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Conserved white rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus

  • Shingo Miyauchi
  • , Hayat Hage
  • , Elodie Drula
  • , Laurence Lesage-Meessen
  • , Jean-Guy Berrin
  • , David Navarro
  • , Anne Favel
  • , Delphine Chaduli
  • , Sacha Grisel
  • , Mireille Haon
  • , François Piumi
  • , Anthony Levasseur
  • , Anne Lomascolo
  • , Steven Ahrendt
  • , Kerrie Barry
  • , Kurt M LaButti
  • , Didier Chevret
  • , Chris Daum
  • , Jérôme Mariette
  • , Christophe Klopp
  • Daniel Cullen, Ronald P de Vries, Allen C Gathman, Matthieu Hainaut, Bernard Henrissat, Kristiina S Hildén, Ursula Kües, Walt Lilly, Anna Lipzen, Miia R Mäkelä, Angel T Martinez, Mélanie Morel-Rouhier, Emmanuelle Morin, Jasmyn Pangilinan, Arthur F J Ram, Han A B Wösten, Francisco J Ruiz-Dueñas, Robert Riley, Eric Record, Igor V Grigoriev, Marie-Noëlle Rosso
  • Université de Lorraine, INRAE, UMR1136, Interactions Arbres/Microorganismes, France.
  • INRAE, Aix Marseille Univ, BBF, Marseille, France.
  • INRAE, Aix Marseille Univ, CIRM-CF, UMR1163, Marseille, France.
  • US Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
  • INRAE, UMR1319, Micalis, Plateforme d'Analyse Protéomique de Paris Sud-Ouest, Jouy-en-Josas, France.
  • INRAE, Genotoul Bioinfo, UR875, Mathématiques et Informatique Appliquées de Toulouse, Castanet-Tolosan, France.
  • USDA Forest Products Laboratory, Madison, WI, USA.
  • Department of Biology, Southeast Missouri State University, Cape Girardeau, Missouri, United States of America.
  • INRAE, USC1408, AFMB, Marseille, France.
  • Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT, Utrecht, The Netherlands; Department of Food and Environmental Sciences, Division of Microbiology and Biotechnology, P.O. Box 56, Viikinkaari 9, University of Helsinki, Helsinki, Finland, Finland.
  • Center for Molecular Biosciences (GZMB), Georg-August-University Göttingen, Göttingen, Germany.
  • Department of Cellular and Molecular Biology, Centro de Investigaciones Biológicas CSIC, Madrid, 28040, Spain.
  • Leiden University
  • Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA.
  • extern

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood decaying activity within the Basidiomycota genus Pycnoporus. We observed strong conservation in the genome structures and the repertoires of protein coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analyzed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2 producing enzymes with H2O2 consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 LPMO gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood decaying process.

Original languageEnglish
Pages (from-to)1-14
JournalDNA Research
Volume27
Issue number2
DOIs
Publication statusPublished - 12 Jun 2020

Keywords

  • wood decay
  • lignocellulose
  • CAZyme
  • Lytic Polysaccharide Monooxygenase (LPMO)
  • Class II Peroxidase

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