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Fungal Biodegradation of Lignocelluloses

  • Annele HatakkaEmail author
  • Kenneth E. Hammel
Chapter
Part of the The Mycota book series (MYCOTA, volume 10)

Abstract

Many fungi degrade cellulose and hemicelluloses using extracellular hydrolytic enzymes, but fungi that degrade woody biomass are the only ones to efficiently degrade polysaccharides encased in lignin. White-rot basidiomycetes begin by mineralizing the lignin, using extracellular oxidative enzymes to cleave this recalcitrant biopolymer. Enzymes with likely roles include lignin peroxidases, manganese peroxidases, versatile peroxidases and laccases. In some cases the enzyme may attack the lignin polymer directly; in others the ligninolytic agent is likely a small molecule that one of the enzymes has oxidized to a reactive form. So far, all white rot fungi appear to secrete manganese peroxidases, and most produce laccases, whereas the other two enzymes are less common. After ligninolysis, white-rot fungi assimilate the remaining polysaccharides using conventional glycosylhydrolase systems that contain both endo- and exo-acting enzymes. Brown rot basidiomycetes also degrade lignocellulose efficiently, but their biodegradative systems are less comprehensive. These fungi generally lack ligninolytic enzymes, initiating decay instead with reactive oxygen species generated from the reaction between Fe2+ and H2O2. The limited disruption caused by these oxidants apparently allows a limited set of endo-acting glycosylhydrolases to depolymerize the remaining polysaccharides. Biological wood pulping is one promising application of ligninolytic fungi.

Keywords

Lignin Degradation Versatile Peroxidase Multicopper Oxidase Fenton Reagent Fenton Chemistry 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Akhtar M, Blanchette RA, Myers GC, Kirk TK (1998) An overview of biomechanical pulping research. In: Young RA, Akhtar M (eds) Environmentally friendly technologies for the pulp and paper industry. Wiley, New York, pp 309–419Google Scholar
  2. Ander P, Eriksson KE (1977) Selective degradation of wood components by white-rot fungi. Physiol Plant 41:239–248Google Scholar
  3. Ander P, Hatakka A, Eriksson K-E (1980) Vanillic acid metabolism by the white-rot fungus Sporotrichum pulverulentum. Arch Microbiol 125:189–202Google Scholar
  4. Argyropoulos DS, Menachem SB (1997) Lignin. Adv Biochem Eng Biotechnol 57:127–158Google Scholar
  5. Baldrian P (2006) Fungal laccases – occurrence and properties. FEMS Microbiol Rev 30:215–242Google Scholar
  6. Baldrian P, Valášková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521Google Scholar
  7. Bao W, Fukushima Y, Jensen KA, Moen MA, Hammel KE (1994) Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase. FEBS Lett 354:297–300Google Scholar
  8. Bavendamm W (1928) Über das Vorkommen den Nachweis von Oxydasen bei holzzerstörenden Pilzen. Z Pflanzenkr Pflanzenschutz 38:257–276Google Scholar
  9. Berka RM, Schneider P, Golightly EJ, Brown SH, Madden M, Brown KM, Halkier T, Mondorf K, Xu F (1997) Characterization of the gene encoding an extracellular laccase of Myceliophthora thermophila and analysis of the recombinant enzyme expressed in Aspergillus oryzae. Appl Environ Microbiol 63:3151–3157Google Scholar
  10. Bermek H, Yazici H, Öztürk, Tamerler C, Jung H, Li K, Brown KM, Ding H, Xu F (2004) Purification and characterization of manganese peroxidase from wood-degrading fungus Trichophyton rubrum LSK-27. Enzyme Microb Technol 35:87–92Google Scholar
  11. 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. Biochem 41:7325–7333Google Scholar
  12. Blanchette RA (1995) Degradation of the lignocellulose complex in wood. Can J Bot 73[Suppl 1]:S999–S1010Google Scholar
  13. Blanchette RA, Burnes TA, Leatham GF, Effland MJ (1988) Selection of white-rot fungi for biopulping. Biomass 15:93–101Google Scholar
