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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
Mini-Review

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.

Keywords

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

Notes

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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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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