Industrial and biotechnological applications of

Biotechnology Advances 24 (2006) 500 – 513 www.elsevier.com/locate/biotechadv

Research review paper

Industrial and biotechnological applications of laccases: A review Susana Rodríguez Couto ⁎, José Luis Toca Herrera ⁎ Department of Chemical Engineering, Rovira i Virgili University, Av. Països Catalans 26, 43007 Tarragona, Spain Received 20 January 2006; received in revised form 29 March 2006; accepted 1 April 2006 Available online 18 April 2006

Abstract Laccases have received much attention from researchers in last decades due to their ability to oxidise both phenolic and nonphenolic lignin related compounds as well as highly recalcitrant environmental pollutants, which makes them very useful for their application to several biotechnological processes. Such applications include the detoxification of industrial effluents, mostly from the paper and pulp, textile and petrochemical industries, use as a tool for medical diagnostics and as a bioremediation agent to clean up herbicides, pesticides and certain explosives in soil. Laccases are also used as cleaning agents for certain water purification systems, as catalysts for the manufacture of anti-cancer drugs and even as ingredients in cosmetics. In addition, their capacity to remove xenobiotic substances and produce polymeric products makes them a useful tool for bioremediation purposes. This paper reviews the applications of laccases within different industrial fields as well as their potential extension to the nanobiotechnology area. © 2006 Elsevier Inc. All rights reserved. Keywords: Food industry; Industrial applications; Laccase; Nanobiotechnology; Pulp and paper industry; Textile industry

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . Potential industrial and biotechnological 2.1. Food industry . . . . . . . . . . 2.2. Pulp and paper industry . . . . . 2.3. Textile industry . . . . . . . . . 2.4. Nanobiotechnology . . . . . . . 2.5. Other laccase applications . . . . 2.5.1. Soil bioremediation . . . 2.5.2. Synthetic chemistry . . . 2.5.3. Cosmetics . . . . . . . . 3. Future outlook . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . .

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⁎ Corresponding authors. Tel.: +34 977 55 9617; fax: +34 977 55 9667. E-mail addresses: [email protected] (S. Rodríguez Couto), [email protected] (J.L. Toca Herrera). 0734-9750/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.biotechadv.2006.04.003

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S. Rodríguez Couto, J.L. Toca Herrera / Biotechnology Advances 24 (2006) 500–513

1. Introduction Although oxidation reactions are essential in several industries, most of the conventional oxidation technologies have the following drawbacks: non-specific or undesirable side-reactions and use of environmentally hazardous chemicals. This has impelled the search for new oxidation technologies based on biological systems such as enzymatic oxidation. These systems show the following advantages over chemical oxidation: enzymes are specific and biodegradable catalysts and enzyme reactions are carried out in mild conditions. Enzymatic oxidation techniques have potential within a great variety of industrial fields including the pulp and paper, textile and food industries. Enzymes recycling on molecular oxygen as an electron acceptor are the most interesting ones. Thus, laccase (benzenediol: oxygen oxidoreductase; EC 1.10.3.2) is a particularly promising enzyme for the above-mentioned purposes. The laccase molecule is a dimeric or tetrameric glycoprotein, which usually contains four copper atoms per monomer distributed in three redox sites (Gianfreda et al., 1999). This enzyme catalyses the oxidation of ortho and paradiphenols, aminophenols, polyphenols, polyamines, lignins and aryl diamines as well as some inorganic ions coupled to the reduction of molecular dioxygen to water (Yaropolov et al., 1994; Solomon et al., 1996). The reported redox potentials of laccases are lower than those of non-phenolic compounds, so these enzymes cannot oxidise such substances. However, it was shown that in the presence of small molecules capable to act as electron transfer mediators laccases were also able to oxidise non-phenolic structures (Bourbonnais and Paice, 1990; Call and Mücke, 1997), expanding, thus, the range of compounds that can be oxidised by these enzymes. Laccase-mediated systems (LMS) have been applied to numerous processes such as pulp delignification (Bourbonnais et al., 1997; Bourbonnais et al., 1998; Crestini and Argyropoulos, 1998; Li et al., 1999), oxidation of organic pollutants (Collins et al., 1996) and the development of biosensors (Kulys et al., 1997; Trudeau et al., 1997; Kuznetsov et al., 2001) or biofuel cells (Palmore and Kim, 1999). Several organic and inorganic compounds have been reported as effective mediators for the above-mentioned purposes. These include thiol and phenol aromatic derivatives, N-hydroxy compounds and ferrocyanide, respectively. Claus et al. (2002) found that the LMS enhanced dye decolourization and some dyes resistant to laccase degradation were decolourised. Lu and Xia (2004) have recently reviewed the applications of the LMS, which comprise pulp bleaching, textile biofinishing and environmental protection processes. However, de-

