Fungal Oxidoreductases and Humification in Forest Soils

  • A. G. ZavarzinaEmail author
  • A. A. Lisov
  • A. A. Zavarzin
  • A. A. Leontievsky
Part of the Soil Biology book series (SOILBIOL, volume 22)


Humification is aerobic, largely oxidative process of non-living organic matter biotransformation into recalcitrant humic substances (HS). HS comprise up to 90% of soil organic matter and represent a long-time sink for atmospheric CO2 with mean residence time of 102–103 years. Wood- and soil-colonizing fungi are the major driving force in humification, being involved in transformation of plant residues, synthesis, and degradation of HS. The chapter is focused on production of ligninolytic oxidoreductases by different groups of fungi and their role in humus synthesis and transformation in forest soils. White-rot fungi and litter-decomposing basidiomycetes producing acidic laccases and ligninolytic peroxidases are mainly involved in delignification and HS degradation, leading to release of small soluble fragments (fulvic acids, monomers) and CO2. Brown-rot fungi producing non-enzymatic oxidative agents and probably laccase are responsible for synthesis of high molecular weight humic acids from partially oxidized lignin. Ascomycetes produce non-ligninolytic peroxidases, neutral laccases, and tyrosinases and are mainly involved in synthesis of HS by partial lignin oxidation or extracellular polymerization of low molecular weight polyphenols. Laccases of ectomycorrhizae and lichens may participate in humus formation via polymerization of phenols, while tyrosinases may contribute to humic acid fraction via melanization.


Humic Substance Humic Acid Laccase Activity Phenol Oxidase Versatile Peroxidase 
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.



Financial support from the Russian Foundation for Fundamental Research (grant 09-04-00570) and from the Programme No.15 of the Presidium of Russian Academy of Sciences “Origin of the Biosphere and Evolution of Geobiological systems” is gratefully acknowledged. We are expressing our sincere thanks to Prof. Richard P. Beckett for long lasting cooperation, his valuable comments and revising the language of the manuscript.


  1. Alexandrova LN (1980) Soil organic matter and processes of its transformation. Nauka, Leningrad (in Russian)Google Scholar
  2. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochem 81:361–373CrossRefGoogle Scholar
  3. Almendros G, Dorado J (1999) Molecular characteristics related to the biodegradability of humic acid preparations. Eur J Soil Sci 50:227–236CrossRefGoogle Scholar
  4. Baldrian P (2006) Fungal laccases: occurrence and properties. FEMS Microbiol Rev 30:215–242PubMedCrossRefGoogle Scholar
  5. Batjes NH (1996) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 47:151–163CrossRefGoogle Scholar
  6. Beckett RP, Kranner I, Minibaeva F (2008) Stress physiology and the symbiosis. In: Nash TH (ed) Lichen Biology, 2nd edn, Cambridge Univ Press, Cambridge, pp 134–151Google Scholar
  7. Bending GD, Read DJ (1996a) Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1595–1602Google Scholar
  8. Bending GD, Read DJ (1996b) Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1603–1612CrossRefGoogle Scholar
  9. Bending GD, Read DJ (1997) Lignin and soluble-phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol Res 101:1348–1354CrossRefGoogle Scholar
  10. Burke RM, Cairney JWG (2002) Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 12:105–116PubMedCrossRefGoogle Scholar
  11. Cairney JWG, Burke RM (1994) Fungal enzymes degrading plant cell walls: their possible significance in the ectomycorrhizal symbiosis. Mycol Res 98:1345–1356CrossRefGoogle Scholar
  12. Cairney JWG, Burke RM (1998) Do ecto- and ericoid mycorrhizal fungi produce peroxidase activity? Mycorrhiza 8:61–65CrossRefGoogle Scholar
