Applied Microbiology and Biotechnology

, Volume 93, Issue 4, pp 1395–1410 | Cite as

Fungal aryl-alcohol oxidase: a peroxide-producing flavoenzyme involved in lignin degradation

  • Aitor Hernández-Ortega
  • Patricia Ferreira
  • Angel T. MartínezEmail author


Aryl-alcohol oxidase (AAO) is an extracellular flavoprotein providing the H2O2 required by ligninolytic peroxidases for fungal degradation of lignin, the key step for carbon recycling in land ecosystems. O2 activation by Pleurotus eryngii AAO takes place during the redox-cycling of p-methoxylated benzylic metabolites secreted by the fungus. Only Pleurotus AAO sequences were available for years, but the number strongly increased recently due to sequencing of different basidiomycete genomes, and a comparison of 112 GMC (glucose–methanol–choline oxidase) superfamily sequences including 40 AAOs is presented. As shown by kinetic isotope effects, alcohol oxidation by AAO is produced by hydride transfer to the flavin, and hydroxyl proton transfer to a base. Moreover, site-directed mutagenesis studies showed that His502 activates the alcohol substrate by proton abstraction, and this result was extended to other GMC oxidoreductases where the nature of the base was under discussion. However, in contrast with that proposed for GMC oxidoreductases, the two transfers are not stepwise but concerted. Alcohol docking at the buried AAO active site resulted in only one catalytically relevant position for concerted transfer, with the pro-R α-hydrogen at distance for hydride abstraction. The expected hydride-transfer stereoselectivity was demonstrated, for the first time in a GMC oxidoreductase, by using the (R) and (S) enantiomers of α-deuterated p-methoxybenzyl alcohol. Other largely unexplained aspects of AAO catalysis (such as the unexpected specificity on substituted aldehydes) can also be explained in the light of the recent results. Finally, the biotechnological interest of AAO in flavor production is extended by its potential in production of chiral compounds taking advantage from the above-described stereoselectivity.


Aryl-alcohol oxidase Fungal enzymes GMC oxidoreductases Lignin biodegradation Reaction mechanism Stereoselectivity 



This work was supported by the Spanish projects BIO2008-01533 and BIO2011-26694, and by the PEROXICATS (KBBE-2010-4-265397) European project. The cited SAP (Saprotrophic Agaricomycotina project), C. subvermispora, and P. ostreatus JGI genome projects ( were coordinated by David Hibbett (Clark University, USA), Daniel Cullen (USDA Forest Products Laboratory, Madison, USA), and Gerardo Pisabarro (Universidad Pública de Navarra, Pamplona, Spain), respectively, and supported by the Office of Science of the U.S. Department of Energy. The authors thank Victor Guallar (Barcelona Supercomputing Center), Francisco Guillén (University of Alcalá), Ana Gutiérrez (IRNAS, CSIC, Seville), María Jesús Martínez (CIB, CSIC, Madrid), Milagros Medina (University of Zaragoza), Pedro Merino (University of Zaragoza), Antonio Romero (CIB, CSIC, Madrid), Elvira Romero (VirginiaTech, Blacksburg), Francisco J. Ruiz-Dueñas (CIB, CSIC, Madrid), Elisa Varela (CNIO, Madrid), and Willem J.H. van Berkel (Wageningen University) for their contributions to AAO studies. José M. Barrasa (University of Alcala) is acknowledged for microscopy of fungal colonization of wheat straw. A.H.-O. thanks a contract of the Comunidad de Madrid.


