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

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Abstract

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.

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References

  • Aguilar C, Urzúa U, Koenig C, Vicuña R (1999) Oxalate oxidase from Ceriporiopsis subvermispora: biochemical and cytochemical studies. Arch Biochem Biophys 366:275–282

    Article  CAS  Google Scholar 

  • 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 43:11683–11690

    Article  CAS  Google Scholar 

  • 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 64:325–332

    CAS  Google Scholar 

  • Borrelli KW, Vitalis A, Alcantara R, Guallar V (2005) PELE: Protein energy landscape exploration. A novel Monte Carlo based technique. J Chem Theory Comput 1:1304–1311

    Article  CAS  Google Scholar 

  • Bourbonnais R, Paice MG (1988) Veratryl alcohol oxidases from the lignin degrading basidiomycete Pleurotus sajor-caju. Biochem J 255:445–450

    Google Scholar 

  • Bright HJ, Appleby M (1969) The pH dependence of the individual steps in the glucose oxidase reaction. J Biol Chem 244:3625–3634

    CAS  Google Scholar 

  • Camarero S, Böckle B, Martínez MJ, Martínez AT (1996) Manganese-mediated lignin degradation by Pleurotus pulmonarius. Appl Environ Microbiol 62:1070–1072

    CAS  Google Scholar 

  • Carey JS, Laffan D, Thomson C, Williams MT (2006) Analysis of the reactions used for the preparation of drug candidate molecules. Org Biomol Chem 4:2337–2347

    Article  CAS  Google Scholar 

  • Cavener DR (1992) GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J Mol Biol 223:811–814

    Article  CAS  Google Scholar 

  • 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 60:2524–2532

    CAS  Google Scholar 

  • 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 73:6241–6253

    Article  CAS  Google Scholar 

  • 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 60:271–277

    Google Scholar 

  • de Jong E, Field JA, de Bont JAM (1994b) Aryl alcohols in the physiology of ligninolytic fungi. FEMS Microbiol Rev 13:153–188

    Article  Google Scholar 

  • 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

  • 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 48:3370–3377

    Article  CAS  Google Scholar 

  • Dym O, Eisenberg D (2001) Sequence–structure analysis of FAD-containing proteins. Protein Sci 10:1712–1728

    Article  CAS  Google Scholar 

  • 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 17:268–274

    Article  CAS  Google Scholar 

  • 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 23:257–262

    Article  CAS  Google Scholar 

  • Escalettes F, Turner NJ (2008) Directed evolution of galactose oxidase: generation of enantioselective secondary alcohol oxidases. ChemBioChem 9:857–860

    Article  CAS  Google Scholar 

  • Evans CS, Dutton MV, Guillén F, Veness RG (1994) Enzymes and small molecular mass agents involved with lignocellulose degradation. FEMS Microbiol Rev 13:235–240

    Article  CAS  Google Scholar 

  • Faison BD, Kirk TK (1983) Relationship between lignin degradation and production of reduced oxygen species by Phanerochaete chrysosporium. Appl Environ Microbiol 46:1140–1145

    CAS  Google Scholar 

  • Fan F, Gadda G (2005) On the catalytic mechanism of choline oxidase. J Am Chem Soc 127:2067–2074

    Article  CAS  Google Scholar 

  • Fan F, Germann MW, Gadda G (2006) Mechanistic studies of choline oxidase with betaine aldehyde and its isosteric analogue 3,3-dimethylbutyraldehyde. Biochemistry 45:1979–1986

    Article  CAS  Google Scholar 

  • Farmer VC, Henderson MEK, Russell JD (1960) Aromatic-alcohol-oxidase activity in the growth medium of Polystictus versicolor. Biochem J 74:257–262

    CAS  Google Scholar 

  • 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 65:1196–1205

    Article  CAS  Google Scholar 

  • 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 389:731–738

    Article  CAS  Google Scholar 

  • 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 273:4878–4888

    Article  CAS  Google Scholar 

  • 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 284:24840–24847

    Article  CAS  Google Scholar 

  • 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 425:585–593

    Article  CAS  Google Scholar 

  • 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 257:11455–11462

    CAS  Google Scholar 

  • 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 234:271–277

    Article  CAS  Google Scholar 

  • Fraatz MA, Zorn H (2011) Fungal flavours. In: Hofrichter M (ed) The Mycota. X Industrial applications, 2nd edn. Springer, Berlin, pp 249–268

    Google Scholar 

  • 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 1650:4–9

    CAS  Google Scholar 

  • Gadda G (2008) Hydride transfer made easy in the reaction of alcohol oxidation catalyzed by flavin-dependent oxidases. Biochemistry 47:13745–13753

    Article  CAS  Google Scholar 

  • 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 426–442

  • Ghanem M, Gadda G (2005) On the catalytic role of the conserved active site residue His466 of choline oxidase. Biochemistry 44:893–904

    Article  CAS  Google Scholar 

  • Goetghebeur M, Brun S, Galzy P, Nicolas M (1993) Benzyl alcohol oxidase and laccase synthesis in Botrytis cinerea. Biosci Biotechnol Biochem 57:1380–1381

