Oxidoreductases and cellulases in lichens: Possible roles in lichen biology and soil organic matter turnover

Fungal Biology

Volumn 117, Issue 6, 2013, Pages 431-438

  Beckett, Richard P ^a   Zavarzina, Anna G ^b   Liers, Christiane ^c  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c International Graduate School Zittau   (Germany)

Author keywords

Humic substances; Laccase; Peroxidase; Reactive oxygen species; Stress; Tyrosinases

Indexed keywords

CELLULASE; ORGANIC COMPOUND; OXIDOREDUCTASE;

BIOMASS; BIOTRANSFORMATION; CATALYSIS; CYANOBACTERIUM; DISTURBANCE; ENZYME ACTIVITY; FUNGUS; GREEN ALGA; LICHEN; SOIL ECOSYSTEM; SOIL ORGANIC MATTER; TUNDRA; TURNOVER;

ARTICLE; BIOTRANSFORMATION; CHEMISTRY; ENZYMOLOGY; ISOLATION AND PURIFICATION; LICHEN (ORGANISM); METABOLISM; MICROBIOLOGY; SOIL;

BIOTRANSFORMATION; CELLULASES; LICHENS; ORGANIC CHEMICALS; OXIDOREDUCTASES; SOIL; SOIL MICROBIOLOGY;

ANTARCTICA; ARCTIC;

ASCOMYCOTA; CHLOROPHYTA; FUNGI; PELTIGERALES;

EID: 84879784593     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2013.04.007     Document Type: Article

References (70)