  13. Cairney JWG, Taylor AFS, Burke RM (2003) No evidence for lignin peroxidase genes in ectomycorrhizal fungi. New Phytol 160:461–462Google Scholar
  14. Camarero S, Sarcar S, Ruiz-Duenas FJ, Martinez MJ, Martinez AT (1999) Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction site. J Biol Chem 274:10324–10330PubMedCrossRefGoogle Scholar
  15. Chambers SM, Burke RM, Brooks PR, Cairney JWG (1999) Molecular and biochemical evidence for manganese-dependent peroxidase activity in Tylospora fibrillosa. Mycol Res 103:1098–1102CrossRefGoogle Scholar
  16. Chen DM, Bastias BA, Taylor AFS, Cairney JWG (2003) Identification of laccase-like genes in ectomycorrhizal basidiomycetes and transcriptional regulation by nitrogen in Piloderma byssinum. New Phytol 157:547–554CrossRefGoogle Scholar
  17. Chen J, Blume HP, Beyer L (2000) Weathering of rocks induced by lichen colonization – a review. Catena 39:121–146CrossRefGoogle Scholar
  18. Dahlman L, Person J, Palmqvist K, Nashholm T (2004) Organic and inorganic nitrogen uptake in lichens. Plants 219:459–467Google Scholar
  19. Dey S, Maiti TK, Bhattacharyya BC (1991) Lignin peroxidase production by a brown rot fungus Polyporus ostreiformis. J Ferment Bioeng 72:402–404CrossRefGoogle Scholar
  20. Duran N, Ferrer I, Rodriguez J (1987) Ligninases from Chrysonilia sitophila (TFB-27441). Appl Microbiol Biotechnol 16:157–167Google Scholar
  21. Eggert C, Temp U, Eriksson KEL (1996) Lignin degradation by a fungus lacking lignin and Mn peroxidase. In: Jeffries T, Vikarii L (eds) Enzymes in the pulp and paper manufacturing. ACS Symp Ser 655: 130–150Google Scholar
  22. Fakoussa RM, Frost PJ (1999) In vivo-decolorization of coal-derived humic acids by laccase-excreting fungus Trametes versicolor. Appl Microbiol Biotechnol 52:60–65CrossRefGoogle Scholar
  23. Fakoussa RM, Hofrichter M (1999) Biotechnology and microbiology of coal degradation. Appl Microbiol Biotechnol 52:25–40PubMedCrossRefGoogle Scholar
  24. Flaig W (1966) The chemistry of humic substances. In: The use of isotopes in soil organic matter studies, Report of FAO/IAEA technical meeting. Pergamon, New York, pp 103–127Google Scholar
  25. Galliano H, Gas G, Seris JL, Boudet AM (1991) Lignin degradation by Rigidoporus lignosus involves synergistic action of two oxidizing enzymes: Mn-peroxidase and laccase. Enzym Microb Technol 13:478–482CrossRefGoogle Scholar
  26. Ghosh D, Mukherjee R (1998) Modeling tyrosinase monooxygenase activity. Spectroscopic and magnetic investigations of products due to reactions between copper(I) complexes of xylyl-based dinucleating ligands and dioxygen: aromatic ring hydroxylation and irreversible oxidation products. Inorg Chem 37:6597–6605PubMedCrossRefGoogle Scholar
  27. Glazovskaya MA (1996) Role and functions of the pedosphere in geochemical carbon cycles. Pochvovedenije 2:174–186 (in Russian)Google Scholar
  28. Goodell B (2003) Brown-rot fungal degradation of wood: our evolving view. ACS Symp Ser 845:97–118CrossRefGoogle Scholar
  29. Gramss G, Ziegenhagen D, Sorge S (1999) Degradation of soil humic extract by wood- and soil-associated fungi, bacteria, and commercial enzymes. Microb Ecol 137:140–151CrossRefGoogle Scholar
  30. Grinhut T, Hadar Y, Chen Y (2007) Degradation and transformation of humic substances by saprotrophic fungi: processes and mechanisms. Fungal Biol Rev 21:179–189CrossRefGoogle Scholar
  31. Guillén F, Muñoz C, Gómez-Toribio V, Martínez AT, Jesús Martínez M (2000) Oxygen activation during oxidation of methoxyhydroquinones by laccase from Pleurotus eryngii. Appl Environ Microbiol 66:170–175Google Scholar
  32. Haider K, Trojanowski J (1975) Decomposition of specifically 14C-labelled phenols and dehydropolymers of coniferyl alcohol as models for lignin degradation by soft and white rot fungi. Arch Microbiol 105:33–41CrossRefGoogle Scholar
