A Review on Properties，Production，and Application of Fungal Laccases

doi:10.13560/j.cnki.biotech.bull.1985.2016.04.003

Abstract

Abstract: As one of copper-containing oxidoreductases，fungal laccase shows better thermal stability，higher metal tolerance and catalytic oxidative to substrates than bacterial or plant ones，and thereby draws great attentions on applications in industry，agriculture and environmental protection. It is widely considered that the factors limiting the extensive application of laccase are production scale，process cost as well as its properties. Laccase can be produced via solid or liquid state fermentation，and the latter is usually adopted for industrial purposes. Recent progress has expanded the novel applications of laccase in addition to its conventional uses such as dye decolorization，treating wastewater of dyeing and paper pulp bleaching. This paper reviews the published literatures in recent years while focusing on the production，properties，and application of fungal laccase.

Key words: white-rot fungi, laccase, fermentation, enzymatic properties, application

LIU Jia-yang，, JIAO Guo-bao ,YOU Xiao-juan ,LIAO Xiang-ru, SUN Li-peng. A Review on Properties，Production，and Application of Fungal Laccases[J]. Biotechnology Bulletin, 2016, 32(4): 24-33.

References

［1］司静, 李伟, 崔宝凯, 等. 真菌漆酶性质、分子生物学及其应用研究进展［J］. 生物技术通报, 2011（2）：48-55.
［2］Couto SR, Toca-Herrera JL. Laccase production at reactor scale by filamentous fungi［J］. Biotechnol Adv 2007, 25：558-569.
［3］Eggert C, Temp U, Eriksson KE. Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus［J］. FEBS Lett, 1997, 407：89-92.
［4］魏玉莲, 戴玉成. 木材腐朽菌在森林生态系统中的功能［J］. 应用生态学报, 2004, 15：1935-1938.
［5］Rodríguez Couto S, Rodríguez A, Paterson RRM, et al. Laccase activity from the fungus Trametes hirsuta using an air-lift bioreactor［J］. Lett Appl Microbial, 2006, 42：612-616.
［6］Baldrian P. Fungal laccases-occurrence and properties［J］. FEMS Microbiol Rev, 2006, 30：215-242.
［7］Tien M, Kirk TK. Lignin-Degrading Enzyme from the Hymenomycete Phanerochaete chrysosporium Burds［J］. Science, 1983, 221：661-663.
［8］Martínez áT, Ruiz-Due?as FJ, Martínez MJ, et al. Enzymatic delignification of plant cell wall：from nature to mill［J］. Curr Opin Biotech, 2009, 20：348-357.
［9］Vivekanand V, Dwivedi P, Sharma A, et al. Enhanced delignification of mixed wood pulp by Aspergillus fumigatus laccase mediator system［J］. World J Microbiol Biotechnol, 2008, 24：2799-2804.
［10］Floudas D, Binder M, Riley R, et al. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes［J］. Science, 2012, 336：1715-1719.
［11］Arora DS, Gill PK. Laccase production by some white rot fungi under different nutritional conditions［J］. Bioresour Technol, 2000, 73：283-285.
［12］Bermek H, Li K, Eriksson L. Laccase-less mutants of the white-rot fungus Pycnoporus cinnabarinus cannot delignify kraft pulp［J］. J Biotechnol, 1998, 66：117-124.
［13］Praveen K, Viswanath B, Usha KY, et al. Lignolytic enzymes of a mushroom Stereum ostrea isolated from wood logs［J］. Enzyme Res, 2011, 2011：ID:749518.
［14］Moreira S, Milagres AMF, Mussatto SI. Reactive dyes and textile effluent decolorization by a mediator system of salt-tolerant laccase from Peniophora cinerea［J］. Sep Purif Technol, 2014, 135：183-189.
［15］Rodgers CJ, Blanford CF, Giddens SR, et al. Designer laccases：a vogue for high-potential fungal enzymes?［J］Trends Biotechnol, 2009, 28：63-72.
［16］Briving C, Gandvik EK, Nyman PO. Structural studies around cysteine and cystine residues in the “blue” oxidase fungal laccase B. Similarity in amino acid sequence with ceruloplasmin［J］. Biochem Bioph Res Commun, 1980, 93：454-461.
［17］Hoegger PJ, Kilaru S, James TY, et al. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences［J］. FEBS J, 2006, 273：2308-2326.
［18］Chernykh A, Myasoedova N, Kolomytseva M, et al. Laccase isoforms with unusual properties from the basidiomycete Steccherinum ochraceum strain 1833［j］. J Appl Microbiol, 2008, 105：2065-2075.