  1. Aguilar C, Urzúa U, Koenig C, Vicuña R (1999) Oxalate oxidase from Ceriporiopsis subvermispora: biochemical and cytochemical studies. Arch Biochem Biophys 366:275–282CrossRefGoogle Scholar
  2. Bannwarth M, Bastian S, Heckmann-Pohl D, Giffhorn F, Schulz GE (2004) Crystal structure of pyranose 2-oxidase from the white-rot fungus Peniophora sp. Biochemistry 43:11683–11690CrossRefGoogle Scholar
  3. Barrasa JM, Gutiérrez A, Escaso V, Guillén F, Martínez MJ, Martínez AT (1998) Electron and fluorescence microscopy of extracellular glucan and aryl-alcohol oxidase during wheat-straw degradation by Pleurotus eryngii. Appl Environ Microbiol 64:325–332Google Scholar
  4. Borrelli KW, Vitalis A, Alcantara R, Guallar V (2005) PELE: Protein energy landscape exploration. A novel Monte Carlo based technique. J Chem Theory Comput 1:1304–1311CrossRefGoogle Scholar
  5. Bourbonnais R, Paice MG (1988) Veratryl alcohol oxidases from the lignin degrading basidiomycete Pleurotus sajor-caju. Biochem J 255:445–450Google Scholar
  6. Bright HJ, Appleby M (1969) The pH dependence of the individual steps in the glucose oxidase reaction. J Biol Chem 244:3625–3634Google Scholar
  7. Camarero S, Böckle B, Martínez MJ, Martínez AT (1996) Manganese-mediated lignin degradation by Pleurotus pulmonarius. Appl Environ Microbiol 62:1070–1072Google Scholar
  8. Carey JS, Laffan D, Thomson C, Williams MT (2006) Analysis of the reactions used for the preparation of drug candidate molecules. Org Biomol Chem 4:2337–2347CrossRefGoogle Scholar
  9. Cavener DR (1992) GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol 223:811–814CrossRefGoogle Scholar
  10. Daniel G, Volc J, Kubátová E (1994) Pyranose oxidase, a major source of H2O2 during wood degradation by Phanerochaete chrysosporium, Trametes versicolor, and Oudemansiella mucida. Appl Environ Microbiol 60:2524–2532Google Scholar
  11. Daniel G, Volc J, Filonova L, Plihal O, Kubátová E, Halada P (2007) Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood. Appl Environ Microbiol 73:6241–6253CrossRefGoogle Scholar
  12. de Jong E, Cazemier AE, Field JA, de Bont JAM (1994a) Physiological role of chlorinated aryl alcohols biosynthesized de novo by the white rot fungus Bjerkandera sp strain BOS55. Appl Environ Microbiol 60:271–277Google Scholar
  13. de Jong E, Field JA, de Bont JAM (1994b) Aryl alcohols in the physiology of ligninolytic fungi. FEMS Microbiol Rev 13:153–188CrossRefGoogle Scholar
  14. Di Gioia D, Luziatelli F, Negroni A, Ficca AG, Fava F, Ruzzi M (2011) Metabolic engineering of Pseudomonas fluorescens for the production of vanillin from ferulic acid. J Biotechnol Online. doi: 10.1016/j.jbiotec.2011.08.014
  15. Dreveny I, Andryushkova AS, Glieder A, Gruber K, Kratky C (2009) Substrate binding in the FAD-dependent hydroxynitrile lyase from almond provides insight into the mechanism of cyanohydrin formation and explains the absence of dehydrogenation activity. Biochemistry 48:3370–3377CrossRefGoogle Scholar
  16. Dym O, Eisenberg D (2001) Sequence–structure analysis of FAD-containing proteins. Protein Sci 10:1712–1728CrossRefGoogle Scholar
  17. Eisses KT (1989) On the oxidation of aldehydes by alcohol-dehydrogenase of Drosophila melanogaster—evidence for the gem-diol as the reacting substrate. Bioorg Chem 17:268–274CrossRefGoogle Scholar
  18. Eriksson K-E, Pettersson B, Volc J, Musílek V (1986) Formation and partial characterization of glucose-2-oxidase, a H2O2 producing enzyme in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 23:257–262CrossRefGoogle Scholar
  19. Escalettes F, Turner NJ (2008) Directed evolution of galactose oxidase: generation of enantioselective secondary alcohol oxidases. ChemBioChem 9:857–860CrossRefGoogle Scholar
