Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus
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 a 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 analysed 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 lytic polysaccharide monooxygenase gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood-decaying process.
- Authors:
-
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- Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE; Université de Lorraine, Nancy (France). Interactions Arbres/Microorganismes. INRAE
- Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE
- Aix Marseille Univ. (France). Biodiversity and Biotechnology of Fungi. INRAE; Aix Marseille Univ. (France). INRAE. CIRM-CF
- INRAE, UMR1163, Biodiversity and Biotechnology of Fungi, Aix Marseille University, 13009 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
- Fungal Physiology, Westerdijk Fungal Biodiversity Institute and Fungal Molecular Physiology, Utrecht University, Utrecht, The Netherlands; Department of Microbiology, University of Helsinki, Helsinki, Finland
- Department of Biology, Southeast Missouri State University, Cape Girardeau, MI, USA
- CNRS, UMR7257, AFMB, Aix Marseille University, Marseille, France; INRAE, USC1408, AFMB, Marseille, France
- Department of Microbiology, University of Helsinki, Helsinki, Finland
- Department of Molecular Wood Biotechnology and Technical Mycology, Büsgen-Institute, Georg-August-University Göttingen, Göttingen, Germany; Center for Molecular Biosciences (GZMB), Georg-August-University Göttingen, Göttingen, Germany
- Centro de Investigaciones Biológicas, CSIC, Madrid, Spain
- INRAE, UMR1136, Interactions Arbres/Microorganismes, Université de Lorraine, Nancy, France
- Molecular Microbiology and Biotechnology, Institute of Biology Leiden, Leiden University, Leiden, The Netherlands
- Microbiology, Utrecht University, Utrecht, The Netherlands
- US Department of Energy, Joint Genome Institute, Walnut Creek, CA, USA; Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- Contributing Org.:
- UMR INRAE Research Collaboration
- OSTI Identifier:
- 1816251
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- DNA Research
- Additional Journal Information:
- Journal Volume: 27; Journal Issue: 2; Journal ID: ISSN 1340-2838
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., and Rosso, Marie-Noëlle. Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. United States: N. p., 2020.
Web. doi:10.1093/dnares/dsaa011.
Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., & Rosso, Marie-Noëlle. Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. United States. https://doi.org/10.1093/dnares/dsaa011
Miyauchi, Shingo, Hage, Hayat, Drula, Elodie, Lesage-Meessen, Laurence, Berrin, Jean-Guy, Navarro, David, Favel, Anne, Chaduli, Delphine, Grisel, Sacha, Haon, Mireille, Piumi, François, Levasseur, Anthony, Lomascolo, Anne, Ahrendt, Steven, Barry, Kerrie, LaButti, Kurt M., Chevret, Didier, Daum, Chris, Mariette, Jérôme, Klopp, Christophe, Cullen, Daniel, de Vries, Ronald P., Gathman, Allen C., Hainaut, Matthieu, Henrissat, Bernard, Hildén, Kristiina S., Kües, Ursula, Lilly, Walt, Lipzen, Anna, Mäkelä, Miia R., Martinez, Angel T., Morel-Rouhier, Mélanie, Morin, Emmanuelle, Pangilinan, Jasmyn, Ram, Arthur F. J., Wösten, Han A. B., Ruiz-Dueñas, Francisco J., Riley, Robert, Record, Eric, Grigoriev, Igor V., and Rosso, Marie-Noëlle. Wed .
"Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus". United States. https://doi.org/10.1093/dnares/dsaa011. https://www.osti.gov/servlets/purl/1816251.
@article{osti_1816251,
title = {Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus},
author = {Miyauchi, Shingo and Hage, Hayat and Drula, Elodie and Lesage-Meessen, Laurence and Berrin, Jean-Guy and Navarro, David and Favel, Anne and Chaduli, Delphine and Grisel, Sacha and Haon, Mireille and Piumi, François and Levasseur, Anthony and Lomascolo, Anne and Ahrendt, Steven and Barry, Kerrie and LaButti, Kurt M. and Chevret, Didier and Daum, Chris and Mariette, Jérôme and Klopp, Christophe and Cullen, Daniel and de Vries, Ronald P. and Gathman, Allen C. and Hainaut, Matthieu and Henrissat, Bernard and Hildén, Kristiina S. and Kües, Ursula and Lilly, Walt and Lipzen, Anna and Mäkelä, Miia R. and Martinez, Angel T. and Morel-Rouhier, Mélanie and Morin, Emmanuelle and Pangilinan, Jasmyn and Ram, Arthur F. J. and Wösten, Han A. B. and Ruiz-Dueñas, Francisco J. and Riley, Robert and Record, Eric and Grigoriev, Igor V. and Rosso, Marie-Noëlle},
abstractNote = {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 a 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 analysed 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 lytic polysaccharide monooxygenase gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood-decaying process.},
doi = {10.1093/dnares/dsaa011},
journal = {DNA Research},
number = 2,
volume = 27,
place = {United States},
year = {Wed Apr 01 00:00:00 EDT 2020},
month = {Wed Apr 01 00:00:00 EDT 2020}
}
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Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass
journal, July 2018
- Miyauchi, Shingo; Rancon, Anaïs; Drula, Elodie
- Biotechnology for Biofuels, Vol. 11, Issue 1
Lignin-degrading Peroxidases from Genome of Selective Ligninolytic Fungus Ceriporiopsis subvermispora
journal, March 2012
- Fernández-Fueyo, Elena; Ruiz-Dueñas, Francisco J.; Miki, Yuta
- Journal of Biological Chemistry, Vol. 287, Issue 20
Glyoxal oxidases: their nature and properties
journal, April 2017
- Daou, Marianne; Faulds, Craig B.
- World Journal of Microbiology and Biotechnology, Vol. 33, Issue 5
Extracellular electron transfer systems fuel cellulose oxidative degradation
journal, April 2016
- Kracher, D.; Scheiblbrandner, S.; Felice, A. K. G.
- Science, Vol. 352, Issue 6289
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown
journal, January 2014
- Levasseur, Anthony; Lomascolo, Anne; Chabrol, Olivier
- BMC Genomics, Vol. 15, Issue 1
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014
- Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Fungal secretomics to probe the biological functions of lytic polysaccharide monooxygenases
journal, August 2017
- Berrin, Jean-Guy; Rosso, Marie-Noëlle; Abou Hachem, Maher
- Carbohydrate Research, Vol. 448