501

spite that LMS has been studied extensively there are still unsolved problems concerned with mediator recycling, cost and toxicity. Laccases have been reviewed several times in recent years, generally with emphasis on narrow aspects. The reviews by Messerschmidt (1993, 1997) and by Solomon et al. (1996) provide excellent summaries of the enzymology and electron transfer mechanism of the laccases and a book edited by Messerschmidt (1997) contains a series of articles dealing with different aspects of laccase kinetics and mechanism of action and the possible roles of this enzyme. The aim of this review is to highlight the potential industrial and biotechnological applications of laccase enzyme. 2. Potential industrial and biotechnological applications of laccase enzyme Table 1 shows different applications of laccases in the last two decades. Laccases find applications within the following fields: 2.1. Food industry Laccases can be applied to certain processes that enhance or modify the colour appearance of food or beverage. In this way, an interesting application of laccases involves the elimination of undesirable phenolics, responsible for the browning, haze formation and turbidity development in clear fruit juice, beer and wine. Laccases are currently of interest in baking due to its ability to cross-link biopolymers. Thus, Selinheimo et al. (2006) showed that a laccase from the white-rot fungus Trametes hirsuta increased the maximum resistance of dough and decreased the dough extensibility in both flour and gluten dough. Recently, Minussi et al. (2002) have described the potential applications of laccase in different aspects of the food industry such as bioremediation, beverage processing, ascorbic acid determination, sugar beet pectin gelation, baking and as a biosensor. However, they suggested that more studies of laccase production and immobilisation techniques at lower costs are needed to improve the industrial application of this enzyme. 2.2. Pulp and paper industry The industrial preparation of paper requires separation and degradation of lignin in wood pulp. Environmental concerns urge to replace conventional and polluting chlorine-based delignification/bleaching procedures (Kuhad et al., 1997). Oxygen delignification

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Table 1 Different laccase applications Application

Laccase source

Decolourization of Aspergillus (genetically modified) dyes Aspergillus (genetically modified) Aspergillus niger Cerrena unicolor Coriolopsis gallica Coriolopsis rigida Funalia trogii Irpex lacteus Myceliophthora thermophila, Polyporus pinsitus, Trametes versicolor Pleurotus eryngii, Pycnoporus cinnabarinus, T. versicolor Pleurotus ostreatus P. ostreatus P. cinnabarinus P. cinnabarinus Sclerotium rolfsii, Trametes hirsuta Streptomyces cyaneus T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta T. hirsuta, T. versicolor Trametes modesta T. modesta Trametes trogii T. versicolor T. versicolor T. versicolor T. versicolor T. versicolor T. versicolor Trametes villosa T. villosa Degradation of xenobiotics

strain I-4 of the family Chaetomiaceae Cladosporium sphaerospermum Coprinus cinereus, Myceliophthora thermophila, P. pinsitus, Rhizoctonia solani C. gallica C. gallica Coriolus hirsutus Coriolus versicolor C. versicolor Myceliophtora thermophyla, Trametes pubescens Panus tigrinus P. osteratus P. ostreatus P. ostreatus, T. versicolor P. cinnabarinus Pyricularia oryzae

