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

  1. Dan Cullenf,1
  1. aLos Alamos National Laboratory/Joint Genome Institute, P.O. Box 1663, Los Alamos, NM 87545;
  2. bDepartment of Biology, University of New Mexico, Albuquerque, NM 87131;
  3. cBiology Department, Clark University, Worcester, MA 01610;
  4. dResearch Area Gene Technology and Applied Biochemistry, Institute of Chemical Engineering, Technische Universitat Wien, Getreidemarkt 9/166, A-1060 Vienna, Austria;
  5. eCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Cientificas, Ramiro de Maeztu 9, E-28040 Madrid, Spain;
  6. fForest Products Laboratory, Madison, WI 53726;
  7. gDepartment of Bacteriology, University of Wisconsin, Madison, WI 53706;
  8. hU.S. Department of Energy Joint Genome Institute, 2800 Mitchell Avenue, Walnut Creek, CA 94598;
  9. iUniversity of Wisconsin Biotechnology Center, Madison, WI 53706;
  10. jDepartamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Millennium Institute for Fundamental and Applied Biology, Pontifica Universidad Católica de Chile, Casilla 114-D, Santiago 833-1010, Chile;
  11. kDepartment of Environmental Health, University of Cincinnati, Cincinnati, OH 45267;
  12. lGenetics and Microbiology Research Group, Public University of Navarre, 31006 Pamplona, Spain;
  13. mChemical Engineering, University of Toronto, Toronto, ON, Canada M5S 3E5;
  14. nArchitecture et Fonction des Macromolécules Biologiques, Unité Mixte de Recherche 6098, Centre National de la Recherche Scientifique, Universités d'Aix-Marseille I and II, Case 932, 163 Avenue de Luminy, 13288 Marseille, France;
  15. oNovozymes Inc., 1445 Drew Avenue, Davis, CA 95618;
  16. pPacific Northwest National Laboratory, P.O. Box 999, Richland, WA 99352;
  17. qMascoma Inc., Lebanon, NH 03766;
  18. rMolecular Wood Biotechnology and Technical Mycology, Büsgen-Institute, Georg-August-University Göttingen, Büsgenweg 2, D-37077 Göttingen, Germany;
  19. sDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109; and
  20. tFaculty of Science, Charles University, Vinicna 5, 12844 Prague, Czech Republic

  1. Edited by Richard A. Dixon, The Samuel Roberts Noble Foundation, Ardmore, OK, and approved December 15, 2008 (received for review September 24, 2008)

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 H2O2. These observations are consistent with a biodegradative role for Fenton chemistry in which Fe(II) and H2O2 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.

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: dcullen{at}wisc.edu

  • Author contributions: D.M., J.C., D.H., E.L., S.S.B., I.V.G., T.B., D.R., R.B., and D.C. designed research; A.V.W., J.G., G.S., and D.C. performed research; D.M., J.C., I.M., D.H., M.S., C.P.K., P.F., F.J.R.-D., A.T.M., P.K., K.E.H., A.V.W., J.G., E.L., G.S., S.S.B., L.F.L., P.C., R.V., J.Y., H.D., V.S., A.G.P., J.L.L., J.A.O., E.M., B.H., P.M.C., P.H., J.K.M., S.E.B., K.B., W.K., P.J.H., U.K., P.R., S.L., A.S., H.S., H.T., C.L.C., M. Misra, G.X., S.T., D.Y., T.J., M. Mokrejs, M.P., I.V.G., R.B., and D.C. analyzed data; and D.M., P.K., K.E.H., R.B., and D.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The annotated genome is available on an interactive web portal at http://www.jgi.doe.gov/Postia. The sequences reported in this paper have been deposited in the GenBank database (accession nos. ABWF00000000 and FL595400-FL633513). The model and microarray results reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE12540).

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0809575106/DCSupplemental.

  • Received September 24, 2008.

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