1. Ahmadjian V. Lichens are more important than you think. Bioscience 1995, 45:123-124.
2. Armstrong R.A., Welch A.R. Competition in lichen communities. Symbiosis 2007, 43:1-12.
3. Baldrian P. Enzymes of saprotrophic basidiomycetes. British Mycological Society Symposia Series 2008, 28:19-41.
4. Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs?. Oecologia 2009, 161:657-660.
5. Baldrian P., Voříšková J., Dobiášová P., Merhautová V., Lisá L., Valášková V. Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant and Soil 2011, 338:111-125.
6. Beckett R.P., Kranner I., Minibayeva F.V. Stress physiology and the symbiosis. Lichen Biology 2008, 134-151. Cambridge University Press, Cambridge. 2nd edn. T.H. Nash (Ed.).
7. Beckett R.P., Minibayeva F.V., Laufer Z. Extracellular reactive oxygen species production by lichens. Lichenologist 2005, 37:397-407.
8. Beckett R.P., Minibayeva F.V., Liers C. Occurrence of high tyrosinase activity in the non-Peltigeralean lichen Dermatocarpon miniatum (L.) W. Mann. Lichenologist 2012, 44:827-832.
9. Beckett R.P., Minibayeva F.V., Liers C. On the occurrence peroxidase and laccase activity in lichens. Lichenologist 2013, 45:277-283.
10. Büdel B., Darienko T., Deutschewitz K., Dojani S., Friedl T., Mohr K.I., Salisch M., Reisser W., Weber B. Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microbial Ecology 2009, 57:229-247.
11. Chen J., Blume H.P., Beyer L. Weathering of rocks induced by lichen colonization - a review. Catena 2000, 39:121-146.
12. de los Ríos A., Ramírez R., Estévez P. Production of several isoforms of ß-1, 4-glucanase by the cyanolichen Peltigera canina. Physiologia Plantarum 1997, 100:159-164.
13. Durrens P. The phenoloxidases of the ascomycete Podospora anserina: the three forms of the major laccase activity. Archives of Microbiology 1981, 130:121-124.
14. Edens W.A., Goins T.Q., Dooley D., Henson J.M. Purification and characterization of a secreted laccase of Gaeumannomyces graminis var. tritici. Applied and Environmental Microbiology 1999, 65:3071-3074.
15. Elbert W., Weber B., Burrows S., Steinkamp J., Büdel B., Andreae M.O., Poschl U. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nature Geoscience 2012, 5:459-462.
16. Estevez M.P. The synthesis of plant cell wall polysaccharide degrading enzymes by lichens. Surface Physiology of Lichens 1985, 115-126. Universidad Complutense de Madrid, Madrid. C. Vicente, D.H. Brown, M.E. Legaz (Eds.).
17. Gauslaa Y., Solhaug K.A. Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 2001, 126:462-471.
18. Ghosh D., Mukherjee R. 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. Inorganic Chemistry 1998, 37:6597-6605.
19. Gómez-Toribio V., García-Martín A.B., Martínez M.J., Martínez Á.T., Guillén F. Enhancing the production of hydroxyl radicals by Pleurotus eryngii via quinone redox cycling for pollutant removal. Applied and Environmental Microbiology 2009, 75:3954-3962.
20. Gómez-Toribio V., García-Martín A.B., Martínez M.J., Martínez Á.T., Guillén F. Induction of extracellular hydroxyl radical production by white-rot fungi through quinone redox cycling. Applied and Environmental Microbiology 2009, 75:3944-3953.
21. Goodell B. Brown-rot fungal degradation of wood: our evolving view. Wood Deterioration and Preservation 2003, 845:97-118.
22. Grinhut T., Hadar Y., Chen Y. Degradation and transformation of humic substances by saprotrophic fungi: processes and mechanisms. Fungal Biology Reviews 2007, 21:179-189.
23. Guillen F., Munoz C., Gomez-Toribio V., Martinez A.T., Martinez M.J. Oxygen activation during oxidation of methoxyhydroquinones by laccase from Pleurotus eryngii. Applied and Environmental Microbiology 2000, 66:170-175.
24. Halaouli S., Asther M., Sigoillot J.C., Hamdi M., Lomascolo A. Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. Journal of Applied Microbiology 2006, 100:219-232.
25. Hatakka A., Lundell T.K., Tervilä-Wilo A.L.M., Brunow G. Metabolism of non-phenolic β-O-4 lignin model compounds by the white-rot fungus Phlebia radiata. Applied Microbiology and Biotechnology 1991, 36:270-277.