Reference Soares et al. (2001a) Soares et al. (2001b) Soares et al. (2002) Michniewicz et al. (2003) Reyes et al. (1999) Gómez et al. (2005) Ünyayar et al. (2005) Kasinath et al. (2003) Claus et al. (2002) Camarero et al. (2004) Hou et al. (2004) Palmieri et al. (2005) Mccarthy et al. (1999) Schliephake et al. (2000) Campos et al. (2001) Arias et al. (2003) Abadulla et al. (2000) Domínguez et al. (2005) Moldes et al. (2003) Rodríguez Couto et al. (2004a) Rodríguez Couto et al. (2004c) Rodríguez Couto et al. (2005) Rodríguez Couto et al. (2006) Rodríguez Couto and Sanromán (2006) Rodríguez Couto and Sanromán (2005) Rodríguez Couto et al. (2004b) Nyanhongo et al. (2002) Rehorek et al. (2004) Levin et al. (2005) Maceiras et al. (2001) Lorenzo et al. (2002) Rodríguez Couto et al. (2002) Peralta-Zamora et al. (2003) Blánquez et al. (2004) Tavares et al. (2004) Zille et al. (2003) Knutson and Ragauskas (2004) Saito et al. (2004) Potin et al. (2004) Kulys et al. (2003) Pickard et al. (1999) Vandertol-Vanier et al. (2002) Cho et al. (2002) Itoh et al. (2000) Okazaki et al. (2002) Nicotra et al. (2004) Zavarzina et al. (2004) Eggen (1999) Hublik and Schinner (2000) Keum and Li (2004) Mougin et al. (2002) Lante et al. (2000)


503

Table 1 (continued ) Application

Laccase source

Reference

P. oryzae Rhus vernicifera T. hirsuta

Carunchio et al. (2001) Moeder et al. (2004) Niku-Paavola and Viikari (2000) Böhmer et al. (1988) Tanaka et al. (2001) Tanaka et al. (2003) Collins et al. (1996) Johannes et al. (1998) Majcherczyk et al. (1998) Johannes and Majcherczyk (2000) Majcherczyk and Johannes (2000) Castro et al. (2003) Dodor et al. (2004) Fabbrini et al. (2001) Fukuda et al. (2001) Kang et al. (2002) Cantarella et al. (2003) Jung et al. (2003) Zhang et al. (2002) Timur et al. (2004) Vianello et al. (2004) Kulys and Vidziunaite (2003) Jarosz-Wilkołazka et al. (2004) Jarosz-Wilkołazka et al. (2005) Marko-Varga et al. (1995) Lisdat et al. (1997) Bauer et al. (1999) Kuznetsov et al. (2001) Freire et al. (2002) Gupta et al. (2003) Gomes and Rebelo (2003) Leite et al. (2003) Palmore and Kim (1999) Gardiol et al. (1996) Leech and Daigle (1998) Freire et al. (2001) Gomes and Rebelo (2003) Haghighi et al. (2003) Gomes et al. (2004) Roy et al. (2005) Ferry and Leech (2005) Calvo et al. (1998) Murugesan (2003) D'Annibale et al. (1999) D'Annibale et al. (2000) Casa et al. (2003) D'Annibale et al. (2004) Aggelis et al. (2003) Tsioulpas et al. (2002) Jaouani et al. (2005) Durante et al. (2004) Xiao et al. (2003) Jolivalt et al. (2000)

T. hirsuta D10 Trametes sp. Trametes sp. T. versicolor T. versicolor T. versicolor T. versicolor T. versicolor

Biosensors

T. versicolor T. versicolor T. villosa T. villosa T. villosa T. villosa Trichophyton sp. LKY-7 unspecified Agaricus bisporus, A. niger, T. versicolor Agaricus bisporus, R. vernicifera Rigidoporus lignosus, T. versicolor Aspergillus oryzae, Myceliophtora Thermophila, P. pinsitus C. unicolor C. unicolor

Effluent treatment

C. hirsutus C. hirsutus C. hirsutus C. hirsutus C. hirsutus C. hirsutus, R. vernicifera C. versicolor P. ostreatus P. oryzae R. vernicifera T. versicolor T. versicolor T. versicolor T. versicolo T.. versicolor T. versicolor T. versicolor C. gallica Gliocladium virens Lentinula edodes L. edodes L. edodes P. tigrinus P. ostreatus Pleurotus spp. Pycnoporus coccineus R. vernicifera Trametes sp. strain AH28-2 T. versicolor

(continued on next page)

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Table 1 (continued ) Application

