Abstract
Laccases (benzenediol:oxygen oxidoreductases, EC 1.10.3.2) are blue multicopper oxidases that catalyze the oxidation of an array of aromatic substrates concomitantly with the reduction of molecular oxygen to water. In fungi, laccases carry out a variety of physiological roles during their life cycle. These enzymes are being increasingly evaluated for a variety of biotechnological applications due to their broad substrate range. In this review, the most recent studies on laccase structural features and catalytic mechanisms along with analyses of their expression are reported and examined with the aim of contributing to the discussion on their structure–function relationships. Attention has also been paid to the properties of enzymes endowed with unique characteristics and to fungal laccase multigene families and their organization.
Similar content being viewed by others
References
Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2605
Messerschmidt A (1997) Multi-copper oxidases. World Scientific, Singapore
Yoshida H (1883) Chemistry of lacquer (urushi). Part I. J Chem Soc 43:472–486
Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26
Gianfreda L, Xu F, Bollag JM (1999) Laccases: a useful group of oxidoreductive enzymes. Bioremediat J 3:1–26
Heinzkill M, Messner K (1997) The ligninolytic system of fungi. In: Anke T (ed) Fungal biotechnology. Chapman & Hall, Weinheim, pp 213–226
Bao W, O’Malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260:672–674
Sato Y, Bao W, Sederoff R, Whetten R (2001) Molecular cloning and expression of eight laccase cDNAs in loblolly pine (Pinus taeda). J Plant Res 114:147–155
Sharma P, Goel R, Capalash N (2007) Bacterial laccases. World J Microbiol Biotechnol 23:823–832
Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR (2002) Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 99:2766–2771
Enguita FJ, Martins LO, Henriques AO, Carrondo MA (2003) Crystal structure of a bacterial endospore coat component. A laccase with enhanced thermostability properties. J Biol Chem 278:19416–19425
Dittmer NT, Suderman RJ, Jiang H, Zhu YC, Gorman MJ, Kramer KJ, Kanost MR (2004) Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 34:29–41
Parkinson NM, Conyers CM, Keen JN, MacNicoll AD, Smith I, Weaver RJ (2003) cDNAs encoding large venom proteins from the parasitoid wasp Pimpla hypochondriaca identified by random sequence analysis. Comp Biochem Physiol C Toxicol Pharmacol 134:513–520
Yaropolov AI, Skorobogat’ko OV, Vartanov SS, Varfolomeev SD (1994) Laccase: properties, catalytic mechanism, and applicability. Appl Biochem Biotechnol 49:257–280
Sakurai T (1992) Anaerobic reactions of Rhus vernicifera laccase and its type-2 copper-depleted derivatives with hexacyanoferrate(II). Biochem J 284:681–685
Hofer C, Schlosser D (1999) Novel enzymatic oxidation of Mn2+ to Mn3+ catalyzed by a fungal laccase. FEBS Lett 451:186–190
Schlosser D, Hofer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521
De Souza CGM, Peralta RM (2003) Purification and characterization of the main laccase produced by the white-rot fungus Pleurotus pulmonarius on wheat bran solid state medium. J Basic Microbiol 43:278–286
Shleev SV, Morozova O, Nikitina O, Gorshina ES, Rusinova T, Serezhenkov VA, Burbaev DS, Gazaryan IG, Yaropolov AI (2004) Comparison of physico-chemical characteristics of four laccases from different basidiomycetes. Biochimie 86:693–703
Kumar SVS, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394
Larrondo LF, Salas L, Melo F, Vicuna R, Cullen D (2003) A novel extracellular multicopper oxidase from Phanerochaete chrysosporium with ferroxidase activity. Appl Environ Microbiol 69:6257–6263
Ducros V, Brzozowski AM, Wilson KS, Brown SH, Østergaard P, Schneider P, Yaver DS, Pedersen AH, Davies GJ (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution. Nat Struct Biol 5:310–316
Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-Å resolution containing a full complement of coppers. J Biol Chem 277:37663–37669
Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C, Mougin C (2002) Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41:7325–7333
Garavaglia S, Cambria MT, Miglio M, Ragusa S, Iacobazzi V, Palmieri F, D’Ambrosio C, Scaloni A, Rizzi M (2004) The structure of Rigidoporus lignosus laccase containing a full complement of copper ions, reveals an asymmetrical arrangement for the T3 copper pair. J Mol Biol 342:1519–1531
Ferraroni M, Myasoedova NM, Schmatchenko V, Leontievsky AA, Golovleva LA, Scozzafava A, Briganti F (2007) Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Struct Biol 7:60–72
Matera I, Gullotto A, Tilli S, Ferraroni M, Scozzafava A, Briganti F (2008) Crystal structure of the blue multicopper oxidase from the white-rot fungus Trametes trogii complexed with p-toluate. Inorg Chim Acta 361:4129–4137
Hakulinen N, Kiiskinen LL, Kruus K, Saloheimo M, Paananen A, Koivula A, Rouvinen J (2002) Crystal structure of a laccase from Melanocarpus albomyces with an intact trinuclear copper site. Nat Struct Biol 9:601–605
Hakulinen N, Andberg M, Kallio J, Koivula A, Kruus K, Rouvinen J (2008) A near atomic resolution structure of a Melanocarpus albomyces laccase. J Struc Biol 162:29–39
Murphy MEP, Lindley PF, Adman ET (1997) Structural comparison of cupredoxin domains: domain recycling to construct proteins with novel functions. Protein Sci 6:761–770
Messerschmidt A, Ladenstein R, Huber R, Bolognesi M, Avigliano L, Petruzzelli R, Rossi A, Finazzi Agrò A (1992) Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J Mol Biol 224:179–205
Zaitsev I, Zaitsev V, Card G, Moshkov K, Bax B, Ralph A, Lindley P (1996) The nature of the copper centres in human ceruloplasmin. J Biol Inorg Chem 1:15–23
Lee SK, George SD, Antholine WE, Hedman B, Hodgson KO, Solomon EI (2002) Nature of the intermediate formed in the reduction of O2 to H2O at the trinuclear copper cluster active site in native laccase. J Am Chem Soc 124:6180–6193
Solomon EI, Augustine AJ, Yoon J (2008) O2 reduction to H2O by the multicopper oxidases. Dalton Trans 30:3921–3932
Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811:265–322
Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, Solomon EI (1996) A study of a series of recombinant fungal laccases and birilubin oxidase that exhibit significant differences in redox potential, substrate specificity and stability. Biochim Biophys Acta 1292:303–311
Xu F, Palmer AE, Yaver DS, Berka RM, Gambetta GA, Brown SH, Solomon EI (1999) Targeted mutations in a Trametes villosa laccase, axial perturbations of the T1 copper. J Biol Chem 274:12372–12375
Klonowska A, Gaudin C, Fournel A, Asso M, Le Petit J, Giorgi M, Tron T (2002) Characterization of a low redox potential laccase from the basidiomycete C30. Eur J Biochem 269:6119–6125
Gray HB, Malmstrom BG, Williams RJ (2000) Copper coordination in blue proteins. J Biol Inorg Chem 5:551–559
Durao P, Bento I, Fernandes AT, Melo EP, Lindley PF, Martins LO (2006) Perturbation of the T1 copper site in CotA-laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies. J Biol Inorg Chem 11:514–526
Enguita FJ, Marcal D, Martins LO, Grenha R, Henriques AO, Lindley PF, Carrondo MA (2004) Substrate and dioxygen binding to the endospore coat laccase from Bacillus subtilis. J Biol Chem 279:23472–23476
Xu F (1997) Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem 272:924–928
Xu F, Berka RM, Wahleithner JA, Nelson BA, Shuster JR, Brown SH, Palmer AE, Solomon EI (1998) Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem J 334:63–70
Madzak C, Mimmi MC, Caminade E, Brault A, Baumberger S, Briozzo P, Mougin C, Jolivalt C (2006) Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Eng Des Sel 19:77–84
Bonomo RP, Boudet AM, Cozzolino R, Rizzarelli E, Santoro AM, Sterjiades R, Zappala R (1998) A comparative study of two isoforms of laccase secreted by the “white-rot” fungus Rigidoporus lignosus, exhibiting significant structural and functional differences. J Inorg Biochem 71:205–211
