Aquatic ecosystems house a large biosphere of marine and freshwater organisms, highly diverse in their tolerance of fluctuations in PO2 and temperature, two ...
Introduction to Oxidative Stress in Aquatic Ecosystems Doris Abele1, Jos´e Pablo V´azquez-Medina2,3, and Tania Zenteno-Sav´ın2 1
Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany 2 Centro de Investigaciones Biol´ ogicas del Noroeste, S.C. (CIBNOR), La Paz, Baja California Sur, Mexico 3 School of Natural Sciences, University of California Merced, Merced, CA, USA
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quatic ecosystems house a large biosphere of marine and freshwater organisms, highly diverse in their tolerance of fluctuations in PO2 and temperature, two major modulators of metabolism. Often, both factors act in concert, and some of the most hypoxia-tolerant fish and molluskan species are indeed from cold-water environments. Other marine invertebrate and fish specialists thrive in the mixed waters at hydrothermal vent sites, underwater volcanic outflows where warm and hydrogen-sulfide-enriched, deoxygenated vent waters mix with colder and oxygenated oceanic waters, and temperatures and oxygen concentrations are extremely variable. Many vent species can even deal with toxic hydrogen sulfide that threatens to inhibit their mitochondrial electron transporters. More than 700 Myr of aquatic evolution have fostered a huge variety of ectothermic life-forms that can deal with the most extreme and fluctuating environmental conditions. The discovery of many fascinating underwater biota has raised an interest in the respiratory capacities of aquatic organisms and in how they deal with, from our air breathing perspective,
way too little or way too much and fluctuant oxygen concentrations. As long ago as 1982, James Dykens and Malcolm Shick (Nature 297, 579–580) discovered that high oxygen concentrations, produced by endosymbiontic microalgae, represent a toxic assault which induces antioxidant activities in the cnidarian host cells. In 1984, Janice Blum and Irvin Fridovich investigated the activities of superoxide dismutases (Cu,Zn-, Mn- and Fe-SOD) in tissues of the hydrothermal vent tube worm Riftia pachyptila and the bivalve Calyptogena magnifica (Archives of Biochemistry and Biophysics. 228(2), 617–620). Superoxide dismutases detoxify superoxide anions (O2•− ) by adding another electron and converting O2•− to the less reactive, and therefore less toxic reactive oxygen species (ROS) hydrogen peroxide (H2 O2 ). Both vent species rely largely on energy production by endosymbiontic sulfide-oxidizing bacteria but are still endowed with considerable SOD activity, just as are their sulfide-metabolizing endosymbionts, which feature a special procaryotic Fe-SOD isoform. The central message of Blum and Fridovich’s paper is that cellular antioxidants are ubiquitious and therefore not
Oxidative Stress in Aquatic Ecosystems, First Edition. Edited by Doris Abele, Jos´e Pablo V´azquez-Medina, and Tania Zenteno-Sav´ın. © 2012 by Blackwell Publishing Ltd.
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only present in organisms relying primarily on aerobic energy production. Indeed, SOD enzyme forms developed early in evolution when oxygen started to accumulate: a toxicant in a primarily anoxic world. Together these two seminal papers started a whole new field of research, relating oxidative stress and antioxidant parameters in marine and freshwater organisms to the conditions prevailing in different aquatic habitats and microhabitats, such as the host cell environments of endosymbionts. In 2010, a Google Scholar search for ‘‘oxidative stress’’ and ‘‘marine’’ yielded 50,000 publication hits (‘‘oxidative stress’’ and ‘‘aquatic’’ 25,000 hits). This is indicative of the enormous interest and intensive research in this field, which prompted us to initiate this book project. There is also a growing interest in aquatic organisms as models for clinical and aging studies, which is expected to boost comparative research. A great number of diseases in animals and humans involve oxidative stress phenomena, and many aquatic organisms tolerate extreme states, which are pathological in humans (e.g. ischemia/reperfusion). Finally, global change and pollution massively threaten and change the Earth’s ecosystems and, as over 70% of our planet’s surface area is covered by water, aquatic species have become important sentinels and indicators of change. Since most forms of environmental and pollution stress eventually cause an imbalance between oxygen radical-producing and -scavenging processes, oxidative stress parameters are broadly employed in marine and terrestrial impact studies. In preparing the concept for this book, it seemed fundamental to determine how climate effects in tropical versus polar habitats and natural scenarios in extreme environments shape the basic levels of oxidative stress parameters in aquatic ectotherms (Part I, Climate Regions and Special Habitats). Individual chapters focus on life strategies in special habitats in terms of oxygen availability, such as the sulfidic sedimentary and hydrothermal vent environments, the oxygen minimum layer of the ocean, or the cnidarian host cell of zooxanthellate endosymbionts. Fluctuations of abiotic parameters during tidal cycles confer stress hardening on intertidal species and populations; Chapter 3 delves into the effect of these fluctuations on antioxidant concentrations and enzyme activities in animals and plants from the higher littoral zone. Furthermore, long-term seasonal and climate related fluctuations modulate oxidative stress parameters in aquatic ecosystems, and Chapters 4 and 5 have a
