Analysis of the Phlebiopsis gigantea Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  Hori, Chiaki ^a   Ishida, Takuya ^a   Igarashi, Kiyohiko ^a   Samejima, Masahiro ^a   Suzuki, Hitoshi ^b   Master, Emma ^b   Ferreira, Patricia ^c   Ruiz Dueñas, Francisco J ^d   Held, Benjamin ^e   Canessa, Paulo ^f   Larrondo, Luis F ^f   Schmoll, Monika ^g   Druzhinina, Irina S ^h   Kubicek, Christian P ^h   Gaskell, Jill A ⁱ   Kersten, Phil ⁱ   St John, Franz ⁱ   Glasner, Jeremy ^j   Sabat, Grzegorz ^j   Splinter BonDurant, Sandra ^j   Syed, Khajamohiddin ^k   Yadav, Jagjit ^k   Mgbeahuruike, Anthony C ^l   Kovalchuk, Andriy ^l   Asiegbu, Fred O ^l   Lackner, Gerald ^m   Hoffmeister, Dirk ^m   Rencoret, Jorge ⁿ   Gutiérrez, Ana ⁿ   Sun, Hui ^o   Lindquist, Erika ^o   Barry, Kerrie ^o   Riley, Robert ^o   Grigoriev, Igor V ^o   Henrissat, Bernard ^p   Kües, Ursula ^q   Berka, Randy M ^r   Martínez, Angel T ^d   Covert, Sarah F ^s   Blanchette, Robert A ^e   Cullen, Daniel ⁱ   more..

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF ZARAGOZA   (Spain)

^d CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^e UNIVERSITY OF MINNESOTA   (United States)

^f PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^g Health and Environment Departmentn Institute of Technology GmbH   (Austria)

^h VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

ⁱ FOREST PRODUCTS LABORATORY   (United States)

^j UNIVERSITY OF WISCONSIN MADISON   (United States)

^k UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^l UNIVERSITY OF HELSINKI   (Finland)

^m FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

ⁿ INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

^o DOE JOINT GENOME INSTITUTE   (United States)

^p AIX MARSEILLE UNIVERSITY   (France)

^q UNIVERSITY OF GÖTTINGEN   (Germany)

^r Novozymes Biotech Inc   (United States)

^s UNIVERSITY OF GEORGIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER G1; ALCOHOL DEHYDROGENASE; ALDEHYDE DEHYDROGENASE; BETA MANNOSIDASE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; CYTOCHROME P450; FUNGAL RNA; GLUCAN SYNTHASE; GLUCOSE OXIDASE; GLUTATHIONE TRANSFERASE; GLYCOSIDASE; HEMICELLULOSE; LACCASE; LIGNIN; LIGNOCELLULOSE; LONG CHAIN FATTY ACID COENZYME A LIGASE; MANGANESE PEROXIDASE; PECTINESTERASE; POLYGALACTURONASE; SECRETOME; TRANSCRIPTOME; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; CELLULOSE; FUNGAL PROTEIN;

ARTICLE; CARBON CYCLING; CHRYSOSPORIUM; CONIFER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; FUNGAL CELL WALL; FUNGAL COLONIZATION; FUNGAL GENOME; GENE EXPRESSION; GENE FUNCTION; MASS FRAGMENTOGRAPHY; MULTIGENE FAMILY; NONHUMAN; PHLEBIOPSIS GIGANTEA; PROTEIN DEGRADATION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; UPREGULATION; WHITE ROT FUNGUS; WOOD; WOOD DECAY FUNGUS; BASIDIOMYCETES; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; SECRETION (PROCESS);

BASIDIOMYCOTA; CONIFEROPHYTA; FUNGI; PHLEBIOPSIS GIGANTEA; PINUS TAEDA;

BASIDIOMYCOTA; CELL WALL; CELLULOSE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; LIGNIN; MOLECULAR SEQUENCE ANNOTATION; TRANSCRIPTOME; WOOD;

EID: 84919682712     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004759     Document Type: Article

References (92)