  20. Evans CS, Dutton MV, Guillén F, Veness RG (1994) Enzymes and small molecular mass agents involved with lignocellulose degradation. FEMS Microbiol Rev 13:235–240CrossRefGoogle Scholar
  21. Faison BD, Kirk TK (1983) Relationship between lignin degradation and production of reduced oxygen species by Phanerochaete chrysosporium. Appl Environ Microbiol 46:1140–1145Google Scholar
  22. Fan F, Gadda G (2005) On the catalytic mechanism of choline oxidase. J Am Chem Soc 127:2067–2074CrossRefGoogle Scholar
  23. Fan F, Germann MW, Gadda G (2006) Mechanistic studies of choline oxidase with betaine aldehyde and its isosteric analogue 3,3-dimethylbutyraldehyde. Biochemistry 45:1979–1986CrossRefGoogle Scholar
  24. Farmer VC, Henderson MEK, Russell JD (1960) Aromatic-alcohol-oxidase activity in the growth medium of Polystictus versicolor. Biochem J 74:257–262Google Scholar
  25. Fernández IS, Ruiz-Dueñas FJ, Santillana E, Ferreira P, Martínez MJ, Martínez AT, Romero A (2009) Novel structural features in the GMC family of oxidoreductases revealed by the crystal structure of fungal aryl-alcohol oxidase. Acta Crystallogr D: Biol Crystallogr 65:1196–1205CrossRefGoogle Scholar
  26. Ferreira P, Medina M, Guillén F, Martínez MJ, van Berkel WJH, Martínez AT (2005) Spectral and catalytic properties of aryl-alcohol oxidase, a fungal flavoenzyme acting on polyunsaturated alcohols. Biochem J 389:731–738CrossRefGoogle Scholar
  27. Ferreira P, Ruiz-Dueñas FJ, Martínez MJ, van Berkel WJH, Martínez AT (2006) Site-directed mutagenesis of selected residues at the active site of aryl-alcohol oxidase, an H2O2-producing enzyme. FEBS J 273:4878–4888CrossRefGoogle Scholar
  28. Ferreira P, Hernández-Ortega A, Herguedas B, Martínez AT, Medina M (2009) Aryl-alcohol oxidase involved in lignin degradation: a mechanistic study based on steady and pre-steady state kinetics and primary and solvent isotope effects with two different alcohol substrates. J Biol Chem 284:24840–24847CrossRefGoogle Scholar
  29. Ferreira P, Hernández-Ortega A, Herguedas B, Rencoret J, Gutiérrez A, Martínez MJ, Jiménez-Barbero J, Medina M, Martínez AT (2010) Kinetic and chemical characterization of aldehyde oxidation by fungal aryl-alcohol oxidase. Biochem J 425:585–593CrossRefGoogle Scholar
  30. Forney LJ, Reddy CA, Tien M, Aust SD (1982) The involvement of hydroxyl radical derived from hydrogen peroxide in lignin degradation by the white rot fungus Phanerochaete chrysosporium. J Biol Chem 257:11455–11462Google Scholar
  31. Fraaije MW, Veeger C, van Berkel WJH (1995) Substrate specificity of flavin-dependent vanillyl-alcohol oxidase from Penicillium simplicissimum. Evidence for the production of 4-hydroxycinnamyl alcohols from allylphenols. Eur J Biochem 234:271–277CrossRefGoogle Scholar
  32. Fraatz MA, Zorn H (2011) Fungal flavours. In: Hofrichter M (ed) The Mycota. X Industrial applications, 2nd edn. Springer, Berlin, pp 249–268Google Scholar
  33. Gadda G (2003) pH and deuterium kinetic isotope effects studies on the oxidation of choline to betaine-aldehyde catalyzed by choline oxidase. Biochim Biophys Acta 1650:4–9Google Scholar
  34. Gadda G (2008) Hydride transfer made easy in the reaction of alcohol oxidation catalyzed by flavin-dependent oxidases. Biochemistry 47:13745–13753CrossRefGoogle Scholar
  35. Gallagher IM, Fraser MA, Evans CS, Atkey PT (1989) Ultrastructural localization of lignocellulose-degrading enzymes. In: Lewis NG, Paice MG (eds) ACS Symposium “Plant Cell-Wall Polymers: Biogenesis and Biodegradation”, Vol 399. Amer Chem Soc pp 426–442Google Scholar
  36. Ghanem M, Gadda G (2005) On the catalytic role of the conserved active site residue His466 of choline oxidase. Biochemistry 44:893–904CrossRefGoogle Scholar