Tadesse MA, D’Annibale A, Galli C, Gentilia P, Sergia F (2008) An assessment of the relative contributions of redox and steric issues to laccase specificity towards putative substrates. Org Biomol Chem 6:868–878
Torres J, Svistunenko D, Karlsson B, Cooper CE, Wilson MT (2002) Fast reduction of a copper center in laccase by nitric oxide and formation of a peroxide intermediate. J Am Chem Soc 124:963–967
Yoon J, Solomon EI (2007) Electronic structure of the peroxy intermediate and its correlation to the native intermediate in the multicopper oxidases: insights into the reductive cleavage of the O–O bond. J Am Chem Soc 129:13127–13136
Yoon J, Liboiron BD, Sarangi R, Hodgson KO, Hedman B, Solomon EI (2007) The two oxidized forms of the trinuclear Cu cluster in the multicopper oxidases and mechanism for the decay of the native intermediate. Proc Natl Acad Sci USA 104:13609–13614
Palmer AE, Lee SK, Solomon EI (2001) Decay of the peroxide intermediate in laccase: reductive cleavage of the O–O bond. J Am Chem Soc 123:6591–6599
Zoppellaro G, Sakurai T, Huang H (2001) A novel mixed valence form of Rhus vernicifera laccase and its reaction with dioxygen to give a peroxide intermediate bound to the trinuclear center. J Biochem 129:949–953
Augustine AJ, Quintanar L, Stoj CS, Kosman DJ, Solomon EI (2007) Spectroscopic and kinetic studies of perturbed trinuclear copper clusters: the role of protons in reductive cleavage of the O–O bond in the multicopper oxidase Fet3p. J Am Chem Soc 129:13118–13126
Augustine AJ, Kragh ME, Sarangi R, Fujii S, Liboiron BD, Stoj CS, Kosman DJ, Hodgson KO, Hedman B, Solomon EI (2008) Spectroscopic studies of perturbed T1 Cu sites in the multicopper oxidases Saccharomyces cerevisiae Fet3p and Rhus vernicifera laccase: allosteric coupling between the T1 and trinuclear Cu sites. Biochemistry 47:2036–2045
Quintanar L, Yoon J, Aznar CP, Palmer AE, Andersson KK, Britt RD, Solomon EI (2005) Spectroscopic and electronic structure studies of the trinuclear Cu cluster active site of the multicopper oxidase laccase: nature of its coordination unsaturation. J Am Chem Soc 127:13832–13845
Bento I, Martins LO, Lopes GG, Carrondo MA, Lindley PF (2005) Dioxygen reduction by multi-copper oxidases; a structural perspective. Dalton Trans 21:3507–3513
Kyritsis P, Messerschmidt A, Huber R, Salmon GA, Sykes AG (1993) Pulse-radiolysis studies on the oxidized form of the multicopper enzyme ascorbate oxidase—evidence for 2 intramolecular electron-transfer steps. Dalton Trans 5:731–735
Fernandez Larrea J, Stahl U (1996) Isolation and characterization of a laccase gene from Podospora anserina. Mol Gen Genet 252:539–551
Germann UA, Muller G, Hunziker PE, Lerch K (1988) Characterization of 2 allelic forms of Neurospora crassa laccase amino-terminal and carboxyl-terminal processing of a precursor. J Biol Chem 263:885–896
Kiiskinen LL, Saloheimo M (2004) Molecular cloning and expression in Saccharomyces cerevisiae of a laccase gene from the ascomycete Melanocarpus albomyces. Appl Environ Microb 70:137–144
Bulter T, Alcalde M, Sieber V, Meinhold P, Schlachtbauer C, Arnold FH (2003) Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microb 69:987–995
Zumárraga M, Camarero S, Shleev S, Martínez-Arias A, Ballesteros A, Plou FJ, Alcalde M (2008) Altering the laccase functionality by in vivo assembly of mutant libraries with different mutational spectra. Proteins 71:250–260
Gelo-Pujic M, Kim HH, Butlin NG, Palmore GT (1999) Electrochemical studies of a truncated laccase produced in Pichia pastoris. Appl Environ Microbiol 65:5515–5521
Giardina P, Palmieri G, Scaloni A, Fontanella B, Faraco V, Cennamo G, Sannia G (1999) Protein and gene structure of a blue laccase from Pleurotus ostreatus. Biochem J 341:655–663
Piscitelli A, Giardina P, Mazzoni C, Sannia G (2005) Recombinant expression of Pleurotus ostreatus laccases in Kluyveromyces lactis and Saccharomyces cerevisiae. Appl Microbiol Biotechnol 69:428–439