1. Blanchette R, (1991) Delignification by wood-decay fungi. Ann Rev Phytopath 29: 381–398.
2. Eriksson K-EL, Blanchette RA, Ander P (1990) Microbial and enzymatic degradation of wood and wood components; Timell TE, editor. Berlin: Springer-Verlag.
3. Rayner ADM, Boddy L (1988) Fungal decomposition of wood: its biology and ecology. Chichester: John Wiley and Sons.
4. Kaarik AA (1974) Decomposition of wood. In: Dickinson CH, Pugh GJF, editors.Biology of plant litter composition.New York: Academic Press. pp.129–174.
5. Shigo AL, (1967) Succession of organisms in discoloration and decay wood. Int Rev For Res 2: 237–299.
6. Gutierrez A, Del Rio JC, Martinez AT, (2009) Microbial and enzymatic control of pitch in the pulp and paper industry. Appl Microbiol Biotechnol 82: 1005–1018.
7. Garbelotto M, Guglielmo F, Mascheretti S, Croucher PJ, Gonthier P (2013) Population genetic analyses provide insights on the introduction pathway and spread patterns of the North American forest pathogen Heterobasidion irregulare in Italy. Mol Ecol 10.1111/mec.12452.
8. Rishbeth J, (1963) Stump protection against Fomes annosus. Annals of Applied Biology 52: 63–77.
9. Behrendt CJ, Blanchette RA, (1997) Biological Processing of Pine Logs for Pulp and Paper Production with Phlebiopsis gigantea. Appl Environ Microbiol 63: 1995–2000.
10. Behrendt CJ, Blanchette RA, (2001) Biological control of blue stain in pulpwood: mechanisms of control used by Phlebiopsis gigantea. Holzforschung 55: 238–245.
11. Fischer K, Akhtar M, Blanchette RA, Burnes TA, Messner K, et al. (1994) Reduction in resin content in wood chips during experimental biological pulping processes. Holzforschung 48: 285–290.
12. Martinez-Inigo MJ, Immerzeel P, Gutierrez A, del Rio JC, Sierra-Alvarez R, (1999) Biodegradability of extractives in sapwood and heartwood from Scots Pine by sapstain and white rot fungi. Holzforschung 53: 247–252.
13. Adomas A, Eklund M, Johansson M, Asiegbu FO, (2006) Identification and analysis of differentially expressed cDNAs during nonself-competitive interaction between Phlebiopsis gigantea and Heterobasidion parviporum. FEMS Microbiol Ecol 57: 26–39.
14. Kersten P, Cullen D (2013) Recent advances on the genomics of litter- and soil-inhabiting Agaricomycetes. Genomics of Soil- and Plant-Associated Fungi: Springer. pp. 311–332.
15. Baldrian P, Valaskova V, (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32: 501–521.
16. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233–238.
17. Hori C, Gaskell J, Igarashi K, Samejima M, Hibbett D, et al. (2013) Genome-wide analysis of polysaccharide degrading enzymes in eleven white- and brown-rot polyporales provides insight into mechanisms of wood decay. Mycologia 105: 1412–1427.
18. Bey M, Zhou S, Poidevin L, Henrissat B, Coutinho PM, et al. (2013) Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl Environ Microbiol 79: 488–496.
19. Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JC, et al. (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A 108: 15079–15084.
20. Westereng B, Ishida T, Vaaje-Kolstad G, Wu M, Eijsink VG, et al. (2011) The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS ONE 6: e27807.
21. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, et al. (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715–1719.
22. Fernandez-Fueyo E, Ruiz-Duenas FJ, Ferreira P, Floudas D, Hibbett DS, et al. (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci U S A 109: 5458–5463.
23. Morgenstern I, Klopman S, Hibbett DS, (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. J Mol Evol 66: 243–257.
24. Kawai S, Asukai M, Ohya N, Okita K, Ito T, et al. (1999) Degradation of non-phenolic beta-O-4 susbstructure and of polymeric lignin model compounds by laccase of Coriolus versicolor in the presence of 1-hydroxybenzotriazole. FEMS Microbiol Lett 170: 51–57.
25. 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.
26. Eggert C, Temp U, Eriksson K, (1997) Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett 407: 89–92.
27. Martinez D, Larrondo LF, Putnam N, Sollewijn Gelpke MD, Huang K, et al. (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22: 695–700.
28. Larrondo L, 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.
29. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U, (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273: 2308–2326.
30. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B, (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6: 41.
31. Bastian S, Rekowski MJ, Witte K, Heckmann-Pohl DM, Giffhorn F, (2005) Engineering of pyranose 2-oxidase from Peniophora gigantea towards improved thermostability and catalytic efficiency. Appl Microbiol Biotechnol 67: 654–663.
