skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass

Abstract

Background Plant biomass conversion for green chemistry and bio-energy is a current challenge for a modern sustainable bioeconomy. The complex polyaromatic lignin polymers in raw biomass feedstocks (i.e., agriculture and forestry by-products) are major obstacles for biomass conversions. White-rot fungi are wood decayers able to degrade all polymers from lignocellulosic biomass including cellulose, hemicelluloses, and lignin. The white-rot fungus Polyporus brumalis efficiently breaks down lignin and is regarded as having a high potential for the initial treatment of plant biomass in its conversion to bio-energy. Here, we describe the extraordinary ability of P. brumalis for lignin degradation using its enzymatic arsenal to break down wheat straw, a lignocellulosic substrate that is considered as a biomass feedstock worldwide. Results We performed integrative multi-omics analyses by combining data from the fungal genome, transcriptomes, and secretomes. We found that the fungus possessed an unexpectedly large set of genes coding for Class II peroxidases involved in lignin degradation (19 genes) and GMC oxidoreductases/dehydrogenases involved in generating the hydrogen peroxide required for lignin peroxidase activity and promoting redox cycling of the fungal enzymes involved in oxidative cleavage of lignocellulose polymers (36 genes). The examination of interrelated multi-omics patterns revealed that eleven Class II Peroxidases weremore » secreted by the fungus during fermentation and eight of them where tightly co-regulated with redox cycling enzymatic partners. Conclusion As a peculiar feature of P. brumalis, we observed gene family extension, up-regulation and secretion of an abundant set of versatile peroxidases and manganese peroxidases, compared with other Polyporales species. The orchestrated secretion of an abundant set of these delignifying enzymes and redox cycling enzymatic partners could contribute to the delignification capabilities of the fungus. Our findings highlight the diversity of wood decay mechanisms present in Polyporales and the potentiality of further exploring this taxonomic order for enzymatic functions of biotechnological interest.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [2];  [4];  [5];  [6];  [7];  [7];  [7];  [7];  [6];  [6];  [7];  [8] more »;  [9];  [2]; ORCiD logo [2] « less
  1. Aix-Marseille Univ. (France); Univ. of Lorraine (France)
  2. Aix-Marseille Univ. (France)
  3. Aix-Marseille Univ. (France); INRA, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  4. Consejo Superior de Investigaciones Cientificas (CSIC), Madrid (Spain)
  5. Proteomic Analysis Platform of Paris Sud Ouest (PAPPSO), Jouy-en-Josas (France)
  6. Aix-Marseille Univ. (France); INRA, Marseille (France)
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  8. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  9. Aix-Marseille Univ., and CNRS, Marseille (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1544020
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
[ Journal Volume: 11; Journal Issue: 1]; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Solid-state fermentation; Lignin degradation; Polyporus brumalis; Plant biomass transformation