［19］Wang ZX, Cai YJ, Liao XR, et al. Purification and characterization of two thermostable laccases with high cold adapted characteristics from Pycnoporus sp. SYBC-L1［J］. Proc Biochem, 2010, 45：1720-1729.
［20］Yano A, Kikuchi S, Nakagawa Y, et al. Secretory expression of the non-secretory-type Lentinula edodes laccase by Aspergillus oryzae［J］. Microbiol Res, 2009, 164：642-649.
［21］Cantarella G, d’Acunzo F, Galli C. Determination of laccase activity in mixed solvents：comparison between two chromogens in a spectrophotometric assay［J］. Biotech Bioeng, 2003, 82：395-398.
［22］Carunchio F, Crescenzi C, Girelli AM, et al. Oxidation of ferulic acid by laccase：identification of the products and inhibitory effects of some dipeptides［J］. Talanta, 2001, 55：189-200.
［23］Bose S, Mazumder S, Mukherjee M. Laccase production by the white-rot fungus Termitomyces clypeatus［J］. J Basic Microb, 2007, 47：127-131.
［24］Badiani M, Felici M, Luna M, et al. Laccase assay by means of high-performance liquid chromatography［J］. Anal Biochem, 1983, 133：275-276.
［25］Kahraman S, Yesilada O. Industrial and agricultural wastes as substrates for laccase production by white-rot fungi［J］. Folia Microbiol, 2001, 46：133-136.
［26］Elisashvili V, Kachlishvili E. Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes［J］. J Biotechnol, 2009, 144：37-42.
［27］Que Y, Sun S, Xu L, et al. High-level coproduction, purification and characterisation of laccase and exopolysaccharides by Coriolus versicolor［J］. Food Chem, 2014, 159：208-213.
［28］Liu J, Cai Y, Liao X, et al. Purification and Characterization of a novel thermal stable laccase from Pycnoporus sp. SYBC-L3 and its use in dye decolorization［J］. Biol Environ, 2012, 113：1-13.
［29］Yan J, Chen D, Yang E, et al. Purification and characterization of a thermotolerant laccase isoform in Trametes trogii strain and its potential in dye decolorization［J］. Int Biodeter Biodegr, 2014, 93：186-194.
［30］Marbach I, Harel E, Mayer AM. Molecular properties of extracellular Botrytis cinerea laccase［J］. Phytochemistry, 1984, 23：2713-2717.
［31］de la Rubia T, Ruiz E, Perez J, et al. Properties of a laccase produced by Phanerochaete flavido-alba induced by vanillin［J］. Arch Microbiol, 2002, 179：70-73.
［32］Hatakka A. Lignin-modifying enzymes from selected white-rot fungi：production and role from in lignin degradation［J］. FEMS Microbiol Rev, 1994, 13：125-135.
［33］Kurtz MB, Champe SP. Purification and characterization of the conidial laccase of Aspergillus nidulans［J］. J Bacteriol, 1982, 151：1338-1345.
［34］Klonowska A, Gaudin C, Fournel A, et al. Characterization of a low redox potential laccase from the basidiomycete C30［J］. Eur J Biochem, 2002, 269：6119-6125.
［35］ Haibo Z, Yinglong Z, Feng H, et al. Purification and characterizati-on of a thermostable laccase with unique oxidative characteristics from Trametes hirsuta［J］. Biotechnol Lett, 2009, 31：837-843.
［36］Kim Y, Yeo S, Kim MK, et al. Removal of estrogenic activity from endocrine-disrupting chemicals by purified laccase of Phlebia tremellosa［J］. FEMS Microbiol Lett, 2008, 284：172-175.
［37］Eggert C, Temp U, Eriksson K. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus：purification and characterization of the laccase［J］. Appl Environ Microbiol, 1996, 62：1151-1158.
［38］Hsu CA, Wen TN, Su YC, et al. Biological degradation of anthroquinone and azo dyes by a novel laccase from Lentinus sp.［J］. Environ Sci Technol, 2012, 46：5109-5117.
［39］Abadulla E, Tzanov T, Costa S, et al. Decolorization and detoxific-ation of textile dyes with a laccase from Trametes hirsuta［J］. Appl Environ Microbiol, 2000, 66：3357-3362.
［40］Lu L, Zhao M, Zhang BB, et al. Purification and characterization of laccase from Pycnoporus sanguineus and decolorization of an anthraquinone dye by the enzyme［J］. Appl Microbiol Biotechnol, 2007, 74：1232-1239.