Biopulping

Organic synthesis

Food industry

Biobleaching

Denim bleaching

Laccase source

Reference

T. versicolor Edwards et al. (2002) T. versicolor Lucas et al. (2003) Fomes fomentarius, Ganoderma collosum, Lentinus edades, Merulius tremellosus, Phlebia Bourbonnais et al. (1997) radiata, P. ostreatus T. versicolor C. versicolor Call and Mücke (1997) (Lignozym®-process) Peniophora sp., Pycnoporus sanguineus, T. hirsuta, T. versicolor Kandioller and Christov (2001) T. versicolor Archibald et al. (1997) T. versicolor Crestini and Argyropoulos (1998) unspecified Jacob et al. (1999) unspecified Sealey et al. (1999) unspecified Chakar and Ragauskas (2001) unspecified Poppius-Levlin et al. (2001) unspecified Tamminen et al. (2003) C. hirsuta Baker et al. (1996) C. hirsutus Karamyshev et al. (2003) P. cinnabarinus Mikolasch et al. (2002) P. coccineus Uyama and Kobayashi (2002) P. oryzae Setti et al. (1999) T. versicolor Fritz-Langhals and Kunath (1998) T. versicolor Akta et al. (2001) T. versicolor Schäfer et al. (2001) T. versicolor Akta and Tanyolaç (2003) T. villosa Uchida et al. (2001) Chinese rhus lacquer Huang et al. (1995) Myceliophtora thermophili, P. pinsitius Micard and Thibault (1999) P. cinnabarinus Georis et al. (2003) T. hirsuta Kuuva et al. (2003) T. versicolor Crecchio et al. (1995) unspecified Mathiasen (1996) unspecified Petersen and Mathiasen (1997) unspecified Norsker et al. (2000) C. versicolor Balakshin et al. (2001) P. eryngii, P. cinnabarinus, T. versicolor Camarero et al. (2004) P. cinnabarinus Georis et al. (2003) T. versicolor Paice et al. (1995) T. versicolor Archibald et al. (1997) unspecified Balakshin et al. (2001) unspecified Han et al. (2002) T. versicolor Pazarlıoglu et al. (2005) unspecified Vinod (2001)

processes have been industrially introduced (Carter et al., 1997), but pre-treatments of wood pulp with ligninolytic enzymes might provide milder and cleaner strategies of delignification that are also respectful of the integrity of cellulose (Kuhad et al., 1997). Although extensive studies have been performed to develop alternative bio-bleaching systems, few enzymatic treatments exhibit the delignification/brightening capabilities of modern chemical bleaching technologies. One of the few exceptions to this generalisation is the

development of LMS delignification technologies for kraft pulps. In addition, laccase is more readily available and easier to manipulate than both lignin peroxidase (LiP) and manganese-dependent peroxidase (MnP) and LMS has already found practical applications such as the Lignozym®-process (Call and Mücke, 1997). Several authors applied the LMS to pulp biobleaching (see Table 1). However, all these biobleaching studies were focused on wood pulps and little is known about the efficiency of the LMS on non-wood pulps


including those used for manufacturing specialty papers. In this sense, Camarero et al. (2004) explored the potential of LMS to remove lignin-derived products responsible for colour from a high-quality flax pulp. They showed the feasibility of LMS to substitute chlorine-containing reagents in manufacturing of these high-price paper pulps. The capability of laccases to form reactive radicals in lignin can also be used in targeted modification of wood fibers. For example, laccases can be used in the enzymatic adhesion of fibers in the manufacturing of lignocellulosebased composite materials such as fiberboards. Laccases have been proposed to activate the fiberbound lignin during manufacturing of the composites, thus, resulting in boards with good mechanical properties without toxic synthetic adhesives (Felby et al., 1997; Hüttermann et al., 2001). Another possibility is to functionalise lignocellulosic fibers by laccases in order to improve the chemical or physical properties of the fiber products. Preliminary results have shown that laccases are able to graft various phenolics acid derivatives onto kraft pulp fibers (Lund and Ragauskas, 2001; Chandra and Ragauskas, 2002). This ability could be used in the future to attach chemically versatile compounds to the fiber surfaces, possibly resulting in fiber materials with completely novel properties such as hydrophobicity or charge. 2.3. Textile industry The textile industry accounts for two-thirds of the total dyestuff market (Riu et al., 1998) and consumes large volumes of water and chemicals for wet processing of textiles. The chemical reagents used are very diverse in chemical composition, ranging from inorganic compounds to polymers and organic products (Mishra and Tripathy, 1993; Banat et al., 1996; Juang et al., 1996). There are more than 100,000 commercially available dyes with over 7 × 105 t of dyestuff produced annually (Meyer, 1981; Zollinger, 2002). Due to their chemical structure dyes are resistant to fading on exposure to light, water and different chemicals (Poots and McKay, 1976; McKay, 1979) and most of them are difficult to decolourise due to their synthetic origin. Government legislation is becoming more and more stringent, especially in the more developed countries, regarding the removal of dyes from industrial effluents (O'Neill et al., 1999). Concern arises, as several dyes are made from known carcinogens such as benzidine and other aromatic compounds (Baughman and Perenich, 1988). Most currently existing processes to treat dye wastewater are ineffective and not economical (Cooper, 1995; Stephen, 1995). Therefore, the development of