32. Yadav JS, Soellner MB, Loper JC, Mishra PK, (2003) Tandem cytochrome P450 monooxygenase genes and splice variants in the white rot fungus Phanerochaete chrysosporium: cloning, sequence analysis, and regulation of differential expression. Fungal Genet Biol 38: 10–21.
33. Syed K, Porollo A, Lam YW, Grimmett PE, Yadav JS, (2013) CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol 79: 2692–2702.
34. Syed K, Yadav JS, (2012) P450 monooxygenases (P450ome) of the model white rot fungus Phanerochaete chrysosporium. Crit Rev Microbiol 38: 339–363.
35. Dowd CA, Buckley CM, Sheehan D, (1997) Glutathione S-transferases from the white-rot fungus, Phanerochaete chrysosporium. Biochem J 324 (Pt 1): 243–248.
36. Reiser J, Muheim A, Hardegger M, Frank G, Fiechter A, (1994) Aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium: gene cloning, sequence analysis, expression and purification of recombinant protein. J Biol Chem 269: 28152–28159.
37. Hibbett DS, Donoghue MJ, (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50: 215–242.
38. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al. (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26–32.
39. Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, et al. (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111: 9923–9928.
40. Sjöström E (1993) Wood Chemistry. Fundamentals and Applications. San Diego: Academic Press. 293 p.
41. Kersten PJ, (1990) Glyoxal oxidase of Phanerochaete chrysosporium: Its characterization and activation by lignin peroxidase. Proc Natl Acad Sci USA 87: 2936–2940.
42. de Koker TH, Mozuch MD, Cullen D, Gaskell J, Kersten PJ, (2004) Pyranose 2-oxidase from Phanerochaete chrysosporium: isolation from solid substrate, protein purification, and characterization of gene structure and regulation. Appl Environ Microbiol 70: 5794–5800.
43. Giffhorn F, (2000) Fungal pyranose oxidases: occurrence, properties and biotechnical applications in carbohydrate chemistry. Appl Microbiol Biotechnol 54: 727–740.
44. Sun HW, Plapp BV, (1992) Progressive sequence alignment and molecular evolution of the Zn-containing alcohol dehydrogenase family. J Mol Evol 34: 522–535.
45. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, et al. (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106: 1954–1959.
46. Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, et al. (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333: 762–765.
47. Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, et al. (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77: 7007–7015.
48. Phillips CM, Beeson WT, Cate JH, Marletta MA, (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6: 1399–1406.
49. Macdonald J, Doering M, Canam T, Gong Y, Guttman DS, et al. (2011) Transcriptomic responses of the softwood-degrading white-rot fungus Phanerochaete carnosa during growth on coniferous and deciduous wood. Appl Environ Microbiol 77: 3211–3218.
50. Dorado J, Claassen FW, van Beek TA, Lenon G, Wijnberg JB, et al. (2000) Elimination and detoxification of softwood extractives by white-rot fungi. J Biotechnol 80: 231–240.
51. Gutierrez A, del Rio JC, Gonzalez-Vila FJ, Martin F, (1998) Analysis of lipophilic extractives from wood and pitch deposits by solid-phase extraction and gas chromatography. J Chromatogr 823: 449–455.
52. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265–1272.
53. Daniel G, Volc J, Filonova L, Plihal O, Kubatova E, et al. (2007) Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood. Appl Environ Microbiol 73: 6241–6253.
54. Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S, (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein engineering, design & selection: PEDS 17: 349–356.
55. van Beek TA, Claassen FW, Dorado J, Godejohann M, Sierra-Alvarez R, et al. (2007) Fungal biotransformation products of dehydroabietic acid. J Nat Prod 70: 154–159.
56. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, et al. (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79: 3468–3475.
57. Kumar SV, Phale PS, Durani S, Wangikar PP, (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83: 386–394.
58. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T, (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87: 871–897.
59. Liers C, Pecyna MJ, Kellner H, Worrich A, Zorn H, et al. (2013) Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases. Appl Microbiol Biotechnol 97: 5839–5849.
60. Agger JW, Isaksen T, Varnai A, Vidal-Melgosa S, Willats WG, et al. (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A 10.1073/pnas.1323629111.
61. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, et al. (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330: 219–222.
62. Vanden Wymelenberg A, Minges P, Sabat G, Martinez D, Aerts A, et al. (2006) Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveals complex mixtures of secreted proteins. Fungal Genet Biol 43: 343–356.
63. Wang Y, Lim L, DiGuistini S, Robertson G, Bohlmann J, et al. (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 197: 886–898.
64. Matsuzaki F, Shimizu M, Wariishi H, (2008) Proteomic and metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. J Proteome Res 7: 2342–2350.
65. Shimizu M, Yuda N, Nakamura T, Tanaka H, Wariishi H, (2005) Metabolic regulation at the tricarboxylic acid and glyoxylate cycles of the lignin-degrading basidiomycete Phanerochaete chrysosporium against exogenous addition of vanillin. Proteomics 5: 3919–3931.
66. Annesi T, Curcio G, D'Amico L, Motta E, (2005) Biological control of Heterobasidion annosum on Pinus pinea by Phlebiopsis gigantea. Forest Pathology 35: 127–134.
67. Munir E, Yoon JJ, Tokimatsu T, Hattori T, Shimada M, (2001) A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris. Proc Natl Acad Sci USA 98: 11126–11130.
68. Blanchette RA, Held BW, Arenz BE, Jurgens JA, Baltes NJ, et al. (2010) An Antarctic hot spot for fungi at Shackleton's historic hut on Cape Royds. Microb Ecol 60: 29–38.
69. Grigoriev IV, Martinez DA, Salamov AA (2006) Fungal genomic annotation. In: Arora DK, Berka RA, Singh GB, editors.Applied Mycology and Biotechnology.Amsterdam: Elsevier. pp. 123–142.
70. Parra G, Bradnam K, Korf I, (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061–1067.
71. Vanden Wymelenberg A, Gaskell J, Mozuch MD, Sabat G, Ralph J, et al. (2010) Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol 76: 3599–3610.
72. Ryu JS, Shary S, Houtman CJ, Panisko EA, Korripally P, et al. (2011) Proteomic and functional analysis of the cellulase system expressed by Postia placenta during brown rot of solid wood. Appl Environ Microbiol 77: 7933–7941.
73. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646–4658.
74. Vanden Wymelenberg A, Gaskell J, Mozuch MD, Kersten P, Sabat G, et al. (2009) Transcriptome and secretome analysis of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol 75: 4058–4068.
75. Olson A, Aerts A, Asiegbu F, Belbahri L, Bouzid O, et al. (2012) Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol 194: 1001–1013.
76. Vanden Wymelenberg A, Sabat G, Mozuch MD, Kersten P, Cullen D, et al. (2006) Structure, organization, and transcriptional regulation of a family of copper radical oxidase genes in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 72: 4871–4877.
77. Aspeborg H, Coutinho PM, Wang Y, Brumer H, 3rdHenrissat B, (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12: 186.
78. Rzhetsky A, Nei M, (1992) Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J Mol Evol 35: 367–375.
79. Zuckerkandl J, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors.Evolving genes and proteins. New York: Academic Press.
80. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
81. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
82. Guillen F, Evans CS, (1994) Anisaldehyde and veratraldehyde acting as redox cycling agents for H2O2 production by Pleurotus eryngii. Appl Environ Microbiol 60: 2811–2817.
83. Ferreira P, Ruiz-Duenas FJ, Martinez MJ, van Berkel WJ, Martinez AT, (2006) Site-directed mutagenesis of selected residues at the active site of aryl-alcohol oxidase, an H2O2-producing ligninolytic enzyme. FEBS J 273: 4878–4888.
84. Cavener DR, (1992) GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol 223: 811–814.
85. Thompson JD, Higgins DG, Gibson TJ, (1994) ClustalW improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 2552–2556.
86. Hallberg BM, Henriksson G, Pettersson G, Vasella A, Divne C, (2003) Mechanism of the reductive half-reaction in cellobiose dehydrogenase. J Biol Chem 278: 7160–7166.
87. Lettera V, Piscitelli A, Leo G, Birolo L, Pezzella C, et al. (2010) Identification of a new member of Pleurotus ostreatus laccase family from mature fruiting body. Fungal Biol 114: 724–730.
88. 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.
89. Rühl M, Majcherczyk A, Kues U, (2013) Lcc1 and Lcc5 are the main laccases secreted in liquid cultures of Coprinopsis cinerea strains. Antonie van Leeuwenhoek 103: 1029–1039.
90. Kües U, Rühl M, (2011) Multiple multi-copper oxidase gene families in basidiomycetes - what for? Curr Genomics 12: 72–94.
91. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
92. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.