Festa G, Autore F, Fraternali F, Giardina P, Sannia G (2007) Development of new laccases by directed evolution: functional and computational analyses. Proteins 72:25–34
Kawai S, Umezawa T, Higuchi T (1988) Degradation mechanisms of phenolic beta-1 lignin substructure model compounds by laccase of Coriolus versicolor. Arch Biochem Biophys 262:99–110
Xu F (1996) Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochem 35:7608–7614
Garzillo AM, Colao MC, Caruso C, Caporale C, Celletti D, Buonocore V (1998) Laccase from the white-rot fungus Trametes trogii. Appl Microbiol Biotechnol 49:545–551
Bajpai P (1999) Application of enzymes in the pulp and paper industry. Biotechnol Prog 15:147–157
Durán N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99
Abadulla E, Tzanov T, Costa S, Robra KH, Cavaco-Paulo A, Gübitz GM (2000) Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 66:3357–3362
Minussi R, Pastore GM, Duran N (2002) Potential applications of laccase in the food industry. Trends Food Sci Technol 13:205–216
Amir L, Tam TK, Pita M, Meijler MM, Alfonta L, Katz E (2009) Biofuel cell controlled by enzyme logic systems. J Am Chem Soc 131:826–832
Pereira L, Coelho AV, Viegas CA, Santos MM, Robalo MP, Martins LO (2009) Enzymatic biotransformation of the azo dye Sudan Orange G with bacterial CotA-laccase. J Biotechnol 139:68–77
Couto SR (2007) Decolouration of industrial azo dyes by crude laccase from Trametes hirsuta. J Hazard Mater 148:768–770
Palmieri G, Cennamo G, Sannia G (2005) Remazol Brilliant Blue R decolourisation by the fungus Pleurotus ostreatus and its oxidative enzymatic system. Enzyme Microb Technol 36:17–24
Palmieri G, Giardina P, Sannia G (2005) Laccase-mediated Remazol Brilliant Blue R decolorization in a fixed-bed bioreactor. Biotechnol Prog 21:1436–1441
Vanhulle S, Trovaslet M, Enaud E, Lucas M, Sonveaux M, Decock C, Onderwater R, Schneider YJ, Corbisier AM (2008) Cytotoxicity and genotoxicity evolution during decolourisation of dyes by white rot fungi. World J Microbiol Biotechnol 24:337–344
Vanhulle S, Trovaslet M, Enaud E, Lucas M, Taghavi S, Van Der Lelie D, Van Aken B, Foret M, Onderwater R, Wesenberg D, Agathos S, Schneider YJ, Corbisier AM (2008) Decolourisation, cytotoxicity and genotoxicity reduction during a combined ozonation/fungal treatment of dye contaminated wastewater. Environ Sci Technol 42:584–589
Kunamneni A, Camarero S, García-Burgos C, Plou FJ, Ballesteros A, Alcalde M (2008) Engineering and applications of fungal laccases for organic synthesis. Microb Cell Fact 7:32–49
Aktaş N, Tanyolaç A (2003) Reaction conditions for laccase catalyzed polymerization of catechol. Bioresour Technol 87:209–214
Ceylan H, Kubilay S, Aktas N, Sahiner N (2008) An approach for prediction of optimum reaction conditions for laccase-catalyzed bio-transformation of 1-naphthol by response surface methodology (RSM). Bioresour Technol 99:2025–2031
Ikeda R, Tanaka H, Oyabu H, Uyama H, Kobayashi S (2001) Preparation of artificial urushi via an environmentally benign process. Bull Chem Soc Jpn 74:1067–1073
Bruyneel F, Enaud E, Billottet L, Vanhulle S, Marchand-Brynaert J (2008) Regioselective synthesis of 3-hydroxyorthanilic acid and its biotransformation with laccase into a novel phenoxazinone dye. Eur J Org Chem 1:72–79
Ossiadacz J, Al-Adhami AJH, Bajraszewska D, Fischer P, Peczynska-Czoch W (1999) On the use of Trametes versicolor laccase for the conversion of 4-methyl-3-hydroxyanthranilic acid to actinocin chromophore. J Biotechnol 72:141–149
Nicotra S, Cramarossa MR, Mucci A, Pagnoni UM, Riva S, Forti L (2004) Biotransformation of resveratrol: synthesis of trans-dehydrodimers catalyzed by laccases from Myceliophtora thermophyla and from Trametes pubescens. Tetrahedron 60:595–600
Bourbonnais R, Paice MG, Freiermuth B, Bodie E, Borneman S (1997) Reactivities of various mediators and laccases with kraft pulp and lignin model compounds. Appl Environ Microbiol 63:4627–4632