  14. Blanchette RA, Burnes TA, Eerdmans MM, Akhtar M (1992) Evaluating isolates of Phanerochaete chrysosporium and Ceriporiopsis subvermispora for use in biological pulping processes. Holzforschung 46:109–115Google Scholar
  15. Bollag J-M, Leonowicz A (1984) Comparative studies of extracellular fungal laccases. Appl Environ Microbiol 48:849–854Google Scholar
  16. Bollag JM, Shuttleworth KL, Anderson DH (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54:3086–3091Google Scholar
  17. Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102Google Scholar
  18. Buswell JA, Odier E (1987) Lignin biodegradation. Crit Rev Biotechnol 6:1–60Google Scholar
  19. Call HP, Mücke I (1997) History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (LignozymR-process). J Biotechnol 53:163–202Google Scholar
  20. Camarero S, Ibarra D, Martínez MJ, Martínez ÁT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71:1775–1784Google Scholar
  21. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238Google Scholar
  22. Cho NS, Hatakka AI, Rogalski J, Cho HY, Ohga S (2009) Directional degradation of lignocellulose by Phlebia radiata. J Fac Agric Kyushy Univ 54:73–80Google Scholar
  23. Cohen R, Suzuki MR, Hammel KE (2005) Processive endoglucanase active in crystalline cellulose hydrolysis by the brown-rot basidiomycete Gloeophyllum trabeum. Appl Environ Microbiol 71:2412–2417Google Scholar
  24. Cowling EB (1961) Comparative biochemistry of the decay of sweetgum sapwood by white-rot and brown-rot fungi. USDA Tech Bull 1258Google Scholar
  25. Cunha GGS, Masarin F, Norambuena M, Freer J, Ferraz A (2010) Linoleic acid peroxidation and lignin degradation by enzymes produced by Ceriporiopsis subvermispora grown on wood or in submerged liquid cultures. Enzyme Microb Technol 46:262–267Google Scholar
  26. Decker SR, Siika-Aho M, Viikari L (2008) Enzymatic depolymerization of plant cell wall hemicelluloses. In: Himmel ME (ed) Biomass recalcitrance. Deconstruction of the plant cell wall for bioenergy. Blackwell, London, pp 353–373Google Scholar
  27. Dedeyan B, Klonowska A, Tagger S, Tron T, Iacazio G, Gil G, Petit JL (2000) Biochemical and molecular characterization of a laccase from Marasmius quercophilus. Appl Environ Microbiol 66:925–929Google Scholar
  28. Ding S-Y, Himmel ME (2008) Anatomy and ultrastructure of maize cell walls: an example of energy plants. In: Himmel ME (ed) Biomass recalcitrance. Deconstruction of the plant cell wall for bioenergy. Blackwell, London, pp 38–60Google Scholar
  29. D’Souza TM, Boominathan K, Reddy CA (1996) Isolation of laccase gene-specific sequences from white-rot and brown-rot fungi by PCR. Appl Environ Microbiol 62:3739–3744Google Scholar
  30. 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 5:310–316Google Scholar
  31. Eggert C, Temp U, Dean JFD, Eriksson KEL (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144–148Google Scholar
  32. Enoki A, Hirano T, Tanaka H (1992) Extracellular substance from the brown-rot basidiomycete Gloeophyllum trabeum that produces and reduces hydrogen peroxide. Mater Org 27:247–261Google Scholar
  33. Enoki A, Itakura S, Tanaka H (1997) The involvement of extracellular substances for reducing molecular oxygen to hydroxyl radical and ferric iron to ferrous iron in wood degradation by wood decay fungi. J Biotechnol 53:265–272Google Scholar
  34. Eriksson KE, Blanchette RA, Ander P (1990) Microbial and enzymatic degradation of wood and wood components. Springer, Berlin Heidelberg New YorkGoogle Scholar
  35. Ferraroni M, Myasoedova N, 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 7:60–72Google Scholar
  36. Ferraz A, Guerra A, Mendonça R, Masarin F, Vicentim MP, Aguiar A, Pavan PC (2008) Technological advances and mechanistic basis for fungal biopulping. Enzyme Microb Technol 43:178–185Google Scholar
  37. Ferrer I, Esposito E, Duran N (1992) Lignin peroxidase from Chrysonilia sitophila : Heat-denaturation kinetics and pH stability. Enzyme Microb Technol 14:402–406Google Scholar
  38. Filley TR, Cody GD, Goodell B, Jellison J, Noser C, Ostrofsky A (2002) Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown-rot fungi. Org Geochem 33:111–124Google Scholar
