materials, 153 xenobiotics, 159, 160 Synthetic dyes decolorization, 19, 23 health risks, 18 T Textile dyes marine-derived fungi, 21 Pestalotiopsis sp. NG007, 23 RB5, 22 Textile wastes chemical and physical approaches, 70 heavy metals, 71

synthetic dyes, 71 wet processing, 71 Thermomyces lanuginosus, 224 Total metal mass loss, 106, 107 Total petroleum hydrocarbons (TPH), 141 Toxicity testing, 21 Tricarboxylic acid cycle (TCA), 44 Trichoderma sp., 7, 8 V Versatile peroxidase (VP), 82 W Wastewater treatment azo dyes, 87–89 batik, 90 biological treatment, 70 bioreactor and operation mode, 88, 89 bioremediation, 78 dye, 76 forms, 71 organic pollutants, 73 technology, 73–77 Water pollutants, 57 Water stress, 203, 204 Wavelength dispersive X-ray fluorescence (WDXRF), 109, 110 White rot fungi (WRF), 174 White-rot fungi, 79–81, 122, 127, 144 X Xenobiotics, 159, 160 X-ray diffraction (XRD), 110, 112 Y Yeasts, 31