Citation Formats

Miyauchi, Shingo, Rancon, Anaïs, Drula, Elodie, Hage, Hayat, Chaduli, Delphine, Favel, Anne, Grisel, Sacha, Henrissat, Bernard, Herpoël-Gimbert, Isabelle, Ruiz-Dueñas, Francisco J., Chevret, Didier, Hainaut, Matthieu, Lin, Junyan, Wang, Mei, Pangilinan, Jasmyn, Lipzen, Anna, Lesage-Meessen, Laurence, Navarro, David, Riley, Robert, Grigoriev, Igor V., Zhou, Simeng, Raouche, Sana, and Rosso, Marie-Noëlle. Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass. United States: N. p., 2018. Web. doi:10.1186/s13068-018-1198-5.
Miyauchi, Shingo, Rancon, Anaïs, Drula, Elodie, Hage, Hayat, Chaduli, Delphine, Favel, Anne, Grisel, Sacha, Henrissat, Bernard, Herpoël-Gimbert, Isabelle, Ruiz-Dueñas, Francisco J., Chevret, Didier, Hainaut, Matthieu, Lin, Junyan, Wang, Mei, Pangilinan, Jasmyn, Lipzen, Anna, Lesage-Meessen, Laurence, Navarro, David, Riley, Robert, Grigoriev, Igor V., Zhou, Simeng, Raouche, Sana, & Rosso, Marie-Noëlle. Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass. United States. doi:10.1186/s13068-018-1198-5.
Miyauchi, Shingo, Rancon, Anaïs, Drula, Elodie, Hage, Hayat, Chaduli, Delphine, Favel, Anne, Grisel, Sacha, Henrissat, Bernard, Herpoël-Gimbert, Isabelle, Ruiz-Dueñas, Francisco J., Chevret, Didier, Hainaut, Matthieu, Lin, Junyan, Wang, Mei, Pangilinan, Jasmyn, Lipzen, Anna, Lesage-Meessen, Laurence, Navarro, David, Riley, Robert, Grigoriev, Igor V., Zhou, Simeng, Raouche, Sana, and Rosso, Marie-Noëlle. Mon . "Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass". United States. doi:10.1186/s13068-018-1198-5. https://www.osti.gov/servlets/purl/1544020.
@article{osti_1544020,
title = {Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass},
author = {Miyauchi, Shingo and Rancon, Anaïs and Drula, Elodie and Hage, Hayat and Chaduli, Delphine and Favel, Anne and Grisel, Sacha and Henrissat, Bernard and Herpoël-Gimbert, Isabelle and Ruiz-Dueñas, Francisco J. and Chevret, Didier and Hainaut, Matthieu and Lin, Junyan and Wang, Mei and Pangilinan, Jasmyn and Lipzen, Anna and Lesage-Meessen, Laurence and Navarro, David and Riley, Robert and Grigoriev, Igor V. and Zhou, Simeng and Raouche, Sana and Rosso, Marie-Noëlle},
abstractNote = {Background Plant biomass conversion for green chemistry and bio-energy is a current challenge for a modern sustainable bioeconomy. The complex polyaromatic lignin polymers in raw biomass feedstocks (i.e., agriculture and forestry by-products) are major obstacles for biomass conversions. White-rot fungi are wood decayers able to degrade all polymers from lignocellulosic biomass including cellulose, hemicelluloses, and lignin. The white-rot fungus Polyporus brumalis efficiently breaks down lignin and is regarded as having a high potential for the initial treatment of plant biomass in its conversion to bio-energy. Here, we describe the extraordinary ability of P. brumalis for lignin degradation using its enzymatic arsenal to break down wheat straw, a lignocellulosic substrate that is considered as a biomass feedstock worldwide. Results We performed integrative multi-omics analyses by combining data from the fungal genome, transcriptomes, and secretomes. We found that the fungus possessed an unexpectedly large set of genes coding for Class II peroxidases involved in lignin degradation (19 genes) and GMC oxidoreductases/dehydrogenases involved in generating the hydrogen peroxide required for lignin peroxidase activity and promoting redox cycling of the fungal enzymes involved in oxidative cleavage of lignocellulose polymers (36 genes). The examination of interrelated multi-omics patterns revealed that eleven Class II Peroxidases were secreted by the fungus during fermentation and eight of them where tightly co-regulated with redox cycling enzymatic partners. Conclusion As a peculiar feature of P. brumalis, we observed gene family extension, up-regulation and secretion of an abundant set of versatile peroxidases and manganese peroxidases, compared with other Polyporales species. The orchestrated secretion of an abundant set of these delignifying enzymes and redox cycling enzymatic partners could contribute to the delignification capabilities of the fungus. Our findings highlight the diversity of wood decay mechanisms present in Polyporales and the potentiality of further exploring this taxonomic order for enzymatic functions of biotechnological interest.},
doi = {10.1186/s13068-018-1198-5},
journal = {Biotechnology for Biofuels},
number = [1],
volume = [11],
place = {United States},
year = {2018},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Time-scale dynamics of proteome and transcriptome of the white-rot fungus Phlebia radiata: growth on spruce wood and decay effect on lignocellulose
journal, September 2016


Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay
journal, November 2013

  • Hori, Chiaki; Gaskell, Jill; Igarashi, Kiyohiko
  • Mycologia, Vol. 105, Issue 6
  • DOI: 10.3852/13-072

Multiplicity of enzymatic functions in the CAZy AA3 family
journal, February 2018

  • Sützl, Leander; Laurent, Christophe V. F. P.; Abrera, Annabelle T.
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 6
  • DOI: 10.1007/s00253-018-8784-0

A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach
journal, May 2001


New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Cytochrome P450 enzymes in the fungal kingdom
journal, January 2011

  • Črešnar, B.; Petrič, Š.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1814, Issue 1
  • DOI: 10.1016/j.bbapap.2010.06.020

Comparative and transcriptional analysis of the predicted secretome in the lignocellulose-degrading basidiomycete fungus Pleurotus ostreatus : Functional study of
journal, June 2016

  • Alfaro, Manuel; Castanera, Raúl; Lavín, José L.
  • Environmental Microbiology, Vol. 18, Issue 12
  • DOI: 10.1111/1462-2920.13360

Fast solubilization of recalcitrant cellulosic biomass by the basidiomycete fungus Laetisaria arvalisinvolves successive secretion of oxidative and hydrolytic enzymes
journal, October 2014

  • Navarro, David; Rosso, Marie-Noëlle; Haon, Mireille
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/s13068-014-0143-5

A PCR-based method to quantify fungal growth during pretreatment of lignocellulosic biomass
journal, August 2015

  • Simeng, Zhou; Sacha, Grisel; Isabelle, Herpoël-Gimbert
  • Journal of Microbiological Methods, Vol. 115
  • DOI: 10.1016/j.mimet.2015.05.024

Variation in the chemical composition of wheat straw: the role of tissue ratio and composition
journal, August 2014

  • Collins, Samuel RA; Wellner, Nikolaus; Martinez Bordonado, Isabel
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/s13068-014-0121-y

A novel glucose dehydrogenase from the white-rot fungus Pycnoporus cinnabarinus: production in Aspergillus niger and physicochemical characterization of the recombinant enzyme
journal, June 2014

  • Piumi, François; Levasseur, Anthony; Navarro, David
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 24
  • DOI: 10.1007/s00253-014-5891-4

High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010

  • Gnerre, S.; MacCallum, I.; Przybylski, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
  • DOI: 10.1073/pnas.1017351108

Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose
journal, June 2016

  • Garajova, Sona; Mathieu, Yann; Beccia, Maria Rosa
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep28276

An alcohol oxidase of Phanerochaete chrysosporium with a distinct glycerol oxidase activity
journal, July 2014


Structural implications of the C-terminal tail in the catalytic and stability properties of manganese peroxidases from ligninolytic fungi
journal, November 2014

  • Fernández-Fueyo, Elena; Acebes, Sandra; Ruiz-Dueñas, Francisco J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 12
  • DOI: 10.1107/S1399004714022755

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Solid-state anaerobic digestion of fungal pretreated Miscanthus sinensis harvested in two different seasons
journal, June 2015


Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases
journal, January 2009

  • Ruiz-Duenas, F. J.; Morales, M.; Garcia, E.
  • Journal of Experimental Botany, Vol. 60, Issue 2
  • DOI: 10.1093/jxb/ern261

Phylogenetic and phylogenomic overview of the Polyporales
journal, November 2013

  • Binder, Manfred; Justo, Alfredo; Riley, Robert
  • Mycologia, Vol. 105, Issue 6
  • DOI: 10.3852/13-003

Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007


Activities of Secreted Aryl Alcohol Quinone Oxidoreductases from Pycnoporus cinnabarinus Provide Insights into Fungal Degradation of Plant Biomass
journal, February 2016