  39. Foust TD, Ibsen KN, Dayton DC, Hess JR, Kenney KE (2008) The biorefinery. In: Himmel ME (ed) Biomass recalcitrance. Deconstruction of the plant cell wall for bioenergy. Blackwell, London, pp 7–37Google Scholar
  40. Fritsche W, Hofrichter M (2004) Aerobic degradation of recalcitrant organic compounds by microorganisms. In: Jördening H-J, Winter J (eds) Environmental biotechnology. Wiley-VCH, Weinheim, pp 203–227Google Scholar
  41. Galhaup C, Haltrich D (2001) Enhanced formation of laccase activity by the white-rot fungus Trametes pubescens in the presence of copper. Appl Microbiol Biotechnol 56:225–232Google Scholar
  42. Galkin S, Vares T, Kalsi M, Hatakka A (1998) Production of organic acids by different white-rot fungi as detected using capillary zone electrophoresis. Biotechnol Tech 12:267–271Google Scholar
  43. Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010) Laccases: a never-ending story. Cell Mol Life Sci 67: 369–385Google Scholar
  44. Gilbertson RL (1980) Wood-rotting fungi of North America. Mycologia 72:1–49Google Scholar
  45. Gilbertson RL, Ryvarden L (1986) North American polypores. Fungiflora, OsloGoogle Scholar
  46. Gold MH, Youngs HL, Sollewijn Gelpke MD (2000) Manganese peroxidase. In: Sigel A, Sigel H (eds) Metal ions in biological systems. Dekker, New York, pp 559–586Google Scholar
  47. Gonzales L, Hernáandez JR, Perestelo F, Carnicero A, Falcón MA (2002) Relationship between mineralization of synthetic lignins and the generation of hydroxyl radicals by laccase and a low-molecular weight substance produced by Petriellidium fusoideum. Enzyme Microb Technol 30:474–481Google Scholar
  48. Gramss G (1992) Invasion of wood by basidiomycetous fungi. VI. Quantitative but not qualitative differences in the pathovirulence of pathogenic and saprophytic decay fungi. J Basic Microbiol 32:75–90Google Scholar
  49. Green F, Larsen MJ, Winandy JE, Highley TL (1991) Role of oxalic-acid in incipient brown-rot decay. Mater Org 26:191–213Google Scholar
  50. Haider K, Trojanowski J (1975) Decomposition of specifically 14C-labelled phenol and dehydropolymers of coniferyl alcohols as model for lignin degradation by soft- and white-rot fungi. Arch Microbiol 105:33–41Google Scholar
  51. Hakala TK, Maijala P, Konn J, Hatakka A (2004) Evaluation of novel wood-rotting polypores and corticioid fungi for the decay and biopulping of Norway spruce (Picea abies) wood. Enzyme Microb Technol 34:255–263Google Scholar
  52. Hakala TK, Lundell T, Galkin S, Maijala P, Kalkkinen N, Hatakka A (2005) Manganese peroxidases, laccases and oxalic acid from the selective white-rot fungus Physisporinus rivulosus grown on spruce wood chips. Enzyme Microb Technol 36:461–468Google Scholar
  53. Hakala TK, Hildén K, Maijala P, Olsson C, Hatakka A (2006) Differential regulation of manganese peroxidases and characterization of two variable MnP encoding genes in the white-rot fungus Physisporinus rivulosus. Appl Microbiol Biotechnol 73:839–849Google Scholar
  54. Hakulinen N, Kiiskinen L-L, 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 9:601–605Google Scholar
  55. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  56. Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355Google Scholar
  57. Hammel KE, Kapich AN, Jensen KA, Ryan ZC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453Google Scholar
  58. Harreither W, Sygmund C, Dünhofen E, Vicuna R, Haltrich D, Ludwig R (2009) Cellobiose dehydrogenase from the ligninolytic basidiomycete Ceriporiopsis subvermispora. Appl Environ Microbiol 75:2750–2757Google Scholar
  59. Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi – production and role in lignin degradation. FEMS Microbiol Rev 13:125–135Google Scholar
  60. Hatakka A (2001) Biodegradation of lignin. In: Hofrichter M, Steinbüchel A (eds) Biopolymers, vol 1: Lignin, humic substances and coal. Wiley-VCH, Weinheim, pp 129–180Google Scholar