Bourbonnais R, Paice MG (1990) Oxidation of nonphenolic substrates—an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102
Barreca AM, Fabbrini M, Galli C, Gentili P, Ljunggren S (2003) Laccase-mediated oxidation of lignin model for improved delignification procedures. J Mol Cat B Enzym 26:105–110
Li K, Xu F, Eriksson KE (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65:2654–2660
Xu F, Kulys JJ, Duke K, Li K, Krikstopaitis K, Deussen HJW, Abbate E, Galinyte V, Schneider P (2000) Redox chemistry in laccase-catalyzed oxidation of N-hydroxy compounds. Appl Environ Microbiol 66:2052–2056
Fabbrini M, Galli C, Gentili P (2002) Comparing the catalytic efficiency of some mediators of laccase. J Mol Cat B Enzym 16:231–240
Brogioni B, Biglino D, Sinicropi A, Reijerse EJ, Giardina P, Sannia G, Lubitz W, Basosi R, Pogni R (2008) Characterization of radical intermediates in laccase-mediator systems. A multifrequency EPR, ENDOR and DFT/PCM investigation. Phys Chem Chem Phys 10:7284–7292
Collins PJ, Kotterman MJJ, Field JA, Dobson ADW (1996) Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Appl Environ Microbiol 62:4563–4567
Camarero S, García O, Vidal T, Colom J, del Río JC, Gutiérrez A, Gras JM, Monje R, Martínez MJ, Martínez T (2004) Efficient bleaching of non-wood high-quality paper pulp using laccase-mediator system. Enzyme Microbiol Technol 35:113–120
Gutiérrez A, del Río JC, Ibarra D, Rencoret J, Romero J, Speranza M, Camarero S, Martínez MJ, Martínez AT (2006) Enzymatic removal of free and conjugated sterols forming pitch deposits in environmentally sound bleaching of eucalypt paper pulp. Environ Sci Technol 40:3416–3422
Hu MR, Chao YP, Zhang GQ, Xue ZQ, Qian S (2009) Laccase-mediator system in the decolorization of different types of recalcitrant dyes. J Ind Microbiol Biotechnol 36:45–51
Galante YM, Formantici C (2003) Enzyme applications in detergency and in manufacturing industries. Curr Org Chem 7:1399–1422
Camarero S, Cañas AI, Nousiainen P, Record E, Lomascolo A, Martínez MJ, Martínez AT (2008) P-hydroxycinnamic acids as natural mediators for laccase oxidation of recalcitrant compounds. Environ Sci Technol 42:6703–6709
Camarero S, Ibarra D, Martínez AT, Romero J, Gutiérrez A, del Río JC (2007) Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 40:1264–1271
Cañas A, Alcalde M, Plou FJ, Martínez MJ, Martínez AT, Camarero S (2007) Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 41:2964–2971
Jeon JR, Murugesan K, Kim YM, Kim EJ, Chang YS (2008) Synergistic effect of laccase mediators on pentachlorophenol removal by Ganoderma lucidum laccase. Appl Microbiol Biotechnol 81:783–790
Nakamura K, Go N (2005) Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci 62:2050–2066
Pezet R (1998) Purification and characterization of a 32-kDa laccase-like stilbene oxidase produced by Botrytis cinerea Pers.:Fr. FEMS Microbiol Lett 167:203–208
Wang HX, Ng TB (2004) Purification of a novel low molecular-mass laccase with HIV-1 reverse transcriptase inhibitory activity from the mushroom Tricholoma giganteum. Biochem Biophys Res Commun 315:450–454
Yaver DS, Xu F, Golightly EJ, Brown KM, Brown SH, Rey MW, Schneider P, Halkier T, Mondorf K, Dalboge H (1996) Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl Environ Microbiol 62:834–841
Min KL, Kim YH, Kim YW, Jung HS, Hah YC (2001) Characterization of a novel laccase produced by the wood-rotting fungus Phellinus ribis. Arch Biochem Biophys 392:279–286
Wahleithner JA, Xu F, Brown KM, Brown SH, Golightly EJ, Halkier T, Kauppinen S, Pederson A, Schneider P (1996) The identification and characterization of four laccases from the plant pathogenic fungus Rhizoctonia solani. Curr Genet 29:395–403
Edens WA, Goins TQ, Dooley D, Henson JM (1999) Purification and characterization of a secreted laccase of Gaeumannomyces graminis var. tritici. Appl Environ Microbiol 65:3071–3074