［41］Kurniawati S, Nicell JA. Characterization of Trametes versicolor laccase for the transformation of aqueous phenol［J］. Bioresour Technol, 2008, 99：7825-7834.
［42］Couto SR, Sanromán Má. The effect of violuric acid on the decolou-rization of recalcitrant dyes by laccase from Trametes hirsuta［J］. Dyes Pigments, 2007, 74：123-126.
［43］Aktas N, Cicek H, Unal AT, et al. Reaction kinetics for laccase-catalyzed polymerization of 1-naphthol［J］. Bioresour Technol, 2001, 80：29-36.
［44］Aktas N, Sahiner N, Kantoglu O, et al. Biosynthesis and characterization of laccase catalyzed poly（catechol）［J］. J Polym Environ, 2003, 11：123-128.
［45］Alcantara T, Gomez J, Pazos M, et al. Enhanced production of laccase in Coriolopsis rigida grown on barley bran in flask or expanded-bed bioreactor［J］. World J Microbiol Biotechnol, 2007, 23：1189-1194.
［46］Call HP, Mücke I. History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems（Lignozym?-process）［J］. J Biotechnol, 1997, 53：163-202.
［47］Brogioni B, Biglino D, Sinicropi A, et al. Characterization of radical intermediates in laccase-mediator systems. A multifrequency EPR, ENDOR and DFT/PCM investigation［J］. Physical Chemistry Chemical Physics, 2008, 10：7284-7292.
［48］Bertrand T, Jolivalt C, Briozzo P, et al. Crystal structure of a four-copper laccase complexed with an arylamine：insights into substrate recognition and correlation with kinetics［J］. Biochemistry, 2002, 41：7325-7333.
［49］Liu J, Cai Y, Liao X, et al. Efficiency of laccase production in a 65-liter air-lift reactor for potential green industrial and environmental application［J］. J Clean Prod, 2013, 39：154-160.
［50］司静, 崔宝凯, 戴玉成. 栓孔菌属漆酶高产菌株的初步筛选及其产酶条件的优化［J］. 微生物学通报, 2011, 38：405-416.
［51］Quaratino D, Ciaffi M, Federici E, et al. Response surface methodology study of laccase production in Panus tigrinus liquid cultures［J］. Biochem Eng J, 2008, 39：236-245.
［52］Cambria M, Ragusa S, Calabrese V, et al. Enhanced laccase production in white-rot fungus Rigidoporus lignosus by the addition of selected phenolic and aromatic compounds［J］. Appl Biochem Biotechnol, 2010, 163（3）：415-422.
［53］Liu L, Lin Z, Zheng T, et al. Fermentation optimization and characterization of the laccase from Pleurotus ostreatus strain 10969［J］. Enzyme Microb Technol, 2009, 44：426-433.
［54］Liu J, Wang ML, Tonnis B, et al. Fungal pretreatment of switchgrass for improved saccharification and simultaneous enzyme production［J］. Bioresour Technol, 2013, 135：39-45.
［55］D’Souza-Ticlo D, Sharma D, Raghukumar C. A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus［J］. Mar Biotechnol, 2009, 11：725-737.
［56］Wang F, Hu JH, Guo C, et al. Enhanced laccase production by Trametes versicolor using corn steep liquor as both nitrogen source and inducer［J］. Bioresour Technol, 2014, 166：602-605.
［57］Thurston CF. The structure and function of fungal laccases［J］. Microbiology, 1994, 140：19-26.
［58］Pointing SB, Jones EBG, Vrijmoed LLP. Optimization of laccase production by Pycnoporus sanguineus in submerged liquid culture［J］. Mycologia, 2000, 92：139-144.
［59］Fenice M, Giovannozzi Sermanni G, Federici F, et al. Submerged and solid-state production of laccase and Mn-peroxidase by Panus tigrinus on olive mill wastewater-based media［J］. J Biotechnol, 2003, 100：77-85.
［60］Meza JC, Auria R, Lomascolo A, et al. Role of ethanol on growth, laccase production and protease activity in Pycnoporus cinnabarinus ss3［J］. Enzyme Microb Technol, 2007, 41：162-168.
［61］Kuhar F, Papinutti L. Optimization of laccase production by two strains of Ganoderma lucidum using phenolic and metallic inducers［J］. Revista Argentina de Microbiología, 2014, 46：144-149.
［62］Jamroz T, Sencio B, Ledakowicz S. Efficiency of laccase biosynthesis in various types of fermenters［J］. J Biotechnol, 2007, 131S：S161.
［63］Galhaup C, Haltrich D. Enhanced formation of laccase activity by the white-rot fungus Trametes pubescens in the presence of copper［J］. Appl Microbiol Biotechnol, 2001, 56：225-232.