  61. Hatakka A, Uusi-Rauva AK (1983) Degradation of 14C-labelled poplar wood lignin by selected white-rot fungi. Eur J Appl Microbiol Biotechnol 17:235–242Google Scholar
  62. Hatakka A, Buswell JA, Pirhonen TI, Uusi-Rauva AK (1983) Degradation of 14C‑labelled lignins by white-rot fungi. In: Higuchi T, Chang H-M, Kirk TK (eds) Recent advances in lignin biodegradation research. UNI Publishers, Tokyo, pp 176–187Google Scholar
  63. Hatakka A, Lundell T, Hofrichter M, Maijala P (2003) Manganese peroxidase and its role in the degradation of wood lignin. In: Mansfield SD, Saddler JN (eds) Applications of enzymes to lignocellulosics. ACS symposium series 855. ACS, New York, pp 230–243Google Scholar
  64. Heidorne FO, Magalhães PO, Ferraz AL, Milagres AMF (2006) Characterization of hemicellulases and cellulases produced by Ceriporiopsis subvermispora grown on wood under biopulping conditions. Enzyme Microb Technol 38:436–442Google Scholar
  65. Henriksson G, Johansson G, Pettersson G (2000) A critical review of cellobiose dehydrogenases. J Biotechnol 78:93–113Google Scholar
  66. Herr D, Baumer F, Dellweg H (1978) Purification and properties of an extracellular endo-1,4-beta-glucanase from Lenzites trabea. Arch Microbiol 117:287–292Google Scholar
  67. Hibbett DS, Thorn RG (2001) Basidiomycota: Homobasidiomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The Mycota. Springer, Berlin Heidelberg New York, pp 121–168Google Scholar
  68. Higuchi T (1990) Biosynthesis of lignin. Springer, Berlin Heidelberg New YorkGoogle Scholar
  69. Hildén K, Martinez AT, Hatakka A, Lundell T (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent. Fungal Gen Biol 42:403–419Google Scholar
  70. Hildén KS, Bortfeldt R, Hofrichter M, Hatakka A, Lundell TK (2008) Molecular characterization of the basidiomycete isolate Nematoloma frowardii b19 and its manganese peroxidase places the fungus in the corticioid genus Phlebia. Microbiology 154:2371–2379Google Scholar
  71. 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 273:2308–2326Google Scholar
  72. Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466Google Scholar
  73. Hofrichter M, Vares K, Scheibner K, Galkin S, Sipilä J, Hatakka A (1999a) Mineralization and solubilization of synthetic lignin by manganese peroxidases from Nematoloma frowardii and Phlebia radiata. J Biotechnol 67:217-228Google Scholar
  74. Hofrichter M, Vares T, Kalsi M, Galkin S, Scheibner K, Fritsche W, Hatakka A (1999b) Production of manganese peroxidase and organic acids and mineralization of 14C-labelled lignin (14C-DHP) during solid-state fermentation of wheat straw with the white-rot fungus Nematoloma frowardii. Appl Environ Microbiol 65:1864–1870Google Scholar
  75. Hyde SM, Wood PM (1997) A mechanism for production of hydroxyl radicals by the brown-rot fungus Coniophora puteana: Fe(III) reduction by cellobiose dehydrogenase and Fe(II) oxidation at a distance from the hyphae. Microbiology 143:259–266Google Scholar
  76. Irbe I, Andersone I, Andersons B, Chirkova J (2001) Use of C-13 NMR, sorption and chemical analyses for characteristics of brown-rotted Scots pine. Int Biodeter Biodeg 47:37–45Google Scholar
  77. Irwin DC, Spezio M, Walker LP, Wilson DB (1993) Activity studies of eight purified cellulases – specificity, synergism, and binding domain effects. Biotechnol Bioeng 42:1002–1013Google Scholar
  78. Käärik A (1965) The identification of the mycelia of wood-decay fungi by their oxidation reactions with phenolic compounds. Stud For Suec 31:1–79Google Scholar
  79. Kanayama N, Suzuki T, Kawai K (2002) Purification and characterization of an alkaline manganese peroxidase from Aspergillus terreus LD-1. J Biosci Bioeng 93:405–410Google Scholar
  80. Kapich A, Hofrichter M, Vares T, Hatakka A (1999) Coupling of manganese peroxidase-mediated lipid peroxidation with destruction of nonphenolic lignin model compounds and 14C-labeled lignins. Biochem Biophys Res Commun 259:212–219Google Scholar