26. Hoegger P.J., Kilaru S., James T.Y., Thacker J.R., Kues U. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS Journal 2006, 273:2308-2326.
27. Hofrichter M., Ullrich R., Pecyna M.J., Liers C., Lundell T. New and classic families of secreted fungal heme peroxidases. Applied Microbiology and Biotechnology 2010, 87:871-897.
28. Huneck S., Yoshimura I. Identification of Lichen Substances 1996, Springer-Verlag, Berlin.
29. Kranner I., Zorn M., Turk B., Wornik S., Beckett R.P., Batic F. Biochemical traits of lichens differing in relative desiccation tolerance. New Phytologist 2003, 160:167-176.
30. Laufer Z., Beckett R.P., Minibayeva F.V. Co-occurrence of the multicopper oxidases tyrosinase and laccase in lichens in sub-order Peltigerineae. Annals of Botany 2006, 98:1035-1042.
31. Laufer Z., Beckett R.P., Minibayeva F.V., Lüthje S., Böttger M. Occurrence of laccases in lichenized ascomycetes of the Peltigerineae. Mycological Research 2006, 110:846-853.
32. Laufer Z., Beckett R.P., Minibayeva F.V., Lüthje S., Böttger M. Diversity of laccases from lichens in suborder Peltigerineae. Bryologist 2009, 112:418-426.
33. Leontievsky A.A., Myasoedova N.M., Pozdnyakova N.N., Golovleva L.A. "Yellow" laccase of Panus tigrinus oxidizes non-phenolic substrates without electron-transfer mediators. FEBS Letters 1997, 413:446-448.
34. Leontievsky A.A., Myasoedova N.M., Baskunov B.P., Pozdnyakova N.N., Vares T., Kalkkinen N. Reactions of blue and yellow fungal laccases with lignin model compounds. Biochemistry Moscow 1999, 64:1150-1156.
35. Liers C., Bobeth C., Pecyna M., Ullrich R., Hofrichter M. DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Applied Microbiology and Biotechnology 2010, 85:1869-1879.
36. Liers C., Ullrich R., Hofrichter M., Minibayeva F.V., Beckett R.P. Oxidoreductases from lichenized ascomycetes: purification and characterization of a heme-peroxidase from Leptogium saturninum that oxidizes high-redox potential substrates. Fungal Genetics and Biology 2011, 48:1139-1145.
37. Liers C., Ullrich R., Steffen K.T., Hatakka A., Hofrichter M. Mineralization of C-14-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Applied Microbiology and Biotechnology 2006, 69:573-579.
38. Lisov A.V., Zavarzina A.G., Zavarzin A.A., Leontievsky A.A. Laccases produced by lichens of the order Peltigerales. FEMS Microbiology Letters 2007, 275:46-52.
39. Lisov A.V., Zavarzina A.G., Zavarzin A.A., Demin V.V., Leontievsky A.A. Dimeric and monomeric laccases of soil-stabilizing lichen Solorina crocea: purification, properties and reactions with humic acids. Soil Biology and Biochemistry 2012, 45:161-167.
40. Martinez D., Challacombe J., Morgenstern I., Hibbett D., Schmoll M., Kubicek C.P., Ferreira P., Ruiz-Duenas F.J., Martinez A.T., Kersten P., Hammel K.E., Wymelenberg A.V., Gaskell J., Lindquist E., Sabat G., BonDurant S.S., Larrondo L.F., Canessa P., Vicuna R., Yadav J., Doddapaneni H., Subramanian V., Pisabarro A.G., Lavin J.L., Oguiza J.A., Master E., Henrissat B., Coutinho P.M., Harris P., Magnuson J.K., Baker S.E., Bruno K., Kenealy W., Hoegger P.J., Kues U., Ramaiya P., Lucash S., Salamov A., Shapiro H., Tu H., Chee C.L., Misra M., Xie G., Teter S., Yaver D., James T., Mokrejs M., Pospisek M., Grigoriev I.V., Brettin T., Rokhsar D., Berka R., Cullen D. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:1954-1959.
41. Marusek C.M., Trobaugh N.M., Flurkey W.H., Inlow J.K. Comparative analysis of polyphenol oxidase from plant and fungal species. Journal of Inorganic Biochemistry 2006, 100:108-123.
42. Mayer A.M. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 2006, 67:2318-2331.
43. Mika A., Minibayeva F.V., Beckett R.P., Lüthje S. Possible functions of extracellular peroxidases in stress-induced generation and detoxification of active oxygen species. Phytochemistry Reviews 2004, 3:173-193.
44. Molnár K., Farkas E. Current results on biological activities of lichen secondary metabolites, a review. Zeitschrift Fur Naturforschung Section C 2010, 65:157-173.