  33. Hammel KE, Kapich AN, Jensen KA, Ryan AC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453CrossRefGoogle Scholar
  34. Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355PubMedCrossRefGoogle Scholar
  35. Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol Rev 13:125–135CrossRefGoogle Scholar
  36. Heinfling A, Ruiz-Duenas FJ, Martinez MJ, Bergbauer M, Szewzyk U, Martinez AT (1998) A study on reducing substrates of manganese-oxidising peroxidases from Pleurotus eryngii and Bjerkandera adusta. FEBS Lett 428:141–416PubMedCrossRefGoogle Scholar
  37. Heinzkill M, Bech L, Halkier T, Schneider P, Anke T (1998) Characterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae). Appl Environ Microbiol 64:1601–1606PubMedGoogle Scholar
  38. Hobbie EA, Horton TR (2007) Evidence that saprotrophic fungi mobilize carbon and mycorrhizal fungi mobilize nitrogen during litter decomposition. New Phytol 173:447–449Google Scholar
  39. Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466CrossRefGoogle Scholar
  40. Holker U, Ludwig S, Scheel T, Hofer M (1999) Mechanisms of coal solubilization by the dueteromycetes Trichoderma atroviride and Fusarium oxysporum. Appl Microbiol Biotechnol 52:57–59PubMedCrossRefGoogle Scholar
  41. Kang KS, Felbeck GT (1965) A comparison of the alkaline extract of tissues of Aspergillus niger with humic acids from three soils. Soil Sci 99:175–181CrossRefGoogle Scholar
  42. Kanunfre CC, Zancan GT (1998) Physiology of exolaccase production by Thelephora terrestris. FEMS Microbiol Lett 161:151–156CrossRefGoogle Scholar
  43. Kelleher BP, Simpson AJ (2006) Humic substances in soils: are they really chemically distinct? Environ Sci Technol 40:4605–4611PubMedCrossRefGoogle Scholar
  44. Kirk TK (1975) Effects of a brown-rot fungus Lenzites trabea on lignin in spruce wood. Holzforschung 29:99–107CrossRefGoogle Scholar
  45. Kluczek-Turpeinen B, Steffen KT, Tuomela M, Hatakka A, Hofrichter M (2005) Modification of humic acids by the compost-dwelling deuteromycete Paecilomyces inflatus. Appl Microbiol Biotechnol 66:443–449PubMedCrossRefGoogle Scholar
  46. Kluczek-Turpeinen B, Tuomela M, Hatakka A, Hofrichter M (2003) Lignin degradation in a compost environment by the deuteromycete Paecilomyces inflatus. Appl Microbiol Biotechnol 61:374–379PubMedGoogle Scholar
  47. Kluczek-Turpeinen B, Maijala P, Hofrichter M, Hatakka A (2007) Degradation and enzymatic activities of three Paecilomyces inflatus strains grown on diverse lignocellulosic substrates. Intern Biodeterior Biodegrad 59:283–291CrossRefGoogle Scholar
  48. Kononova MM (1966) Soil organic matter. Pergamon, OxfordGoogle Scholar
  49. Koroleva-Skorobogat’ko O, Stepanova E, Gavrilova V et al (1998) Purification and characterization of the constitutive form of laccases from the basidiomycete Coriolus hirsutus and effect of inducers on laccase synthesis. J Biotechnol Appl Biochem 28:47–54Google Scholar
  50. Koukol O, Gryndler M, Novak F, Vosatka M (2004) Effect of Chalara longipes on decomposition of humic acids from Picea abies needle litter. Folia Microbiol 49:574–578CrossRefGoogle Scholar
  51. Kranner I, Beckett R, Hochman A, Nash TH (2008) Dessication-tolerance in lichens: a review. The Bryol 111:576–593CrossRefGoogle Scholar
  52. Laborda F, Monistrol IF, Luna N, Fernandez M (1999) Processes of liquefaction/solubilization of Spanish coals by microorganisms. Appl Microbiol Biotechnol 52:49–56PubMedCrossRefGoogle Scholar
  53. Laufer Z, Beckett RP, Minibayeva FV, Luthje S, Bottger M (2006a) Occurrence of laccases in lichenized Ascomycetes in the suborder Peltigerineae. Myc Res 110:846–853CrossRefGoogle Scholar
  54. Laufer Z, Beckett RP, Minibayeva FV (2006b) Co-occurrence of the multicopper oxidases tyrosinase and laccase in lichens in sub-order Peltigerineae. Ann Bot 98:1035–1042PubMedCrossRefGoogle Scholar