  81. Kapich AN, Steffen KT, Hofrichter M, Hatakka A (2005) Involvement of lipid peroxidation in the degradation of a non-phenolic lignin model compound by manganese peroxidase of the litter-decomposing fungus Stropharia coronilla. Biochem Biophys Res Commun 330:371–377Google Scholar
  82. Karhunen P, Rummakko P, Sipilä J, Brunow G, Kilpeläinen I (1995) Dibenzodioxocins; a novel type of linkage in softwood lignins. Tetrahedron Lett 36:169–170Google Scholar
  83. Kawai SK, Jensen KA, Bao W, Hammel KE (1995) New polymeric model substrates for the study of microbial ligninolysis. Appl Environ Microbiol 61:3407–3414Google Scholar
  84. Kawai S, Iwatsuki M, Nakagawa M, Inagaki M, Hamabe A, Ohashi H (2004) An alternative β-ether cleavage pathway for a non-phenolic β-O-4 lignin model dimer catalyzed by a laccase-mediator system. Enzyme Microb Technol 35:154–160Google Scholar
  85. Kerem Z, Jensen KA, Hammel KE (1999) Biodegradative mechanism of the brown-rot basidiomycete Gloeophyllum trabeum: evidence for an extracellular hydroquinone-driven Fenton reaction. FEBS Lett 446:49–54Google Scholar
  86. Kersten P, Cullen D (2007) Extracellular oxidative systems of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol 44:77–87Google Scholar
  87. Kirk TK (1975) Effects of a brown-rot fungus, Lenzites trabea, on lignin in spruce wood. Holzforschung 29:99–107Google Scholar
  88. Kirk TK, Adler E (1970) Methoxyl-deficient structural elements in lignin of sweetgum decayed by a brown-rot fungus. Acta Chem Scand 24:3379–3390Google Scholar
  89. Kirk TK, Cullen D (1998) Enzymology and molecular genetics of wood degradation by white-rot fungi. In: Young RA, Akhtar M (eds) Environmentally friendly technologies for the pulp and paper industry. Wiley, New York, pp 273–307Google Scholar
  90. Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Ann Rev Microbiol 41:465–505Google Scholar
  91. Kirk TK, Connors WJ, Bleam RD, Hackett WF, Zeikus JG (1975) Preparation and microbial decomposition of synthetic (14C) lignins. Proc Natl Acad Sci USA 72:2515–2519Google Scholar
  92. Kirk TK, Schultz E, Connors WJ, Lorenz LF, Zeikus JG (1978) Influence of culture parameters on lignin metabolism by Phanerochaete chrysosporium. Arch Microbiol 117:277–285Google Scholar
  93. Kirk TK, Ibach R, Mozuch MD, Conner AH, Highley TL (1991) Characteristics of cotton cellulose depolymerized by a brown-rot fungus, by acid, or by chemical oxidants. Holzforschung 45:239–244Google Scholar
  94. Kishi K, Wariishi H, Marquez L, Dunford BH, Gold MH (1994) Mechanism of manganese peroxidase II reduction. Effect of organic acid chelators and pH. Biochemistry 33:8694–8701Google Scholar
  95. Kluczek-Turpeinen B, Tuomela M, Hatakka A, Hofrichter M (2003) Lignin degradation in a compost environment by the deuteromycete Paecilomyces inflatus. Appl Microbiol Biotechnol 61:374–379Google Scholar
  96. Koenigs JW (1974) Production of hydrogen peroxide by wood-rotting fungi in wood and its correlation with weight loss, depolymerization, and pH changes. Arch Microbiol 99:129–145Google Scholar
  97. Lee KH, Wi SG, Singh AP, Kim YS (2004) Micromorphological characteristics of decayed wood and laccase produced by the brown-rot fungus Coniophora puteana. J Wood Sci 50:281–284Google Scholar
  98. Levasseur A, Piumi F, Coutinho PM, Rancurel C, Asther M, Delattre M, Henrissat B, Pontarotti P, Asther M, Record E (2008) FOLy: An integrated database for the classification and functional annotation of fungal oxidoreductases potentially involved in the degradation of lignin and related aromatic compounds. Fungal Gen Biol 45:638–645Google Scholar
  99. Liers C, Ullrich R, Steffen KT, Hatakka A, Hofrichter M (2006) Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Appl Microbiol Biotechnol 69:573–579Google Scholar
  100. Lobos S, Tello M, Polanco R, Larrondo LF, Manubens A, Salas L, Vicuña R (2001) Enzymology and molecular genetics of the ligninolytic system of the basidiomycete Ceriporiopsis subvermispora. Curr Sci 81:992–997Google Scholar