  37. Goetghebeur M, Brun S, Galzy P, Nicolas M (1993) Benzyl alcohol oxidase and laccase synthesis in Botrytis cinerea. Biosci Biotechnol Biochem 57:1380–1381CrossRefGoogle Scholar
  38. Gómez-Toribio V, García-Martín AB, Martínez MJ, Martínez AT, Guillén F (2009) Induction of extracellular hydroxyl radical production by white-rot fungi through quinone redox cycling. Appl Environ Microbiol 75:3944–3953CrossRefGoogle Scholar
  39. Green F III, Clausen CA, Larsen MJ, Highley TL (1992) Immuno-scanning electron microscopic localization of extracellular wood-degrading enzymes within the fibrillar sheath of the brown-rot fungus Postia placenta. Can J Microbiol 38:898–904CrossRefGoogle Scholar
  40. Greene RV, Gould JM (1984) Fatty acyl-coenzyme A oxidase activity and H2O2 production in Phanerochaete chrysosporium mycelia. Biochem Biophys Res Commun 118:437–443CrossRefGoogle Scholar
  41. Gross B, Asther M, Corrieu G, Brunerie P (1993) Production of vanillin by bioconversion of benzenoid precursors by Pycnoporus. Patent (USA) 5262315Google Scholar
  42. Guillén F, Evans CS (1994) Anisaldehyde and veratraldehyde acting as redox cycling agents for H2O2 production by Pleurotus eryngii. Appl Environ Microbiol 60:2811–2817Google Scholar
  43. Guillén F, Martínez AT, Martínez MJ (1990) Production of hydrogen peroxide by aryl-alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Appl Microbiol Biotechnol 32:465–469CrossRefGoogle Scholar
  44. Guillén F, Martínez AT, Martínez MJ (1992) Substrate specificity and properties of the aryl-alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Eur J Biochem 209:603–611CrossRefGoogle Scholar
  45. Guillén F, Martínez AT, Martínez MJ, Evans CS (1994) Hydrogen peroxide-producing system of Pleurotus eryngii involving the extracellular enzyme aryl-alcohol oxidase. Appl Microbiol Biotechnol 41:465–470Google Scholar
  46. Guillén F, Gómez-Toribio V, Martínez MJ, Martínez AT (2000) Production of hydroxyl radical by the synergistic action of fungal laccase and aryl alcohol oxidase. Arch Biochem Biophys 383:142–147CrossRefGoogle Scholar
  47. Gutiérrez A, Caramelo L, Prieto A, Martínez MJ, Martínez AT (1994) Anisaldehyde production and aryl-alcohol oxidase and dehydrogenase activities in ligninolytic fungi from the genus Pleurotus. Appl Environ Microbiol 60:1783–1788Google Scholar
  48. Hallberg BM, Henriksson G, Pettersson G, Divne C (2002) Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase. J Mol Biol 315:421–434CrossRefGoogle Scholar
  49. Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355CrossRefGoogle Scholar
  50. Hammel KE, Kapich AN, Jensen KA Jr, Ryan ZC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453CrossRefGoogle Scholar
  51. Hecht HJ, Kalisz HM, Hendle J, Schmid RD, Schomburg D (1993) Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3 Å resolution. J Mol Biol 229:153–172CrossRefGoogle Scholar
  52. Hernández-Ortega A, Ferreira P, Martínez MJ, Romero A, Martínez AT (2008) Discriminating the role of His502 and His546 in the catalysis of aryl-alcohol oxidase. In: Frago S, Gómez-Moreno C, Medina M (eds) Flavins and flavoproteins 2008. Prensas Universitarias, Zaragoza, pp 303–308Google Scholar
  53. Hernández-Ortega A, Borrelli K, Ferreira P, Medina M, Martínez AT, Guallar V (2011a) Substrate diffusion and oxidation in GMC oxidoreductases: an experimental and computational study on fungal aryl-alcohol oxidase. Biochem J 436:341–350CrossRefGoogle Scholar
  54. Hernández-Ortega A, Ferreira P, Merino P, Medina M, Guallar V, Martínez AT (2011b) Stereoselective hydride transfer by aryl-alcohol oxidase, a member of the GMC superfamily. ChemBioChem. doi: 10.1002/cbic.201100709