  55. Laufer Z, Beckett RP, Minibaeva FV, Luthje S, Bottger M (2009) Diversity of laccases from lichens in suborder Peltigerineae. The Bryol 112:418–426CrossRefGoogle Scholar
  56. 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 50:281–284CrossRefGoogle Scholar
  57. Leonowicz A, Matuszewska A, Luterek J et al (1999) Biodegradation of lignin by white-rot fungi. Fungal Genet Biol 27:175–185PubMedCrossRefGoogle Scholar
  58. Leontievsky AA, Vares T, Lankinen P, Shergill JK, Pozdnyakova NN, Myasoedova NM, Kalkkinen N, Golovleva LA, Cammack R, Thurston CF, Hatakka A (1997a) Blue and yellow laccases of ligninolytic fungi. FEMS Microbiol Lett 156:9–14PubMedCrossRefGoogle Scholar
  59. Leontievsky AA, Myasoedova N, Pozdnyakova N, Golovleva L (1997b) “Yellow” laccase of Panus tigrinus oxidizes non-phenolic substrates without electron-transfer mediators. FEBS Lett 413:446–448PubMedCrossRefGoogle Scholar
  60. Leontievsky AA, Myasoedova NM, Baskunov BP, Pozdnyakova NN, Vares T, Kalkkinen N et al (1999) Reactions of blue and yellow fungal laccases with lignin model compounds. Biochemistry (Moscow) 64:1150–1156Google Scholar
  61. Liers C, Ulrich 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 69:573–579PubMedCrossRefGoogle Scholar
  62. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620Google Scholar
  63. Lisov AV, Leontievsky AA, Golovleva LA (2003) Hybrid Mn-peroxidase from the ligninolytic fungus Panus tigrinus 8/18. Isolation, substrate specificity, and catalytic cycle. Biochemistry (Moscow) 68:1027–1035CrossRefGoogle Scholar
  64. Lisov AV, Zavarzina AG, Zavarzin AA, Leontievsky AA (2007) Laccases produced by lichens of the order Peltigerales. FEMS Microbiol Lett 275:46–52PubMedCrossRefGoogle Scholar
  65. 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 50:570–579PubMedCrossRefGoogle Scholar
  66. Makino N, McMahill PHS, Masonthe HS (1974) The oxidation state of copper in resting tyrosinase. J Biol Chem 249:6062–6066PubMedGoogle Scholar
  67. Martin JP, Haider K (1971) Microbial activity in relation to soil humus formation. Soil Sci 111:54–63CrossRefGoogle Scholar
  68. Martin JP, Haider K (1969) Phenolic polymers of Stachybotris atra, Stachybotris chartarum and Epicoccum nigrum in relation to humic acid formation. Soil Sci 107:260–270CrossRefGoogle Scholar
  69. Maltseva OV, Niku-Paavola ML, Leontievsky AA, Myasoedova NM, Golovleva LA (1991) Ligninolytic enzymes of the white rot fungus Panus tigrinus. Biotechnol Appl Biochem 13:291–302Google Scholar
  70. Mester T, Field JA (1998) Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjercandera species strain BOS55 in the absence of manganese. J Biol Chem 273: 15412–15417Google Scholar
  71. Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56CrossRefGoogle Scholar
  72. Mirchink TG (1976) Soil mycology. Moscow State University Press, MoscowGoogle Scholar
  73. Morgenstern I, Klopman S, Hibbett D (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. J Mol Evol 66:243–257Google Scholar
  74. Nakayama T, Amachi T (1999) Fungal peroxidase: its structure, function, and application. J Mol Catal B – Enzyme 6:185–198CrossRefGoogle Scholar
  75. Ng TB, Wang HX (2004) A homodimeric laccase with unique characteristics from the yellow mushroom Cantharellus cibarius. Biochem Biophys Res Commun 313:37–41PubMedCrossRefGoogle Scholar
  76. Orlov DS (1990) Humus acids and the general theory of humification. MSU Press, Moscow (in Russian)Google Scholar
  77. Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974CrossRefGoogle Scholar
  78. Perez-Boada M, Ruiz-Duenas FJ, Pogni R, Basosi R, Choinowski T, Martinez MJ, Piontek K, Martinez 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 354:385–402PubMedCrossRefGoogle Scholar
  79. Rabinovich ML, Bolobova AV, Kondrashchenko VI (2001) Theoretical basis of the biotechnology of wood composites. Wood and wood-decaying fungi, vol 1. Nauka, Moscow (in Russian)Google Scholar