  101. Lundell T, Mäkela M, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes: ecological, functional and phylogenetic review. J Basic Microbiol 50:1–16Google Scholar
  102. Lundquist K, Kirk TK (1978) De novo synthesis and decomposition of veratryl alcohol by a lignin-degrading basidiomycete. Phytochemistry 17:1676Google Scholar
  103. Luthardt W (1969) Was ist Mykoholz? (What is mycowood?) Ziemsen, WittenbergGoogle Scholar
  104. Luthardt W (2005) Holzbewohnende Pilze: Anzucht und Holzmykologie (Wood colonizing fungi: cultivation and wood mycology), 2nd edn. Die Neue Brehm-Bücherei Bd 403Google Scholar
  105. Machuca A, Ferraz A (2001) Hydrolytic and oxidative enzymes produced by white- and brown-rot fungi during Eucalyptus grandis decay in solid medium. Enzyme Microb Technol 29:386–391Google Scholar
  106. Maijala P, Kleen M, Westin C, Poppius-Levlin K, Herranen K, Lehto JH, Reponen P, Mäentausta O, Mettälä A, Hatakka A (2008) Biomechanical pulping of softwood with enzymes and white-rot fungus Physisporinus rivulosus. Enzyme Microb Technol 43:169–177Google Scholar
  107. Mäkelä M, Galkin S, Hatakka A, Lundell T (2002) Production of organic acids and oxalate decarboxylase in lignin-degrading white-rot fungi. Enzyme Microb Technol 30:542–549Google Scholar
  108. Mäkelä MR, Hildén K, Hatakka A, Lundell TK (2009) Oxalate decarboxylase of the white-rot fungus Dichomitus squalens demonstrates a novel enzyme primary structure and non-induced expression on wood and in liquid cultures. Microbiology 155:2726–2738Google Scholar
  109. Mansfield SD, Saddler JN, Gübitz GM (1998) Characterization of endoglucanases from the brown-rot fungi Gloeophyllum sepiarium and Gloeophyllum trabeum. Enzyme Microb Technol 23:133–140Google Scholar
  110. Martínez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb Technol 30:425–444Google Scholar
  111. Martínez ÁT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, Del Río JC (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204Google Scholar
  112. Martinez D, Larrondo LF, Putnam N, Sollewijn-Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700Google Scholar
  113. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EGJ, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, Lopez de Leon A, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin ER, Dunn-Coleman N, Ward M, Brettin TS (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:553–560Google Scholar
  114. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Dueñas FJ, Martinez AT, Kersten P, Hammel KE, Wymelenberg AV, Gaskell J, Lindquist E, Sabat G, BonDurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavin 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, Lucash 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 106:1954–1959Google Scholar
  115. Medve J, Karlsson J, Lee D, Tjerneld F (1998) Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: Adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol Bioeng 59:621–634Google Scholar
  116. Miki Y, Morales M, Ruiz-Dueñas FJ, Martinez MJ, Wariishi H, Martinez AT (2009) Escherichia coli expression and in vitro activation of a unique ligninolytic peroxidase that has a catalytic tyrosine residue. Protein Expr Purif 68:208–214Google Scholar
  117. Morgenstern I, Klopman S, Hibbett DS (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. J Mol Evol 66:243–257Google Scholar
  118. Niemenmaa O, Uusi-Rauva A, Hatakka A (2008) Demethoxylation of [(OCH3)-C-14]-labelled lignin model compounds by the brown-rot fungi Gloeophyllum trabeum and Poria (Postia) placenta. Biodegradation 19:555–565Google Scholar
  119. Nilsson T, Ginns J (1979) Cellulolytic activity and the taxonomic position of selected brown-rot fungi. Mycologia 71:170–177Google Scholar
  120. Nilsson T, Daniel G, Kirk TK, Obst JR (1989) Chemistry and microscopy of wood decay by some higher ascomycetes. Holzforschung 43:11–18Google Scholar
  121. Nousiainen P, Maijala P, Hatakka A, Martinez AT, Sipilä J (2009) Syringyl-type simple plant phenolics as mediating oxidants in laccase catalyzed degradation of lignocellulosic materials: Model compound studies. Holzforschung 63:699–704Google Scholar