  55. Hernández-Ortega A, Ferreira P, Merino P, Medina M, Guallar V, Martínez AT (2011c) Stereoselective hydride transfer mechanism in substrate oxidation by aryl-alcohol oxidase. Abs Flavins and Flavoproteins 2011, Berkeley, 24-29 JulyGoogle Scholar
  56. Hernández-Ortega A, Lucas F, Ferreira P, Medina M, Guallar V, Martínez AT (2011d) Modulating O2 reactivity in a fungal flavoenzyme: involvement of aryl-alcohol oxidase Phe-501 contiguous to catalytic histidine. J Biol Chem 25:4115–4114Google Scholar
  57. Higuchi T (1997) Biochemistry and molecular biology of wood. Springer, LondonCrossRefGoogle Scholar
  58. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807CrossRefGoogle Scholar
  59. Iwahara S, Nishihira T, Jomori T, Kuwahara M, Higuchi T (1980) Enzymic oxidation of α, β-unsaturated alcohols in the side chains of lignin-related aromatic compounds. J Ferment Technol 58:183–188Google Scholar
  60. Jensen KA Jr, Evans KMC, Kirk TK, Hammel KE (1994) Biosynthetic pathway for veratryl alcohol in the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 60:709–714Google Scholar
  61. 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 446:49–54CrossRefGoogle Scholar
  62. Kersten PJ (1990) Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proc Natl Acad Sci USA 87:2936–2940CrossRefGoogle Scholar
  63. Kersten P, Cullen D (2007) Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol 44:77–87CrossRefGoogle Scholar
  64. Kersten PJ, Kirk TK (1987) Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Bacteriol 169:2195–2201Google Scholar
  65. Kiess M, Hecht HJ, Kalisz HM (1998) Glucose oxidase from Penicillium amagasakiense. Primary structure and comparison with other glucose–methanol–choline (GMC) oxidoreductases. Eur J Biochem 252:90–99CrossRefGoogle Scholar
  66. Kimura Y, Asada Y, Kuwahara M (1990) Screening of basidiomycetes for lignin peroxidase genes using a DNA probe. Appl Microbiol Biotechnol 32:436–442CrossRefGoogle Scholar
  67. Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505CrossRefGoogle Scholar
  68. Kittl R, Sygmund C, Halada P, Volc J, Divne C, Haltrich D, Peterbauer CK (2008) Molecular cloning of three pyranose dehydrogenase-encoding genes from Agaricus meleagris and analysis of their expression by real-time RT–PCR. Curr Genetics 53:117–127CrossRefGoogle Scholar
  69. Krings U, Berger RG (1998) Biotechnological production of flavours and fragrances. Appl Microbiol Biotechnol 49:1–8CrossRefGoogle Scholar
  70. Lapadatescu C, Giniès C, Djian A, Spinnler HE, Le Quéré J-L, Bonnarme P (1999) Regulation of the synthesis of aryl metabolites by phospholipid sources in the white-rot fungus Bjerkandera adusta. Arch Microbiol 171:151–158CrossRefGoogle Scholar
  71. Lapadatescu C, Giniès C, Le Quéré J-L, Bonnarme P (2000) Novel scheme for biosynthesis of aryl metabolites from L-phenylalanine in the fungus Bjerkandera adusta. Appl Environ Microbiol 66:1517–1522CrossRefGoogle Scholar
  72. Lario PI, Sampson N, Vrielink A (2003) Sub-atomic resolution crystal structure of cholesterol oxidase: what atomic resolution crystallography reveals about enzyme mechanism and the role of the FAD cofactor in redox activity. J Mol Biol 326:1635–1650CrossRefGoogle Scholar
  73. Leskovac V, Trivic S, Wohlfahrt G, Kandrac J, Pericin D (2005) Glucose oxidase from Aspergillus niger: the mechanism of action with molecular oxygen, quinones, and one-electron acceptors. Int J Biochem Cell Biol 37:731–750CrossRefGoogle Scholar
  74. Lundell TK, Leonowicz A, Mohammadi OK, Hatakka AI (1990) Metabolism of veratric acid by lignin-degrading white-rot fungi. In: Kirk TK, Chang H-m (eds) Biotechnology in pulp and paper manufacture. Applications and fundamental investigations. Butterworth-Heinemann, Boston, pp 401–409Google Scholar