Junghanns C, Pecyna MJ, Böhm D, Jehmlich N, Martin C, von Bergen M, Schauer F, Hofrichter M, Schlosser D (2009) Biochemical and molecular genetic characterisation of a novel laccase produced by the aquatic ascomycete Phoma sp. UHH 5-1-03. Appl Microbiol Biotechnol. doi:10.1007/s00253-009-2028-2
Wang HX, Ng TB (2006) Purification of a laccase from fruiting bodies of the mushroom Pleurotus eryngii. Appl Microbiol Biotechnol 69:521–525
Ng TB, Wang HX (2004) A homodimeric laccase with unique characteristics from the yellow mushroom Cantharellus cibarius. Biochem Biophys Res Commun 313:37–41
Lawton TJ, Sayavedra-Soto LA, Arp DJ, Rosenzweig AC (2009) Crystal structure of a two-domain multicopper oxidase: implications for the evolution of multicopper blue proteins. J Biol Chem 284:10174–10180
Skálová T, Dohnálek J, Østergaard LH, Østergaard PR, Kolenko P, Dušková J, Štepánková A, Hašek J (2009) The structure of the small laccase from Streptomyces coelicolor reveals a link between laccases and nitrite reductases. J Mol Biol 385:1165–1178
Komori H, Miyazaki K, Higuchi Y (2009) X-ray structure of a two-domain type laccase: a missing link in the evolution of multi-copper proteins. FEBS Lett 583:1189–1195
Wood DA (1980) Production, purification and properties of extracellular laccase of Agaricus bisporus. J Gen Microbiol 117:327–338
Curir P, Thurston CF, Daquila F, Pasini C, Marchesini A (1997) Characterization of a laccase secreted by Armillaria mellea pathogenic for Genista. Plant Physiol Biochem 35:147–153
Minuth W, Klischies M, Esser K (1978) The phenoloxidases of the ascomycete Podospora anserina. Structural differences between laccases of high and low molecular weight. Eur J Biochem 90:73–82
Kurtz MB, Champe SP (1982) Purification and characterization of the conidial laccase of Aspergillus nidulans. J Bacteriol 151:1338–1345
Thakker GD, Evans CS, Rao KK (1992) Purification and characterization of laccase from Monocillium indicum Saxena. Appl Microbiol Biotechnol 37:321–323
Perry CR, Matcham SE, Wood DA, Thurston CF (1993) The structure of laccase protein and its synthesis by the commercial mushroom Agaricus bisporus. J Gen Microbiol 139:171–178
Palmieri G, Cennamo G, Faraco V, Amoresano A, Sannia G, Giardina P (2003) Atypical laccase isoenzymes from copper supplemented Pleurotus ostreatus cultures. Enzyme Microb Technol 33:220–230
Giardina P, Autore F, Faraco V, Festa G, Palmieri G, Piscitelli A, Sannia G (2007) Structural characterization of heterodimeric laccases from Pleurotus ostreatus. Appl Microbiol Biotechnol 75:1293–1300
Hoegger PJ, Kilaru S, James TY, Thacker JR, Kues U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326
Pezzella C, Autore F, Giardina P, Piscitelli A, Sannia G, Faraco V (2009) The Pleurotus ostreatus laccase multi-gene family: isolation and heterologous expression of new family members. Curr Genet 55:45–57
Faraco V, Ercole C, Festa G, Giardina P, Piscitelli A, Sannia G (2008) Heterologous expression of heterodimeric laccase from Pleurotus ostreatus in Kluyveromyces lactis. Appl Microbiol Biotechnol 77:1329–1335
Mei G, Di Venere A, Buganza M, Vecchini P, Rosato N, Finazzi-Agrò A (1997) Role of quaternary structure in the stability of dimeric proteins: the case of ascorbate oxidase. Biochemistry 36:10917–10922
Nicolai E, Di Venere A, Rosato N, Rossi A, Finazzi Agrò A, Mei G (2006) Physico-chemical properties of molten dimer ascorbate oxidase. FEBS J 273:5194–5204
Vries OMH, Kooistra WHCF, Wessels GH (1986) Formation of an extracellular laccase by Schizophyllum commune dikaryon. J Gen Microbiol 132:2817–2826
Leontievsky A, Myasoedova N, Pozdnyakova N, Golovleva L (1997) “Yellow” laccase of Panus tigrinus oxidizes nonphenolic substrates without electron-transfer mediators. FEBS Lett 413:446–448
Leontievsky AA, Vares T, Lankinen P, Shergill JK, Pozdnyakova NN, Myasoedova NM, Kalkkinen N, Golovleva LA, Cammack R, Thurston CF, Hatakka A (1997) Blue and yellow laccases of ligninolytic fungi. FEMS Microbiol Lett 156:9–14