  122. Orth AB, Royse DJ, Tien M (1993) Ubiquity of lignin-degrading peroxidases among various wood-degrading fungi. Appl Environ Microbiol 59:4017–4023Google Scholar
  123. Otjen L, Blanchette RA (1987) Assessment of 30 white-rot basidiomycetes for selective lignin degradation. Holzforschung 41:343–349Google Scholar
  124. Park JSB, Wood PM, Davies MJ, Gilbert BC, Whitwood AC (1997) A kinetic and ESR investigation of Iron(II) oxalate oxidation by hydrogen peroxide and dioxygen as a source of hydroxyl radicals. Free Radical Res 27:447–458Google Scholar
  125. Paszczynski A, Crawford R, Funk D, Goodell B (1999) De novo synthesis of 4,5-dimethoxycatechol and 2,5-dimethoxyhydroquinone by the brown-rot fungus Gloeophyllum trabeum. Appl Environ Microbiol 65:674–679Google Scholar
  126. Perez J, Jeffries T (1992) Roles of manganese and organic acid chelators in regulating lignin degradation and biosynthesis of peroxidases by Phanerochaete chrysosporium. Appl Environ Microbiol 58:2402–2409Google Scholar
  127. Pérez-Boada M, Ruiz-Dueñas FJ, Pogni R, Basosi R, Choinowski T, Martínez MJ, Piontek K, Martínez AT (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways. J Mol Biol 354:385–402Google Scholar
  128. 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 277:37663–37669Google Scholar
  129. Regalado V, Rodríguez A, Perestelo F, Carnicero A, De La Fuente G, Falcon MA (1997) Lignin degradation and modification by the soil-inhabiting fungus Fusarium proliferatum. Appl Environ Microbiol 63:3716–3718Google Scholar
  130. Regalado V, Perestelo F, Rodríguez A, Carnicero A, Sosa FJ, De La Fuente G, Falcón MA (1999) Activated oxygen species and two extracellular enzymes: Laccase and aryl-alcohol oxidase, novel for the lignin-degrading fungus Fusarium proliferatum. Appl Microbiol Biotechnol 51:388–390Google Scholar
  131. Ritschkoff AC, Buchert J, Viikari L (1994) Purification and characterization of a thermophilic xylanase from the brown-rot fungus Gloeophyllum trabeum. J Biotechnol 32:67–74Google Scholar
  132. Rochefort D, Leech D, Bourbonnais R (2004) Electron transfer mediator systems for bleaching of paper pulp. Green Chem 6:14–24Google Scholar
  133. Rodriguez A, Carnicero A, Perestelo F, De la Fuente G, Milstein O, Falcon MA (1994) Effect of Penicillium chrysogenum on lignin transformation. Appl Environ Microbiol 60:2971–2976Google Scholar
  134. Rodriguez A, Perestelo F, Carnicero A, Regalado V, Perez R, De La Fuente G, Falcon MA (1996) Degradation of natural lignins and lignocellulosic substrates by soil-inhabiting fungi imperfecti. FEMS Microbiol Ecol 21:213–219Google Scholar
  135. Ruiz-Dueñas FJ, Martínez ÁT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2:164–177Google Scholar
  136. Ruiz-Dueñas FJ, Morales M, Garcia E, Miki Y, Martinez MJ, Martinez AT (2009) Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60:441–452Google Scholar
  137. Schmidhalter DR, Canevascini G (1992) Characterization of the cellulolytic enzyme system from the brown-rot fungus Coniophora puteana. Appl Microbiol Biotechnol 37:431–436Google Scholar
  138. Schneider P, Caspersen MB, Mondorf K, Halkier T, Skov LK, Ostergaard PR, Brown KM, Brown SH, Xu F (1999) Characterization of a Coprinus cinereus laccase. Enzyme Microb Technol 25:502–508Google Scholar
  139. Shary S, Kapich AN, Panisko EA, Magnuson JK, Cullen D, Hammel KE (2008) Differential expression in Phanerochaete chrysosporium of membrane-associated proteins relevant to lignin degradation. Appl Environ Microbiol 74:7252–7257Google Scholar
  140. Shimokawa T, Nakamura M, Hayashi N, Ishihara M (2004) Production of 2,5-dimethoxyhydroquinone by the brown-rot fungus Serpula lacrymans to drive extracellular Fenton reaction. Holzforschung 58:305–310Google Scholar
  141. Sjöström E (1993) Wood chemistry, fundamentals and applications. Academic, San DiegoGoogle Scholar