    Article  CAS  Google Scholar 

  • 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 75:3944–3953

    Article  CAS  Google Scholar 

  • 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 38:898–904

    Article  CAS  Google Scholar 

  • Greene RV, Gould JM (1984) Fatty acyl-coenzyme A oxidase activity and H2O2 production in Phanerochaete chrysosporium mycelia. Biochem Biophys Res Commun 118:437–443

    Article  CAS  Google Scholar 

  • Gross B, Asther M, Corrieu G, Brunerie P (1993) Production of vanillin by bioconversion of benzenoid precursors by Pycnoporus. Patent (USA) 5262315

  • Guillén F, Evans CS (1994) Anisaldehyde and veratraldehyde acting as redox cycling agents for H2O2 production by Pleurotus eryngii. Appl Environ Microbiol 60:2811–2817

    Google Scholar 

  • Guillén F, Martínez AT, Martínez MJ (1990) Production of hydrogen peroxide by aryl-alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Appl Microbiol Biotechnol 32:465–469

    Article  Google Scholar 

  • 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 209:603–611

    Article  Google Scholar 

  • 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 41:465–470

    Google Scholar 

  • 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 383:142–147

    Article  CAS  Google Scholar 

  • 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 60:1783–1788

    Google Scholar 

  • Hallberg BM, Henriksson G, Pettersson G, Divne C (2002) Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase. J Mol Biol 315:421–434

    Article  CAS  Google Scholar 

  • Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11:349–355

    Article  CAS  Google Scholar 

  • Hammel KE, Kapich AN, Jensen KA Jr, Ryan ZC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453

    Article  CAS  Google Scholar 

  • 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 229:153–172

    Article  CAS  Google Scholar 

  • 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 303–308

    Google Scholar 

  • 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 436:341–350

    Article  CAS  Google Scholar 

  • 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

  • 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 July

  • 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 25:4115–4114

    Google Scholar 

  • Higuchi T (1997) Biochemistry and molecular biology of wood. Springer, London

    Book  Google Scholar 

  • 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 315:804–807

    Article  CAS  Google Scholar 

  • 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 58:183–188

    CAS  Google Scholar 

  • Jensen KA Jr, Evans KMC, Kirk TK, Hammel KE (1994) Biosynthetic pathway for veratryl alcohol in the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 60:709–714

    CAS  Google Scholar 

  • 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 446:49–54

    Article  CAS  Google Scholar 

  • Kersten PJ (1990) Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proc Natl Acad Sci USA 87:2936–2940

    Article  CAS  Google Scholar 

  • Kersten P, Cullen D (2007) Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol 44:77–87

    Article  CAS  Google Scholar 

  • Kersten PJ, Kirk TK (1987) Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Bacteriol 169:2195–2201

    CAS  Google Scholar 

  • 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 252:90–99

    Article  CAS  Google Scholar 

  • Kimura Y, Asada Y, Kuwahara M (1990) Screening of basidiomycetes for lignin peroxidase genes using a DNA probe. Appl Microbiol Biotechnol 32:436–442

    Article  CAS  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  CAS  Google Scholar 

  • 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 53:117–127

    Article  CAS  Google Scholar 

  • Krings U, Berger RG (1998) Biotechnological production of flavours and fragrances. Appl Microbiol Biotechnol 49:1–8

    Article  CAS  Google Scholar 

  • 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 171:151–158

    Article  CAS  Google Scholar 

  • 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 66:1517–1522

    Article  CAS  Google Scholar 

  • 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 326:1635–1650

    Article  CAS  Google Scholar 

  • 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 37:731–750

    Article  CAS  Google Scholar 

  • 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 401–409

    Google Scholar 

  • Lyubimov AY, Lario PI, Moustafa I, Vrielink A (2006) Atomic resolution crystallography reveals how changes in pH shape the protein microenvironment. Nat Chem Biol 2:259–264

    Article  CAS  Google Scholar 

  • 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 38:12950–12958

    Article  CAS  Google Scholar 

  • 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 8:195–204

    Google Scholar 

  • 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 69:2831–2843

    Article  CAS  Google Scholar 

  • 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 106:1954–1959

    Article  Google Scholar 

  • 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 13:96–107

    Article  CAS  Google Scholar 

  • 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 270:3823–3827

    Article  CAS  Google Scholar 

  • Matsuda T, Yamanaka R, Nakamura K (2009) Recent progress in biocatalysis for asymmetric oxidation and reduction. Tetrahedron-Asymmetry 20:513–557

    Article  CAS  Google Scholar 

  • Minasian SG, Whittaker MM, Whittaker JW (2004) Stereoselective hydrogen abstraction by galactose oxidase. Biochemistry 43:13683–13693

    Article  CAS  Google Scholar 

  • Muheim A, Leisola MSA, Schoemaker HE (1990) Aryl-alcohol oxidase and lignin peroxidase from the white-rot fungus Bjerkandera adusta. J Biotechnol 13:159–167