  75. Lyubimov AY, Lario PI, Moustafa I, Vrielink A (2006) Atomic resolution crystallography reveals how changes in pH shape the protein microenvironment. Nat Chem Biol 2:259–264CrossRefGoogle Scholar
  76. Marchal S, Branlant G (1999) Evidence for the chemical activation of essential Cys-302 upon cofactor binding to nonphosphorylating glyceraldehyde 3-phosphate dehydrogenase from Streptococcus mutans. Biochemistry 38:12950–12958CrossRefGoogle Scholar
  77. Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbiological, chemical and enzymatic aspects of fungal attack to lignin. Intern Microbiol 8:195–204Google Scholar
  78. Martínez AT, Rencoret J, Marques G, Gutiérrez A, Ibarra D, Jiménez-Barbero J, del Río JC (2008) Monolignol acylation and lignin structure in some nonwoody plants: a 2D NMR study. Phytochemistry 69:2831–2843CrossRefGoogle Scholar
  79. Martínez D, Challacombe J, Morgenstern I, Hibbett DS, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Dueñas FJ, Martínez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuña R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kues U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959CrossRefGoogle Scholar
  80. Martínez AT, Rencoret J, Nieto L, Jiménez-Barbero J, Gutiérrez A, del Río JC (2011) Selective lignin and polysaccharide removal in natural fungal decay of wood as evidenced by in situ structural analyses. Environ Microbiol 13:96–107CrossRefGoogle Scholar
  81. Marzullo L, Cannio R, Giardina P, Santini MT, Sannia G (1995) Veratryl alcohol oxidase from Pleurotus ostreatus participates in lignin biodegradation and prevents polymerization of laccase-oxidized substrates. J Biol Chem 270:3823–3827CrossRefGoogle Scholar
  82. Matsuda T, Yamanaka R, Nakamura K (2009) Recent progress in biocatalysis for asymmetric oxidation and reduction. Tetrahedron-Asymmetry 20:513–557CrossRefGoogle Scholar
  83. Minasian SG, Whittaker MM, Whittaker JW (2004) Stereoselective hydrogen abstraction by galactose oxidase. Biochemistry 43:13683–13693CrossRefGoogle Scholar
  84. Muheim A, Leisola MSA, Schoemaker HE (1990) Aryl-alcohol oxidase and lignin peroxidase from the white-rot fungus Bjerkandera adusta. J Biotechnol 13:159–167CrossRefGoogle Scholar
  85. Muheim A, Waldner R, Sanglard D, Reiser J, Schoemaker HE, Leisola MSA (1991) Purification and properties of an aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium. Eur J Biochem 195:369–375CrossRefGoogle Scholar
  86. Muñoz C, Guillén F, Martínez AT, Martínez MJ (1997) Laccase isoenzymes of Pleurotus eryngii: characterization, catalytic properties and participation in activation of molecular oxygen and Mn2+ oxidation. Appl Environ Microbiol 63:2166–2174Google Scholar
  87. Nishida A, Eriksson K-E (1987) Formation, purification, and partial characterization of methanol oxidase, a H2O2-producing enzyme in Phanerochaete chrysosporium. Biotechnol Appl Biochem 9:325–338Google Scholar
  88. Otjen L, Blanchette RA (1986) A discussion of microstructural changes in wood during decomposition by white rot basidiomycetes. Can J Bot 64:905–911CrossRefGoogle Scholar
  89. Plaggenborg R, Overhage J, Loos A, Archer JAC, Lessard P, Sinskey AJ, Steinbuchel A, Priefert H (2006) Potential of Rhodococcus strains for biotechnological vanillin production from ferulic acid and eugenol. Appl Microbiol Biotechnol 72:745–755CrossRefGoogle Scholar
  90. Priefert H, Rabenhorst J, Steinbüchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56:296–314CrossRefGoogle Scholar
  91. Quaye O, Lountos GT, Fan F, Orville AM, Gadda G (2008) Role of Glu312 in binding and positioning of the substrate for the hydride transfer reaction in choline oxidase. Biochemistry 47:243–256CrossRefGoogle Scholar
  92. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489CrossRefGoogle Scholar