505

processes based on laccases seems an attractive solution due to their potential in degrading dyes of diverse chemical structure (Abadulla et al., 2000; Blánquez et al., 2004; Hou et al., 2004), including synthetic dyes currently employed in the industry (Rodríguez Couto et al., 2004a, 2005). The use of laccase in the textile industry is growing very fast, since besides to decolourise textile effluents as commented above, laccase is used to bleach textiles and even to synthetise dyes (Setti et al., 1999). Related to textile bleaching, in 1996 Novozyme (Novo Nordisk, Denmark) launched a new industrial application of laccase enzyme in denim finishing: DeniLite®, the first industrial laccase and the first bleaching enzyme acting with the help of a mediator molecule. Also, in 2001 the company Zytex (Zytex Pvt. Ltd., Mumbai, India) developed a formulation based on LMS capable of degrading indigo in a very specific way. The trade name of the product is Zylite. 2.4. Nanobiotechnology During the past two decades, bioelectrochemistry has received increased attention. Progress on bioelectrochemistry has been integrated into analytical applications, e.g. in biosensors working as detectors in clinical and environmental analysis (Haghighi et al., 2003). Since laccases are able to catalyse electron transfer reactions without additional cofactors, their use has also been studied in biosensors to detect various phenolic compounds, oxygen or azides (see Table 1). Moreover, biosensors for detection of morphine and codeine (Bauer et al., 1999), catecholamines (Lisdat et al., 1997; Leite et al., 2003; Ferry and Leech, 2005), plant flavonoids (Jarosz-Wilkołazka et al., 2004) and also for electroimmunoassay (Kuznetsov et al., 2001) have been developed. Nanotechnology contributes to the development of smaller and more efficient biosensors through controlled deposition and specific adsorption of biomolecules on different types of surfaces, achieving micro and nanometer order. Hammond and Whitesides (1995) have introduced a method to pattern ultrathin ionic multilayer films with micron-sized features onto surfaces building a patterned alkanethiol monolayer with ionic functionality onto a gold surface. Typical molecules used in this process are shown in Fig. 1. Chen et al. (1998) showed a biotechnological application of such micropatterned surfaces: the production of islands of micrometer size of extracellular matrix, where the pattern of these islands could determine the position and distribution of bovine and endothelial cells. The control of the nature and the density of the groups (e.g. alkys, amides, alcohols) of a surface built with assembled

506


a)

Polyanions

Polycations

*

*

n*

n*

NH 3+

PAH

SO 3 -

PSS

* *

n*

N+

n*

H3 C

COO -

PAA

CH3

PDADMAC

b) Alkanethiols

Phospholipids

O

O O

O

+

P OCH2CH2NH3

SH

O O

O–

Fig. 1. a) Polylectrolytes are currently used to build multilayers due to their different versatility. PSS: poly(styrene sulfonate); PAA: Poly(acrylic acid), PAH: poly(allylamine hydrochlorid), PDADMAC: poly(diallyldimethylammonium chloride). b) Phospholipid and alkanethiols have the ability to form bilayers and self-assembled monolayers.