    Article  CAS  Google Scholar 

  • 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 195:369–375

    Article  CAS  Google Scholar 

  • 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 63:2166–2174

    Google Scholar 

  • Nishida A, Eriksson K-E (1987) Formation, purification, and partial characterization of methanol oxidase, a H2O2-producing enzyme in Phanerochaete chrysosporium. Biotechnol Appl Biochem 9:325–338

    CAS  Google Scholar 

  • Otjen L, Blanchette RA (1986) A discussion of microstructural changes in wood during decomposition by white rot basidiomycetes. Can J Bot 64:905–911

    Article  Google Scholar 

  • 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 72:745–755

    Article  CAS  Google Scholar 

  • Priefert H, Rabenhorst J, Steinbüchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56:296–314

    Article  CAS  Google Scholar 

  • 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 47:243–256

    Article  CAS  Google Scholar 

  • 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 311:484–489

    Article  CAS  Google Scholar 

  • 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 3:29–60

    Article  CAS  Google Scholar 

  • 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 1794:689–697

    CAS  Google Scholar 

  • 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 86-91

  • 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 42:4049–4056

    Article  CAS  Google Scholar 

  • 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 2:164–177

    Article  CAS  Google Scholar 

  • 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 45:191–199

    Article  CAS  Google Scholar 

  • 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 60:441–452

    Article  CAS  Google Scholar 

  • Rungsrisuriyachai K, Gadda G (2008) On the role of histidine 351 in the reaction of alcohol oxidation catalyzed by choline oxidase. Biochemistry 47:6762–6769

    Article  CAS  Google Scholar 

  • 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 102:7500–7506

    Article  CAS  Google Scholar 

  • 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 1073:114–119

    Article  CAS  Google Scholar 

  • Schwarze FWMR, Engels J, Mattheck C (2000) Fungal strategies of decay in trees. Springer, Berlin

    Book  Google Scholar 

  • 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 557–619

    Google Scholar 

  • 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 49:3753–3765

    Article  CAS  Google Scholar 

  • 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 28:2731–2739

    Article  CAS  Google Scholar 

  • 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 180:5646–5651

    Google Scholar 

  • 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 97:9455–9460

    Article  Google Scholar 

  • van den Heuvel RH, Fraaije MW, Laane C, van Berkel WJ (2001) Enzymatic synthesis of vanillin. J Agric Food Chem 49:2954–2958

    Article  CAS  Google Scholar 

  • 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 279:33492–33500

    Article  CAS  Google Scholar 

  • 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 75:4058–4068

    Article  CAS  Google Scholar 

  • Varela E, Martínez AT, Martínez MJ (1999) Molecular cloning of aryl-alcohol oxidase from Pleurotus eryngii, an enzyme involved in lignin degradation. Biochem J 341:113–117

    Article  CAS  Google Scholar 

  • 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 1476:129–138

    Article  CAS  Google Scholar 

  • Varela E, Martínez MJ, Martínez AT (2000b) Aryl-alcohol oxidase protein sequence: a comparison with glucose oxidase and other FAD oxidoreductases. Biochim Biophys Acta 1481:202–208

    Article  CAS  Google Scholar 

  • Waldner R, Leisola MSA, Fiechter A (1988) Comparison of ligninolytic activities of selected white-rot fungi. Appl Microbiol Biotechnol 29:400–407

    Article  CAS  Google Scholar 

  • Weibel MK, Bright HJ (1971) The glucose oxidase mechanism. Interpretation of the pH dependence. J Biol Chem 246:2734–2744

    CAS  Google Scholar 

  • 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 167:725–739

    Article  CAS  Google Scholar 

  • 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 347:553–559

    Article  CAS  Google Scholar 

  • 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 55:969–977

    Article  CAS  Google Scholar 

  • 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 260:69–83

    Article  CAS  Google Scholar 

  • 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

  • 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 117–127

    Google Scholar 

  • 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 13:1091–1100

    Article  CAS  Google Scholar 

  • 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 65:2050–2057

    Article  CAS  Google Scholar 

  • 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 38:4277–4286

    Article  CAS  Google Scholar 

  • Zabel R, Morrell J (1992) Wood microbiology: decay and its prevention. Academic, London

    Google Scholar 

  • 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 338:1–14

    Article  CAS  Google Scholar 

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Acknowledgments

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 (http://genome.jgi.doe.gov/programs/fungi) 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.

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  1. Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Ramiro de Maeztu 9, 28040, Madrid, Spain

    Aitor Hernández-Ortega & Angel T. Martínez

  2. Departamento de Bioquímica y Biología Molecular y Celular and Instituto de Biocomputación y Fisica de los Sistemas Complejos, Universidad de Zaragoza, 50009, Zaragoza, Spain

    Patricia Ferreira

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  1. Aitor Hernández-Ortega
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Correspondence to Angel T. Martínez.

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Hernández-Ortega, A., Ferreira, P. & Martínez, A.T. Fungal aryl-alcohol oxidase: a peroxide-producing flavoenzyme involved in lignin degradation. Appl Microbiol Biotechnol 93, 1395–1410 (2012). https://doi.org/10.1007/s00253-011-3836-8

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