  93. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3:29–60CrossRefGoogle Scholar
  94. Romero E, Ferreira P, Martínez AT, Martínez MJ (2009) New oxidase from Bjerkandera arthroconidial anamorph that oxidizes both phenolic and nonphenolic benzyl alcohols. Biochim Biophys Acta 1794:689–697Google Scholar
  95. Romero E, Martínez AT, Martínez MJ (2010) Molecular characterization of a new flavooxidase from a Bjerkandera adusta anamorph. Proc OESIB, Santiago de Compostela, 14–15 September. In: Feijoo G, Moreira MT (eds) ISBN-13: 978-84-614-2824-3) pp 86-91Google Scholar
  96. Rotsaert FAJ, Renganathan V, Gold MH (2003) Role of the flavin domain residues, His689 and Asn732, in the catalytic mechanism of cellobiose dehydrogenase from Phanerochaete chrysosporium. Biochemistry 42:4049–4056CrossRefGoogle Scholar
  97. Ruiz-Dueñas FJ, Martínez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microbial Biotechnol 2:164–177CrossRefGoogle Scholar
  98. Ruiz-Dueñas FJ, Ferreira P, Martínez MJ, Martínez AT (2006) In vitro activation, purification, and characterization of Escherichia coli expressed aryl-alcohol oxidase, a unique H2O2-producing enzyme. Protein Expr Purif 45:191–199CrossRefGoogle Scholar
  99. Ruiz-Dueñas FJ, Morales M, García E, Miki Y, Martínez MJ, Martínez AT (2009) Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60:441–452CrossRefGoogle Scholar
  100. Rungsrisuriyachai K, Gadda G (2008) On the role of histidine 351 in the reaction of alcohol oxidation catalyzed by choline oxidase. Biochemistry 47:6762–6769CrossRefGoogle Scholar
  101. Salvachúa D, Prieto A, Lopez-Abelairas M, Lú-Chau T, Martínez AT, Martínez MJ (2011) Fungal pretreatment: an alternative in second-generation ethanol from wheat straw. Bioresource Technol 102:7500–7506CrossRefGoogle Scholar
  102. Sannia G, Limongi P, Cocca E, Buonocore F, Nitti G, Giardina P (1991) Purification and characterization of a veratryl alcohol oxidase enzyme from the lignin degrading basidiomycete Pleurotus ostreatus. Biochim Biophys Acta 1073:114–119CrossRefGoogle Scholar
  103. Schwarze FWMR, Engels J, Mattheck C (2000) Fungal strategies of decay in trees. Springer, BerlinCrossRefGoogle Scholar
  104. Shimada M, Higuchi T (1991) Microbial, enzymatic and biomimetic degradation of lignin. In: Hon DNS, Shiraishi N (eds) Wood and cellulosic chemistry. Marcel Dekker, New York, pp 557–619Google Scholar
  105. Sucharitakul J, Wongnate T, Chaiyen P (2010) Kinetic isotope effects on the noncovalent flavin mutant protein of pyranose 2-oxidase reveal insights into the flavin reduction mechanism. Biochemistry 49:3753–3765CrossRefGoogle Scholar
  106. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  107. van den Heuvel RHH, Fraaije MW, Laane C, van Berkel WJH (1998) Regio- and stereospecific conversion of 4-alkylphenols by the covalent flavoprotein vanillyl-alcohol oxidase. J Bacteriol 180:5646–5651Google Scholar
  108. van den Heuvel RH, Fraaije MW, Ferrer M, Mattevi A, van Berkel WJ (2000) Inversion of stereospecificity of vanillyl-alcohol oxidase. Proc Natl Acad Sci USA 97:9455–9460CrossRefGoogle Scholar
  109. van den Heuvel RH, Fraaije MW, Laane C, van Berkel WJ (2001) Enzymatic synthesis of vanillin. J Agric Food Chem 49:2954–2958CrossRefGoogle Scholar
  110. van den Heuvel RHH, van den Berg WAM, Rovida S, van Berkel WJH (2004) Laboratory-evolved vanillyl-alcohol oxidase produces natural vanillin. J Biol Chem 279:33492–33500CrossRefGoogle Scholar
  111. Vanden Wymelenberg A, Gaskell J, Mozuch M, Kersten P, Sabat G, Martínez D, Cullen D (2009) Transcriptome and secretome analyses of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol 75:4058–4068CrossRefGoogle Scholar