Pozdnyakova NN, Rodakiewicz-Nowak J, Turkovskaya OV (2004) Catalytic properties of yellow laccase from Pleurotus ostreatus D1. J Mol Catal B 30:19–24
Pozdnyakova NN, Turkovskaya OV, Yudina EN, Rodakiewicz-Nowak Ya (2006) Yellow laccase from the fungus Pleurotus ostreatus D1: purification and characterization. Appl Biochem Microbiol 42:56–61
Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A, Sannia G (1997) A novel white laccase from Pleurotus ostreatus. J Biol Chem 272:31301–31307
Litthauer D, Jansen van Vuuren M, van Tonder A, Wolfaardt FW (2007) Purification and kinetics of a thermostable laccase from Pycnoporus sanguineus (SCC 108). Enzyme MicrobTechnol 40:563–568
Haibo Z, Yinglong Z, Feng H, Peiji G, Jiachuan C (2009) Purification and characterization of a thermostable laccase with unique oxidative characteristics from Trametes hirsuta. Biotechnol Lett 31:837–843
Kaneko S, Cheng M, Murai H, Takenaka S, Murakami S, Aoki K (2009) Purification and characterization of an extracellular laccase from Phlebia radiata strain BP-11-2 that decolorizes fungal melanin. Biosci Biotechnol Biochem 73:939–942
Chernykh A, Myasoedova N, Kolomytseva M, Ferraroni M, Briganti F, Scozzafava A, Golovleva L (2008) Laccase isoforms with unusual properties from the basidiomycete Steccherinum ochraceum strain 1833. J Appl Microbiol 105:2065–2075
Hoshida H, Nakao M, Kanazawa H, Kubo K, Hakukawa T, Morimasa K, Akada R, Nishizawa Y (2001) Isolation of five laccase gene sequences from the white-rot fungus Trametes sanguinea by PCR, and cloning, characterization and expression of the laccase cDNA in yeasts. J Biosci Bioeng 92:372–380
Mansur M, Suárez T, Fernández-Larrea JB, Brizuela MA, González AE (1997) Identification of a laccase gene family in the new lignin-degrading basidiomycete CECT 20197. Appl Environ Microbiol 63:2637–2646
Xiao YZ, Hong YZ, Li JF, Hang J, Tong PG, Fang W, Zhou CZ (2006) Cloning of novel laccase isozyme genes from Trametes sp. AH28–2 and analyses of their differential expression. Appl Microbiol Biotechnol 71:493–501
Litvintseva AP, Henson JM (2002) Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the take-all fungus. Appl Environ Microbiol 68:1305–1311
Soden DM, Dobson AD (2001) Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology 147:1755–1763
Rodríguez E, Ruiz-Dueñas FJ, Kooistra R, Ram A, Martínez AT, Martínez MJ (2008) Isolation of two laccase genes from the white-rot fungus Pleurotus eryngii and heterologous expression of the pel3 encoded protein. J Biotechnol 134:9–19
Kilaru S, Hoegger PJ, Kües U (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50:45–60
Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959
Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182:736–750
Chen S, Ge W, Buswell JA (2004) Molecular cloning of a new laccase from the edible straw mushroom Volvariella volvacea: possible involvement in fruit body development. FEMS Microbiol Lett 30:171–176
Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ (1999) A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181:6469–6477
Missal TA, Moran JM, Corbett JA, Lodge JK (2005) Distinct stress responses of two functional laccases in Cryptococcus neoformans are revealed in the absence of the thiol-specific antioxidant Tsa1. Eukaryot Cell 4:202–208
Iakovlev A, Stenlid J (2000) Spatiotemporal patterns of laccase activity in interacting mycelia of wood-decaying basidiomycete fungi. Microb Ecol 39:236–245
Luis P, Kellner H, Zimdars B, Langer U, Martin F, Buscot F (2005) Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microb Ecol 50:570–579
Terrón MC, González T, Carbajo JM, Yagüe S, Arana-Cuenca A, Téllez A, Dobson AD, González AE (2004) Structural close-related aromatic compounds have different effects on laccase activity and on lcc gene expression in the ligninolytic fungus Trametes sp. I-62. Fungal Genet Biol 41:954–962