monolayers has been used succesfully to investigate the non-specific adsorption of proteins (Sigal et al., 1998). Regarding laccases, the immobilisation has an important influence on the biosensor sensitivity (Freire et al., 2001). Martele et al. (2003) have shown that micropatterning is an efficient method for the immobilisation of laccases on a solid surface in order to develop a multi-functional biosensor. Also, Roy et al. (2005) found that cross-linked enzyme crystals (CLEC) of laccase from Trametes versicolor could be used in biosensor applications with great advantage over the soluble enzyme. More recently, Cabrita et al. (2005) have immobilised laccase from Coriolus versicolor on N-Hydroxysuccinimide-terminated self-assembled monolayers on gold. This procedure could be useful for the further development of biosensors. In addition, an enzyme electrode based on the co-immobilisation of an osmium redox polymer and a laccase from T. versicolor on glassy carbon electrodes has been applied to ultrasensitive amperometric detection of the catecholamine neurotransmitters dopamine, epinephrine and norepinephrine, attaining nanomolar detection limits (Ferry and Leech, 2005). Laccase can also be immobilised

on the cathode of biofuel cells that could provide power, for example, for small transmitter systems (Chen et al., 2001; Calabrese et al., 2002). Biofuel cells are extremely attractive from an environmental point of view because electrical energy is generated without combusting fuel, thus, providing a cleaner source of energy. Fig. 2a shows different functionalised flat surfaces built with polymers and self-assembled monolayers (SAMs) that can be used to adsorb and immobilise proteins or other biomolecules. The layer-by-layer technique (LbL) (Decher, 1997) can be used to build macromolecular structures down to nanometer control leading to surfaces of well-defined thickness (see Fig. 2a). Recently, flat polyelectrolyte multilayers built by alternating adsorption of oppositely charged polyelectrolytes have been used to recrystallise bacterial proteins making the building of artificial cell walls possible (Toca-Herrera et al., 2005). The LbL technique has also been used to build hollow polyelectrolyte capsules after core removal (Donath et al., 1998). Further application of the sequential adsorption of oppositely charged polyelectrolytes onto enzyme crystal templates would permit their encapsulation. Caruso et


a)

507

Enzymes, Proteins

Polyelectrolyte cushion Si, Au, mica, glass

Substrate

Patterning: Polymer Enzyme, protein

Enzyme, protein

SAM S S S S S S S S S S

Si, Au, mica, glass

Au

Substrate

b) Molecules to degrade

Enzyme Polyelectrolyte wall Protein layer

Enzyme, biomolecules Polyelectrolyte wall Colloidal particle

Fig. 2. a) 2D supramacromolecular structures that can be used to immobilise biomolecules. Several structures are suitable: polylectrolyte multilayer, micropatterning and self-assembled monolayers (SAMs). b) 3D supramacromolecular structures that can be used to build microreactors and immobilise biomolecules. In the first case, hollow polelectrolyte shells can host proteins inside, permitting the diffusion of molecules through the shell wall. A colloidal particle covered by polyelectrolytes (and phospholipids) can host proteins and/or other types of functional molecules.

al. (2000) showed that the encapsulated enzyme could retain 100% of its activity after incubation for 100 min with protease. The permeability properties of the wall capsule are important for the proper function of the encapsulated enzyme. Antipov et al. (2002) investigated the permeability properties of hollow polyelectrolyte multilayer capsules as a function of pH and salt concentration. It was shown that the capsule wall was closed to a pH value of 8 and higher, but at pH values

lower than 6 the macromolecules permeate into the capsule interior. In this way, the authors showed how to open and close the capsule wall in a reversible way. This mechanism together with the LbL encapsulation technique permits the development of microreactors Also, colloidal particles covered with polyelectrolytes and phospholipids have been used to host and activate rubella virus (Fischlechner et al., 2005). This type of system is shown in Fig. 2b.