  80. Rabinovich ML, Bolobova AV, Vasilchenko LG (2004) Fungal decomposition of natural aromatic structures and xenobiotics: a review. Appl Biochem Microbiol 40:1–17CrossRefGoogle Scholar
  81. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol 157:475–492Google Scholar
  82. Řezáčová V, Hršelová H, Gryndlerová H, Mikšík I, Gryndler M (2006) Modifications of degradation-resistant soil organic matter by soil saprobic microfungi. Soil Biol Biochem 38:2292–2299CrossRefGoogle Scholar
  83. Rodriguez J, Ferraz A, Nogueira RF, Ferrer I, Esposito E, Duran N (1997) Lignin biodegradation by the ascomycete Chrisonilia sitophila. Appl Biochem Biotechnol 62:233–242PubMedCrossRefGoogle Scholar
  84. Rosenbrock P, Buscot F, Munch JC (1995) Fungal succession and changes in the fungal degradation potential during the initial stage of litter decomposition in a black alder forest (Alnus glutinosa (L.) Gaertn.). Eur J Soil Biol 31:1–11Google Scholar
  85. Rypaсek V, Rypackova M (1975) Brown rot of wood as a model for studies of lignocellulose humification. Biol Plantarum (Praha) 17:452–457CrossRefGoogle Scholar
  86. Sanchez-Ferrer A, Rodriguez-Lopez JN, Garcia-Canovas F, Garcia-Carmona F (1995) Tyrosinase: a comprehensive review of its mechanism. Biochim Biophys Acta 1247:1–11PubMedCrossRefGoogle Scholar
  87. Saparrat MCN, Martinez MJ, Tournier HA, Cabello MN, Arambarri AM (2000) Production of ligninolytic enzymes by Fusarium solani strains isolated from different substrata. World J Microbiol Biotechnol 16:799–803CrossRefGoogle Scholar
  88. 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 68:3514–3521PubMedCrossRefGoogle Scholar
  89. Schwarze FWMR (2007) Wood decay under the microscope. Fungal Biol Rev 21:133–170CrossRefGoogle Scholar
  90. Selinheimo E, Nieidhin D, Steffensen C, Nielsen J, Lomascolo A, Halaouli S, Record E, O’Beirne D, Buchert J, Kruus K (2007) Comparison of the characteristics of fungal and plant tyrosinases. J Biotechnol 130:471–480PubMedCrossRefGoogle Scholar
  91. Shin KS, Oh IK, Kim CJ (1997) Production and purification of Remazol brilliant blue R decolorizing peroxidase from the culture filtrate of Pleurotus ostreatus. Appl Environ Microbiol 63:1744–1748Google Scholar
  92. Silva-Stenico ME, Vengadajellum CJ, Janjua HA, Harrison STL, Burton SG, Cowan DA (2007) Degradation of low rank coal by Trichoderma atroviride ES11. J Ind Microbiol Biotechnol 34:625–631PubMedCrossRefGoogle Scholar
  93. Sklarz G, Antibus RK, Sinsabaugh RL, Linkins AE (1989) Production of phenol oxidases and peroxidases by wood-rotting fungi. Mycologia 81:234–240Google Scholar
  94. Snajdr J, Valaskova V, Merhautova V, Herinkova J, Cajthaml T, Baldrian P (2008) Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem 40:2068–2075CrossRefGoogle Scholar
  95. Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:563–2605CrossRefGoogle Scholar
  96. Steffen KT, Cajthaml T, Snajdr A, Baldrian P (2007) Differential degradation of oak (Quercus petraea) leaf litter by litter-decomposing basidiomycetes. Res Microbiol 158:447–455PubMedCrossRefGoogle Scholar
  97. Steffen KT, Hatakka A, Hofrichter M (2002) Degradation of humic acids by the litter-decomposing basidiomycete Collybia dryophila. Appl Environ Microbiol 68:3442–3448PubMedCrossRefGoogle Scholar
  98. Steffen KT, Hofrichter M, Hatakka A (2000) Mineralization of 14C-labelled synthetic lignin and ligninolytic enzyme activities of litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 54:819–825PubMedCrossRefGoogle Scholar
  99. Stepanova EV, Koroleva OV, Vasilchenko LG, Karapetyan KN, Landesman EO, Yavmetdinov IS, Kozlov YP, Rabinovich ML (2003) Fungal decomposition of oat straw during liquid and solid-state fermentation. Appl Biochem Microbiol (Moscow) 39:65–74CrossRefGoogle Scholar