45. Morgenstern I., Klopman S., Hibbett D.S. Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. Journal of Molecular Evolution 2008, 66:243-257.
46. Palmqvist K. Carbon economy in lichens. New Phytologist 2000, 148:11-36.
47. Plat H., Krenn B.E., Wever R. The bromoperoxidase from the lichen Xanthoria parietina is a novel vanadium enzyme. Biochemical Journal 1987, 248:277-279.
48. Rabinovich M.L., Melnik M.S., Bolobova A.V. The structure and mechanism of action of cellulolytic enzymes. Biochemistry Moscow 2002, 68:850-871.
49. Rast D.M., Baumgartner D., Mayer C., Hollenstein G.O. Cell wall-associated enzymes in fungi. Phytochemistry 2003, 64:339-366.
50. Ratcliffe B., Flurkey W.H., Kuglin J., Dawley R. Tyrosinase, laccase, and peroxidase in mushrooms Agaricus, Crimini, Oyster and Shilitake. Journal of Food Science 1994, 59:824-827.
51. Scheu S., Simmerling F. Growth and reproduction of fungal feeding Collembola as affected by fungal species melanin and mixed diets. Oecologia 2004, 139:347-353.
52. Selinheimo E., Nieidhin D., Steffensen C., Nielsen J., Lomascolo A., Halaouli S., Record E., O'Beirne D., Buchert J., Kruus K. Comparison of the characteristics of fungal and plant tyrosinases. Journal Biotechnology 2007, 130:471-480.
53. Solomon E.I., Chen P., Metz M., Lee S.K., Palmer A.E. Oxygen binding, activation, and reduction to water by copper proteins. Angewandte Chemie - International Edition 2001, 40:4570-4590.
54. Stevenson F.J. Humus Chemistry: genesis, composition, reactions 1994, Wiley, New York. 2nd edn.
55. Talbot J.M., Allison S.D., Treseder K.K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology 2008, 22:955-963.
56. Thurston C.F. The structure and function of fungal laccases. Microbiology 1994, 140:19-26.
57. Tolpysheva T.Y. Dependence on substrate of cellulosolytic activity in the lichen Hypogymnia physodes L. Nyl. Vestnik Moskovskogo Universiteta 2007, 16:19-22.
58. van Gelder C.W., Flurkey W.H., Wichers H.J. Sequence and structural features of plant and fungal tyrosinases. Phytochemistry 1997, 45:1309-1323.
59. Welinder K.G. Superfamily of plant, fungal and bacterial peroxidases. Current Opinion in Structural Biology 1992, 2:388-393.
60. Yagüe E., Estévez M.P. Purification and characterization of ß-1,4-glucanase from Evernia prunastri. European Journal of Biochemistry 1988, 175:627-632.
61. Yagüe E., Estévez M.P. Regulation of ß-1,4-glucanase and ß-glucosidase production by glucose in Evernia prunastri. Journal of Plant Physiology 1988, 133:539-544.
62. Yagüe E., Estévez M.P. Cellobiose induces extracellular ß-1,4-glucanase and ß-glucosidase in the epiphytic lichen Evernia prunastri. Plant Physiology and Biochemistry 1990, 28:203-207.
63. Yagüe E., Estéveza M.P. β-1,4-Glucanase cellulase location in the symbionts of Evernia prunastri. Lichenologist 1989, 21:147-151.
64. Yagüe E., Orus M.I., Estévez M.P. Extracellular polysaccharides synthesized by the epiphytic lichen Evernia prunastri. Planta 1984, 160:212-216.
65. Zagoskina N.V., Nikolaeva T.N., Lapshin P.V., Zavarzina A.G., Zavarzin A.A. On the content of phenolic compounds in different lichen species of the Kola Peninsula. Chemistry of Raw Plant Material 2011, 4:245-249.
66. Zagoskina N.V., Nikolaeva T.N., Lapshin P.V., Zavarzin A.A., Zavarzina A.G., Water-soluble phenolic compounds in lichens. Microbiology (Moscow), 2013, 82/3, in press.
67. Zavarzina A.G. Heterophase synthesis of humic acids in soils by immobilized phenol oxidases. Soil Enzymology 2011, 207-228. Springer Verlag, Berlin. G. Shukla, A. Varma (Eds.).
68. Zavarzina AG, Lisov AV, 2012. Adsorption of lichen laccases on hydroxyaluminum-kaolinite: properties of immobilized enzymes and their role in synthesis of humic acids. Proceedings of the 4th International Congress Eurosoil-2012, Bari, Italy, 2-6 July, 2012. p. 2291.
69. Zavarzina A.G., Lisov A.A., Zavarzin A.A., Leontievsky A.A. Fungal oxidoreductases and humification in forest soils. Soil Enzymology 2011, 187-205. Springer Verlag, Berlin. G. Shukla, A. Varma (Eds.).
70. Zavarzina A.G., Zavarzin A.A. Laccase and tyrosinase activities in lichens. Microbiology 2006, 75:546-556.