  142. Steffen KT, Hofrichter M, Hatakka A (2000) Mineralisation of 14C-labelled synthetic lignin and ligninolytic enzyme activities of litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 54:819–825Google Scholar
  143. Steffen KT, Hofrichter M, Hatakka A (2002) Purification and characterization of manganese peroxidases from the litter-decomposing basidiomycetes Agrocybe praecox and Stropharia coronilla. Enzyme Microb Technol 30:550–555Google Scholar
  144. Sundaramoorthy M, Kishi K, Gold MH, Poulos TL (1997) The crystal structures of substrate binding site mutants of manganese peroxidase. J Biol Chem 272:17574–17580Google Scholar
  145. Suzuki MR, Hunt CG, Houtman CJ, Dalebroux ZD, Hammel KE (2006) Fungal hydroquinones contribute to brown-rot of wood. Environ Microbiol 8:2214–2223Google Scholar
  146. Tadesse MH, D’Annibale A, Galli C, Gentili P, Sergi F (2008) An assessment of the relative contributions of redox and steric issues to laccase specificity towards putative substrates. Org Biomol Chem 6:868–878Google Scholar
  147. Tanaka H, Yoshida G, Baba Y, Matsumura K, Wasada H, Murata J, Agawa M, Itakura S, Enoki A (2007) Characterization of a hydroxyl-radical-producing glycoprotein and its presumptive genes from the white-rot basidiomycete Phanerochaete chrysosporium. J Biotechnol 128:500–511Google Scholar
  148. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26Google Scholar
  149. Tuomela M, Vikman M, Hatakka A, Itävaara M (2000) Biodegradation of lignin in a compost environment: a review. Bioresour Technol 72:169–183Google Scholar
  150. Uzcategui E, Johansson G, Ek B, Pettersson G (1991a) The 1,4-β-glucan glucanohydrolases from Phanerochaete chrysosporium. Re-assessment of their significance in cellulose degradation mechanisms. J Biotechnol 21:143–159Google Scholar
  151. Uzcategui E, Ruiz A, Montesino R, Johansson G, Pettersson G (1991b) The 1,4-β-glucan cellobiohydrolases from Phanerochaete chrysosporium. I. A system of synergistically acting enzymes homologous to Trichoderma reesei. J Biotechnol 19:271–285Google Scholar
  152. Vanden Wymelenberg A, Minges P, Sabat G, Martinez D, Aerts A, Salamov A, Grigoriev I, Shapiro H, Putnam N, Belinky P, Dosoretz C, Gaskell J, Kersten P, Cullen D (2006) Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveal complex mixtures of secreted proteins. Fungal Genet Biol 43:343–356Google Scholar
  153. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285Google Scholar
  154. Vares T, Kalsi M, Hatakka A (1995) Lignin peroxidases, manganese peroxidases, and other ligninolytic enzymes produced by Phlebia radiata during solid-state fermentation of wheat straw. Appl Environ Microbiol 61:3515–3520Google Scholar
  155. Wang W, Gao PJ (2003) Function and mechanism of a low-molecular-weight peptide produced by Gloeophyllum trabeum in biodegradation of cellulose. J Biotechnol 101:119–130Google Scholar
  156. Wei DS, Houtman CJ, Kapich AN, Hunt CG, Cullen D, Hammel KE (2010) Laccase and its role in the production of extracellular reactive oxygen species during wood decay by the brown-rot basidiomycete Postia placenta. Appl Environ Microbiol. 76:2091–2097Google Scholar
  157. Widsten P, Kandelbauer A (2008) Laccase applications in the forest products industry: a review. Enzyme Microb Technol 42:293–307Google Scholar
  158. 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 62:834–841Google Scholar
  159. Yelle DJ, Ralph J, Lu FC, Hammel KE (2008) Evidence for cleavage of lignin by a brown-rot basidiomycete. Environ Microbiol 10:1844–1849Google Scholar
  160. Yoon JJ, Cha CJ, Kim YS, Kim W (2008) Degradation of cellulose by the major endoglucanase produced from the brown-rot fungus Fomitopsis pinicola. Biotechnol Lett 30:1373–1378Google Scholar

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© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Food and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.USDA Forest Products LaboratoryOne Gifford Pinchot DriveMadisonUSA

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