［64］Galhaup C, Wagner H, Hinterstoisser B, et al. Increased production of laccase by the wood-degrading basidiomycete Trametes pubescens［J］. Enzyme Microb Technol, 2002, 30：529-536.
［65］Sharma A, Thakur VV, Shrivastava A, et al. Xylanase and laccase based enzymatic kraft pulp bleaching reduces adsorbable organic halogen（AOX）in bleach effluents：A pilot scale study［J］. Bioresour Technol, 2014, 169：96-102.
［66］Eugenio ME, Santos SM, Carbajo JM, et al. Kraft pulp biobleaching using an extracellular enzymatic fluid produced by Pycnoporus sanguineus［J］. Bioresour Technol, 2010, 101：1866-1870.
［67］Alberts JF, Gelderblom WCA, Botha A, et al. Degradation of aflatoxin B1 by fungal laccase enzymes［］J［. Int J Food Microbiol, 2009, 135：47-52.
［68］Godoy-Navajas J, Aguilar-Caballos MP, Gómez-Hens A. Automatic determination of polyphenols in wines using laccase and terbium oxide nanoparticles［J］. Food Chem, 2015, 166：29-34.
［69］袁海生, 戴玉成, 曹云, 等. 白腐真菌染料脱色菌株筛选及一色齿毛菌脱色条件的研究［J］. 菌物学报, 2010, 29：429-436.
［70］Misra N, Kumar V, Goel NK, et al. Laccase immobilization on radiation synthesized epoxy functionalized polyethersulfone beads and their application for degradation of acid dye［J］. Polymer, 2014, 55：6017-6024.
［71］司静, 崔宝凯, 戴玉成. 东方栓孔菌在染料脱色中的应用及其脱色条件的优化［J］. 基因组学与应用生物学, 2011, 30：364-371.
［72］Liu J, Cai Y, Liao X, et al. Simultaneous laccase production and color removal by culturing fungus Pycnoporus sp. SYBC-L3 in a textile wastewater effluent supplemented with a lignocellulosic waste Phragmites australis［J］. Bull Environ Contam Toxicol, 2012, 89：269-273.
［73］司静, 崔宝凯, 贺帅, 等. 微酸多年卧孔菌产漆酶条件优化及其在染料脱色中的应用［J］. 应用与环境生物学报, 2011, 26：130-137.
［74］Auriol M, Filali-Meknassi Y, Adams CD, et al. Removal of estrogenic activity of natural and synthetic hormones from a municipal wastewater：efficiency of horseradish peroxidase and laccase from Trametes versicolor［J］. Chemosphere, 2008, 70：445-452.
［75］Canfora L, Iamarino G, Rao MA, et al. Oxidative transformation of natural and synthetic phenolic mixtures by Trametes versicolor laccase［J］. J Agric Food Chem, 2008, 56：1398-1407.
［76］Shi L, Ma F, Han Y, et al. Removal of sulfonamide antibiotics by oriented immobilized laccase on Fe3O4 nanoparticles with natural mediators［J］. J Hazard Mater, 2014, 279：203-211.
［77］Polak J, Jarosz-Wilkolazka A. Whole-cell fungal transformation of precursors into dyes［J］. Microb Cell Fact, 2010, 9：51.
［78］López J, Alonso-Omlin EM, Hernández-Alcántara JM, et al. Novel photoluminescent material by laccase-mediated polymerization of 4-fluoroguaiacol throughout defluorination［J］. J Mol Catal B Enzym, 2014, 109：70-75.
［79］Gazme B, Madadlou A. Fabrication of whey protein-pectin conjugate particles through laccase-induced gelation of microemulsified nanodroplets［J］. Food Hydrocolloids, 2014, 40：189-195.
［80］Zhang GQ, Wang YF, Zhang XQ, et al. Purification and characterization of a novel laccase from the edible mushroom Clitocybe maxima［J］. Proc Biochem, 2010, 45：627-633.
［81］Kunamneni A, Camarero S, Garcia-Burgos C, et al. Engineering and applications of fungal laccases for organic synthesis［J］. Microb Cell Fact, 2008, 7：32.
［82］Liu J, Zeng L, Carrow RN, et al. Novel approach for alleviation of soil water repellency using a crude enzyme extract from fungal pretreatment of switchgrass［J］. Soil Res, 2013, 51：322-329.
［83］Zeng L, Liu J, Carrow RN, et al. Evaluation of direct application of enzymes to remediate soil water repellency［J］. HortScience, 2014, 49：662-666.
［84］Sidhu SS, Huang Q, Carrow RN, et al. Use of fungal laccases to facilitate biodethatching：a new approach［J］. HortScience, 2012, 47：1536-1542.
［85］Sidhu SS, Huang Q, Carrow RN, et al. Efficacy of fungal laccase to facilitate biodethatching in Bermudagrass and Zoysiagrass［J］. Agronomy Journal, 2013, 105：1247-1252.

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