  100. Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd edn. Wiley, New YorkGoogle Scholar
  101. Stolbovoi V (2006) Soil carbon in the forests of Russia. Mitig Adap Strat Gl Change 11:203–222CrossRefGoogle Scholar
  102. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963Google Scholar
  103. Temp U, Meyrahn H, Eggert C (1999) Extracellular phenol oxidase patterns during depolymerization of low-rank coal by three basidiomycetes. Biotechnol Lett 21:281–287CrossRefGoogle Scholar
  104. Tien M, Kirk TK (1983) Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science 221:661–663PubMedCrossRefGoogle Scholar
  105. Thurston C (1994) The structure and function of fungal laccases. Microbiol 140:19–26CrossRefGoogle Scholar
  106. Valaskova V, Snajdr J, Bittner B, Cajthaml T, Merhautova V, Hofrichter M, Baldrian P (2007) Production of lignocellulose-degrading enzymes and degradation of leaf litter by saprotrophic basidiomycetes isolated from a Quercus petraea forest. Soil Biol Biochem 39:651–660Google Scholar
  107. Valmaseda M, Martinez AT, Almendros D (1989) Contribution by pigmented fungi to P-type humic acid formation in two forest soils. Soil Biol Biochem 21:23–28CrossRefGoogle Scholar
  108. Vares T, Lundell TK, Hatakka AI (1992) Novel heme-containing enzyme possibly involved in lignin degradation by the white-rot fungus Junghuhnia separabilima. FEMS Microbiol Lett 99:53–58CrossRefGoogle Scholar
  109. Waksman SA (1931) Humus. Williams and Wilkins, BaltimoreGoogle Scholar
  110. Welinder KG (1992) Superfamily of plant, fungal and bacterial peroxidases. Curr Opin Struct Biol 2:388–393CrossRefGoogle Scholar
  111. Wong DWS (2008) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol. doi: Google Scholar
  112. Yanagi Y, Tamaki H, Otsuka H, Fujitake N (2002) Comparison of decolorization by microorganisms of humic acids with different 13C NMR properties. Soil Biol Biochem 34:729–731CrossRefGoogle Scholar
  113. Yang JS, Yuan HL, Wang HX, Chen WX (2005) Purification and characterization of lignin peroxidases from Penicillium decumbens P6. World J Microbiol Biotechnol 21:435–440CrossRefGoogle Scholar
  114. Yaropolov AI, Skorobogat’ko OV, Vartanov SS, Varfolomeyev SD (1994) Laccase. Properties, catalytic mechanism, and applicability. Appl Biochem Biotechnol 49:257–280CrossRefGoogle Scholar
  115. Yavmetdinov IS, Stepanova EV, Gavrilova VP, Lokshin BV, Perminova IV, Koroleva OV (2003) Isolation and characterization of humin-like substances produced by wood-degrading white-rot fungi. Appl Biochem Microbiol (Moscow) 39:257–264CrossRefGoogle Scholar
  116. Zaprometova KM, Mirchink TG, Orlov DS, Yukhnin AA (1971) Characteristics of black pigments of the dark-colored soil fungi. Soviet Soil Sci 7:22–30Google Scholar
  117. Zavarzina AG, Leontievsky AA, Golovleva LA, Trofimov SY (2004) Biotransformation of soil humic acids by blue laccase of Panus tigrinus 8/18: an in vitro study. Soil Biol Biochem 36:359–369CrossRefGoogle Scholar
  118. Zavarzina AG, Zavarzin AA (2006) Laccase and tyrosinase activities in lichens. Microbiol (Moscow) 75:546–556CrossRefGoogle Scholar
  119. Zavgorodnyaya YA, Demin VV, Kurakov AV (2002) Biochemical degradation of soil humic acids and fungal melanins. Org Geochem 33:347–355CrossRefGoogle Scholar
  120. Zviagintsev DG, Mirchink TG (1986) On the nature of soil humic acids. Soviet Soil Sci 5:68–75Google Scholar

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Authors and Affiliations

  • A. G. Zavarzina
    • 1
    Email author
  • A. A. Lisov
    • 2
  • A. A. Zavarzin
    • 3
  • A. A. Leontievsky
    • 2
  1. 1.Faculty of Soil ScienceMoscow State UniversityMoscowRussia
  2. 2.Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchinoRussia
  3. 3.Faculty of Biology and Soil SciencesSt. Petersburg State UniversitySt. PetersburgRussia

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