special focus on the expected consequences for primary producers at the base of aquatic food chains. Part II of this book addresses the specific features of oxidative stress parameters with respect to respiration in water- and air-breathing aquatic animals. The respiratory medium water contains 30 times less oxygen per liter than air, and water-breathing organisms are generally adapted to perform at these lower oxygen concentrations. What this means for animal respiratory performance, including active swimmers such as sharks, and how cellular oxygen sensing mechanisms have evolved under aquatic conditions is explored in Part II (Aquatic Respiration and Oxygen Sensing). Furthermore, aquatic animals are increasingly discussed and tested as model organisms for aging and disease. The longest lived of all noncolonial organisms so far known is the hard clam Arctica islandica. Several authors have summarized what is new in the field of aging in marine ectotherms, a recent hot topic in aging research. Aquatic models for human diseases, including fish and invertebrate immune function and cellular signaling pathways, where ROS play different roles in development of cancer, are reviewed in Part III (Marine Animal Models for Aging, Development, and Disease). Many current papers on oxidative stress in aquatic organisms lack information about gender, reproductive or molting state, and age distribution in the experimental animals. While we know that in many cases it is still difficult to supply these data, we strongly encourage choosing model species that help us to understand the relevance of life-history-related physiological change on oxidative stress parameters in aquatic ectotherms. Part IV (Marine Animal Stress Response and Biomonitoring) delves into the general stress response in aquatic fauna and the applicability of oxidative stress markers as indicators of environmental stress and pollution in biomonitoring studies. One important takehome message in many chapters, especially in this Part, is that it does not suffice for stress assessment to compare only the levels of antioxidants, or measure the rates of radical production alone. A stress response should be characterized by measurements of different oxidative damage markers and antioxidants, ideally complemented by a confirmation of higher radical production under stress. On one hand, the mere increase in antioxidant activity of animal tissues is not a confirmation of a physiological stress condition and, much to the contrary, can indicate the activation of antioxidant defense systems in control or anticipation of increased ROS
Introduction to Oxidative Stress In Aquatic Ecosystems
production. On the other hand, different toxicants can interfere with each other, and a decline in antioxidant defense systems or the absence of a stress signaling (e.g. for immune stimulation) are, in many cases, the result of toxicant cross-effects, often worsening the situation. The last and most comprehensive part of the book (Methods of Oxidative Stress Detection) presents an evaluation of classic and modern methods for the assessment of oxidative stress in aquatic animals and plant material. We asked experts in different analytical fields to describe the relevant methods and their analytical background. Many of our colleagues not only provide detailed measurement protocols but also suggest where to start troubleshooting. Importantly, the authors of the method chapters make suggestions concerning the applicability of different methods. Indeed, the classic methods to assess lipid or protein oxidation are widely used and applicable in environmental studies, in spite of known constraints with respect to accuracy and specificity. More accurate techniques are now available, including those for direct analysis of various radical species or oxidative damage parameters, such as DNA adducts. Often these require complex and costly analytical equipment, such as an EPR (electron paramagnetic resonance spectrometry) or chromatography with mass spectrometric detection. The authors share their expertise and at the same time evaluate the usefulness of alternative methods for different problems in aquatic oxidative stress research. New tools are also coming into reach for genetic and genomic stress research, which promise a rapid advance in the understanding of molecular pathways in the response of aquatic organisms to different stressors and stress scenarios. At present, measurements of transcript levels can be compared to the antioxidant enzyme activities in most aquatic organisms, as a growing amount of partial or full sequences become available in gene banks. Antibodies for measuring antioxidant protein levels are less available, perhaps because for many questions the catalytic activity seems more functionally important than the amount of enzyme subunits present in a sample. However, antibodies that tag regulatory proteins and transcription factors in aquatic species are urgently needed for the mechanistic assessment of stress response capacities in different species. Further work is needed to verify the applicability of mammalian cell stress research kits designed to detect activity of cellular processes, such as apoptosis and autophagy, in aquatic invertebrates, often genetically distant from the originally targeted model system.
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In future research it will also be important to establish closely related model species or single species with wide geographical distribution (migrating species) for functional studies of animal adaptation and effects of climate change in marine and freshwater systems. Cultures of different cell types, such as hemocytes or liver cells of aquatic species, need to be established as test systems and for intercalibration of methods among laboratories. These mechanistic model systems and the enormous advances in organic environmental chemistry, especially with respect to identification and elucidation of chemical compound structures, can be instrumental in the assessment of pollution and anthropogenic disturbance in aquatic habitats and, within a short time, will allow chemists to identify sources of pollution in the globally interconnected oceanic environments. An important motivation for us as editors of this book was the great enthusiasm of our fellow authors. The readiness with which many young authors engaged with this project was inspiring. We are especially proud of the fact that several chapters were co-authored or have been reviewed by graduate students from different laboratories, who have greatly contributed to improve the understandability of the text and the completeness of the experimental protocols. We hope that this book can further stimulate research in the exciting field of oxygen toxicity, stress and molecular signaling in marine and freshwater organisms.
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Introduction to Oxidative Stress In Aquatic Ecosystems
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