  112. Varela E, Martínez AT, Martínez MJ (1999) Molecular cloning of aryl-alcohol oxidase from Pleurotus eryngii, an enzyme involved in lignin degradation. Biochem J 341:113–117CrossRefGoogle Scholar
  113. Varela E, Böckle B, Romero A, Martínez AT, Martínez MJ (2000a) Biochemical characterization, cDNA cloning and protein crystallization of aryl-alcohol oxidase from Pleurotus pulmonarius. Biochim Biophys Acta 1476:129–138CrossRefGoogle Scholar
  114. Varela E, Martínez MJ, Martínez AT (2000b) Aryl-alcohol oxidase protein sequence: a comparison with glucose oxidase and other FAD oxidoreductases. Biochim Biophys Acta 1481:202–208CrossRefGoogle Scholar
  115. Waldner R, Leisola MSA, Fiechter A (1988) Comparison of ligninolytic activities of selected white-rot fungi. Appl Microbiol Biotechnol 29:400–407CrossRefGoogle Scholar
  116. Weibel MK, Bright HJ (1971) The glucose oxidase mechanism. Interpretation of the pH dependence. J Biol Chem 246:2734–2744Google Scholar
  117. Wierenga RK, Drenth J, Schulz GE (1983) Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain of p-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase. J Mol Biol 167:725–739CrossRefGoogle Scholar
  118. Witt S, Wohlfahrt G, Schomburg D, Hecht HJ, Kalisz HM (2000) Conserved arginine-516 of Penicillium amagasakiense glucose oxidase is essential for the efficient binding of β-D-glucose. Biochem J 347:553–559CrossRefGoogle Scholar
  119. Wohlfahrt G, Witt S, Hendle J, Schomburg D, Kalisz HM, Hecht H-J (1999) 1.8 and 1.9 Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidase as a basis for modelling substrate complexes. Acta Crystallogr D 55:969–977CrossRefGoogle Scholar
  120. Wohlfahrt G, Trivic S, Zeremski J, Pericin D, Leskovac V (2004) The chemical mechanism of action of glucose oxidase from Aspergillus niger. Mol Cell Biochem 260:69–83CrossRefGoogle Scholar
  121. Wongnate T, Sucharitakul J, Chaiyen P (2011) Identification of a catalytic base for sugar oxidation in the pyranose-2 oxidation reaction. ChemBioChem Online. doi: 10.1002/cbc.201100564
  122. Wünning P (2001) Applications and use of lignin as raw material. In: Hofrichter M, Steinbüchel A (eds) Biopolymers. Lignin, humic substances and coal. Wiley–VCH, Weinheim, pp 117–127Google Scholar
  123. Yelle DJ, Wei DS, Ralph J, Hammel KE (2011) Multidimensional NMR analysis reveals truncated lignin structures in wood decayed by the brown rot basidiomycete. Environ Microbiol 13:1091–1100CrossRefGoogle Scholar
  124. Yoshida M, Ohira T, Igarashi K, Nagasawa H, Aida K, Hallberg BM, Divne C, Nishino T, Samejima M (2001) Production and characterization of recombinant Phanerochaete chrysosporium cellobiose dehydrogenase in the methylotrophic yeast Pichia pastoris. Biosci Biotechnol Biochem 65:2050–2057CrossRefGoogle Scholar
  125. Yue QK, Kass IJ, Sampson NS, Vrielink A (1999) Crystal structure determination of cholesterol oxidase from Streptomyces and structural characterization of key active site mutants. Biochemistry 38:4277–4286CrossRefGoogle Scholar
  126. Zabel R, Morrell J (1992) Wood microbiology: decay and its prevention. Academic, LondonGoogle Scholar
  127. Zámocký M, Hallberg M, Ludwig R, Divne C, Haltrich D (2004) Ancestral gene fusion in cellobiose dehydrogenases reflects a specific evolution of GMC oxidoreductases in fungi. Gene 338:1–14CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Aitor Hernández-Ortega
    • 1
  • Patricia Ferreira
    • 2
  • Angel T. Martínez
    • 1
    Email author
  1. 1.Centro de Investigaciones BiológicasConsejo Superior de Investigaciones Científicas (CSIC)MadridSpain
  2. 2.Departamento de Bioquímica y Biología Molecular y Celular and Instituto de Biocomputación y Fisica de los Sistemas ComplejosUniversidad de ZaragozaZaragozaSpain

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