Solé M, Kellner H, Brock S, Buscot F, Schlosser D (2008) Extracellular laccase activity and transcript levels of putative laccase genes during removal of the xenoestrogen technical nonylphenol by the aquatic hyphomycete Clavariopsis aquatica. FEMS Microbiol Lett 288:47–54
Galhaup C, Goller S, Peterbauer CK, Strauss J, Haltrich D (2002) Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology 148:2159–2169
Collins PJ, Dobson A (1997) Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol 63:3444–3450
Karahanian E, Corsini G, Lobos S, Vicuña R (1998) Structure and expression of a laccase gene from the ligninolytic basidiomycete Ceriporiopsis subvermispora. Biochim Biophys Acta 26:65–74
Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66:920–924
Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206:69–74
Manubens A, Canessa P, Folch C, Avila M, Salas L, Vicuña R (2007) Manganese affects the production of laccase in the basidiomycete Ceriporiopsis subvermispora. FEMS Microbiol Lett 275:139–145
Faraco V, Giardina P, Sannia G (2003) Metal-responsive elements in Pleurotus ostreatus laccase gene promoters. Microbiology 149:2155–2162
Buchman C, Scroch P, Welch J, Fogel S, Karin M (1989) The CUP2 gene product, regulator of yeast metallothionein expression, is a copper-activated DNA-binding protein. Mol Cell Biol 9:4091–4095
Alvarez JM, Canessa P, Mancilla RA, Polanco R, Santibáñez PA, Vicuña R (2009) Expression of genes encoding laccase and manganese-dependent peroxidase in the fungus Ceriporiopsis subvermispora is mediated by an ACE1-like copper-fist transcription factor. Fungal Genet Biol 46:104–111
Giatti Marques De Souza C, Tychanowicz GK, Farani De Souza D, Peralta RM (2004) Production of laccase isoforms by Pleurotus pulmonarius in response to presence of phenolic and aromatic compounds. J Basic Microbiol 44:129–136
Vanhulle S, Enaud E, Trovaslet M, Nouaimeh N, Bols CM, Keshavarz T, Tron T, Sannia G, Corbisier AM (2007) Overlap of laccases/cellobiose dehydrogenase activities during the decolourisation of anthraquinonic dyes with close chemical structures by Pycnoporus strains. Enzyme Microb Technol 40:1723–1731
Eggert C, Temp U, Eriksson KE (1996) The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62:1151–1158
Mansur M, Suárez T, González AE (1998) Differential gene expression in the laccase gene family from basidiomycete I-62 (CECT 20197). Appl Environ Microbiol 64:771–774
Colao MC, Garzillo AM, Buonocore V, Schiesser A, Ruzzi M (2003) Primary structure and transcription analysis of a laccase-encoding gene from the basidiomycete Trametes trogii. Appl Microbiol Biotechnol 63:153–158
Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32:169–178
Ohga S, Smith M, Thurston CF, Wood DA (1999) Transcriptional regulation of laccase and cellulase genes in the mycelium of Agaricus bisporus during fruit body development on a solid substrate. Mycol Res 103:1557–1560
Ohga S, Royse DJ (2001) Transcriptional regulation of laccase and cellulose genes during growth and fruiting of Lentinula edodes on supplemented sawdust. FEMS Microbiol Lett 201:111–115
Zhang S, Hacham M, Panepinto J, Hu G, Shin S, Zhu X, Williamson PR (2006) The Hsp70 member, Ssa1, acts as a DNA-binding transcriptional co-activator of laccase in Cryptococcus neoformans. Mol Microbiol 62:1090–1101
Acknowledgements
This work is supported by grants from the Ministero dell’Università e della Ricerca Scientifica (Progetti di Rilevante Interesse Nazionale, PRIN) and from COST Action FP0602 “Biotechnology for lignocellulose biorefineries” (BIOBIO).
Author information
Authors and Affiliations
Corresponding author
Additional information
Dedicated to the memory of our missed friend and colleague Sophie Vanhulle who died suddenly and tragically.
Rights and permissions
About this article
Cite this article
Giardina, P., Faraco, V., Pezzella, C. et al. Laccases: a never-ending story. Cell. Mol. Life Sci. 67, 369–385 (2010). https://doi.org/10.1007/s00018-009-0169-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-009-0169-1