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2.5. Other laccase applications 2.5.1. Soil bioremediation Polycyclic aromatic hydrocarbons (PAHs) together with other xenobiotics are a major source of contamination in soil, therefore, their degradation is of great importance for the environment. The catalytic properties of laccases can be used to degrade such compounds. Thus, laccases were able to mediate the coupling of reduced 2,4,6-trinitrotoluene (TNT) metabolites to an organic soil matrix, which resulted in detoxification of the munition residue (Durán and Esposito, 2000). Moreover, PAHs, which arise from natural oil deposits and utilisation of fossil fuels, were also found to be degraded by laccases (Pointing, 2001). Recently, Nyanhongo et al. (in press) showed that a laccase from Trametes modesta was involved in immobilisation of TNT degradation products. 2.5.2. Synthetic chemistry In the future laccases may also be of great interest in synthetic chemistry, where they have been proposed to be applicable for oxidative deprotection (Semenov et al., 1993) and production of complex polymers and medical agents (Xu, 1999 and Refs. therein, Mai et al., 2000; Uyama and Kobayashi, 2002; Kurisawa et al., 2003; Nicotra et al., 2004). Recently, Mustafa et al. (2005) synthetised phenolic colourants by using an industrial laccase named Suberase® (Novo Nordisk A/S, Bagsvaerdt, Denmark). 2.5.3. Cosmetics The cosmetic world has not been indifferent to the application of laccase: for example, laccase-based hair dyes are less irritant and easier to handle than current hair dyes, since laccases replace H2O2 as an oxidising agent in the dye formulation (Roure et al., 1992; Aaslyng et al., 1996; Lang and Cotteret, 1999). More recently, cosmetic and dermatological preparations containing proteins for skin lightening have also been developed (Golz-Berner et al., 2004). 3. Future outlook The most important obstacles to commercial application of laccases are the lack of sufficient enzyme stocks and the cost of redox mediators. Marked progress has been made over the last years to solve these problems and it is expected that laccases will be able to compete with other processes such as elemental chlorine-free (ECF) and totally chlorine-free (TCF) bleaching. Thus, efforts have to be made in order to achieve cheap overproduc-

tion of this biocatalyst in heterologous hosts and also their modification by chemical means or protein engineering to obtain more robust and active enzymes. On the other hand, the development of an effective system for laccase immobilisation also deserves great attention. Immobilisation could be achieved by chemical modification of the substrates. Hence, micropatterning, SAMs and LbL techniques can be used to functionalise flat and curved surfaces in order to have specific adsorption. Laccase encapsulation with polyelectrolytes will be used as a microreactor for catalytic reactions by changing the permeability properties of the capsule wall. Since the general goal is to obtain stable catalysts with long life times and low cost, we think that the combination of these techniques will enhance: i) the adsorption of laccase on a suitable substrate, ii) the lifetime of the laccase activity and iii) reutilisation of the substrate/laccase product. Our research group is currently working in this direction. Acknowledgments SRC and JLTH are Ramón y Cajal Senior Research Fellows. Therefore, the authors thank the Spanish Ministry of Education and Science for promoting the Ramón y Cajal Programme. References Aaslyng D, Rorbaek K, Sorensen NH, (29.11.1996). An ezyme for dying keratinous fibres. Int Pat Apl WO9719998. Abadulla E, Tzanov T, Costa S, Robra KH, Cavaco-Paulo A, Gübitz G. Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 2000;66: 3357–62. Aggelis G, Iconomou D, Christouc M, Bokas D, Kotzailias S, Christou G, et al. Phenolic removal in a model olive oil mill wastewater using Pleurotus ostreatus in bioreactor cultures and biological evaluation of the process. Water Res 2003;37:3897–904. Akta N, Tanyolaç A. Reaction conditions for laccase catalyzed polymerization of catechol. Bioresour Technol 2003;87:209–14. Akta N, Çiçek H, Tapınar ÜA, Kibarer G, Kolankaya N, Tanyolaç A. Reaction kinetics for laccase-catalyzed polymerization of 1naphthol. Bioresour Technol 2001;80:29–36. Antipov A, Sukhorukov GB, Leporatti S, Radtchenko IL, Donath E, Möhwald H. Polyelectrolyte nultilayer capsule permeability control. Colloids Surf A Physicochem Eng Asp 2002;198-200:535–41. Archibald FS, Bourbonnais R, Jurasek L, Paice MG, Reid ID. Kraft pulp bleaching and delignification by Trametes versicolor. J Biotechnol 1997;53:215–36. Arias ME, Arenas M, Rodríguez J, Soliveri J, Ball AS, Hernández M. Kraft pulp biobleaching and mediated oxidation of a nonphenolic substrate by laccase from Streptomyces cyaneus CECT 3335. Appl Environ Microbiol 2003;69:1953–8. Baker WL, Sabapathy K, Vibat M, Lonergan G. Lactase catalyzes formation of an indamine dye between 3-methyl-2-benzothiazolinone hydrazone and 3-dimethylaminobenzoic acid. Enzyme Microb Technol 1996;18: 90–4.

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