Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion

Journal Article
Proceedings of the National Academy of Sciences, vol. 106, iss. 6, pp. 1954-1959, 2009
Authors
Diego Martinez, Jean Challacombe, Ingo Morgenstern, David Hibbett, Monika Schmoll, Christian P. Kubicek, Patricia Ferreira, Francisco J. Ruiz-Duenas, Angel T. Martinez, Phil Kersten, Kenneth E. Hammel, Amber Vanden Wymelenberg, Jill Gaskell, Erika Lindquist, Grzegorz Sabat, Sandra Splinter BonDurant, Luis F. Larrondo, Paulo Canessa, Rafael Vicuna, Jagjit Yadav, Harshavardhan Doddapaneni, Venkataramanan Subramanian, Antonio G. Pisabarro, José L. Lavin, José A. Oguiza, Emma Master, Bernard Henrissat, Pedro M. Coutinho, Paul Harris, Jon Karl Magnuson, Scott E. Baker, Kenneth Bruno, William Kenealy, Patrik J. Hoegger, Ursula Kües, Preethi Ramaiya, Susan Lucas, Asaf Salamov, Harris Shapiro, Hank Tu, Christine L. Chee, Monica Misra, Gary Xie, Sarah Teter, Debbie Yaver, Tim James, Martin Mokrejs, Martin Pospisek, Igor V. Grigoriev, Thomas Brettin, Dan Rokhsar, Randy Berka, Dan Cullen
Abstract
Brown-rot fungi such as Postia placenta are common inhabitants of forest ecosystems and are also largely responsible for the destructive decay of wooden structures. Rapid depolymerization of cellulose is a distinguishing feature of brown-rot, but the biochemical mechanisms and underlying genetics are poorly understood. Systematic examination of the P. placenta genome, transcriptome, and secretome revealed unique extracellular enzyme systems, including an unusual repertoire of extracellular glycoside hydrolases. Genes encoding exocellobiohydrolases and cellulose-binding domains, typical of cellulolytic microbes, are absent in this efficient cellulose-degrading fungus. When P. placenta was grown in medium containing cellulose as sole carbon source, transcripts corresponding to many hemicellulases and to a single putative β-1–4 endoglucanase were expressed at high levels relative to glucose-grown cultures. These transcript profiles were confirmed by direct identification of peptides by liquid chromatography-tandem mass spectrometry (LC-MS/MS). Also up-regulated during growth on cellulose medium were putative iron reductases, quinone reductase, and structurally divergent oxidases potentially involved in extracellular generation of Fe(II) and H 2 O 2 . These observations are consistent with a biodegradative role for Fenton chemistry in which Fe(II) and H 2 O 2 react to form hydroxyl radicals, highly reactive oxidants capable of depolymerizing cellulose. The P. placenta genome resources provide unparalleled opportunities for investigating such unusual mechanisms of cellulose conversion. More broadly, the genome offers insight into the diversification of lignocellulose degrading mechanisms in fungi. Comparisons with the closely related white-rot fungus Phanerochaete chrysosporium support an evolutionary shift from white-rot to brown-rot during which the capacity for efficient depolymerization of lignin was lost.
English