  • Mathieu, Yann; Piumi, Francois; Valli, Richard
  • Applied and Environmental Microbiology, Vol. 82, Issue 8
  • DOI: 10.1128/AEM.03761-15

Fungal Communities in Ancient Peatlands at Sanjiang Plain, China
journal, January 2017


Highly Efficient Production of Laccase by the Basidiomycete Pycnoporus cinnabarinus
journal, November 2004

  • Alves, Alexandra M. C. R.; Record, Eric; Lomascolo, Anne
  • Applied and Environmental Microbiology, Vol. 70, Issue 11, p. 6379-6384
  • DOI: 10.1128/AEM.70.11.6379-6384.2004

Extracellular electron transfer systems fuel cellulose oxidative degradation
journal, April 2016


Fungal pretreatment of lignocellulosic biomass
journal, November 2012


Visual Comparative Omics of Fungi for Plant Biomass Deconstruction
journal, August 2016


OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


A revised family-level classification of the Polyporales (Basidiomycota)
journal, September 2017


A Combined Transmembrane Topology and Signal Peptide Prediction Method
journal, May 2004

  • Käll, Lukas; Krogh, Anders; Sonnhammer, Erik L. L.
  • Journal of Molecular Biology, Vol. 338, Issue 5
  • DOI: 10.1016/j.jmb.2004.03.016

Fungal pretreatment of switchgrass for improved saccharification and simultaneous enzyme production
journal, May 2013


Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes
journal, November 2013

  • Ruiz-Dueñas, Francisco J.; Lundell, Taina; Floudas, Dimitrios
  • Mycologia, Vol. 105, Issue 6
  • DOI: 10.3852/13-059

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002


Biological wheat straw valorization: Multicriteria optimization of Polyporus brumalis pretreatment in packed bed bioreactor
journal, October 2017

  • Zhou, Simeng; Herpoël-Gimbert, Isabelle; Grisel, Sacha
  • MicrobiologyOpen, Vol. 7, Issue 1
  • DOI: 10.1002/mbo3.530

The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012


A survey of genes encoding H2O2-producing GMC oxidoreductases in 10 Polyporales genomes
journal, August 2015

  • Ferreira, P.; Carro, J.; Serrano, A.
  • Mycologia, Vol. 107, Issue 6
  • DOI: 10.3852/15-027

Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen
journal, March 2012


Effect of microbial pretreatment on enzymatic hydrolysis and fermentation of cotton stalks for ethanol production
journal, January 2009


Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

M-Coffee: combining multiple sequence alignment methods with T-Coffee
journal, March 2006


Genomics of wood-degrading fungi
journal, November 2014


Estimating Gene Gain and Loss Rates in the Presence of Error in Genome Assembly and Annotation Using CAFE 3
journal, May 2013

  • Han, Mira V.; Thomas, Gregg W. C.; Lugo-Martinez, Jose
  • Molecular Biology and Evolution, Vol. 30, Issue 8
  • DOI: 10.1093/molbev/mst100

Genome-Wide Annotation and Comparative Analysis of Cytochrome P450 Monooxygenases in Basidiomycete Biotrophic Plant Pathogens
journal, November 2015


Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis
journal, March 2012

  • Fernandez-Fueyo, E.; Ruiz-Duenas, F. J.; Ferreira, P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 14, p. 5458-5463
  • DOI: 10.1073/pnas.1119912109

Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000

  • Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren
  • Journal of Molecular Biology, Vol. 300, Issue 4
  • DOI: 10.1006/jmbi.2000.3903

Protein structure homology modeling using SWISS-MODEL workspace
journal, December 2008

  • Bordoli, Lorenza; Kiefer, Florian; Arnold, Konstantin
  • Nature Protocols, Vol. 4, Issue 1
  • DOI: 10.1038/nprot.2008.197

Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes
journal, January 2012

  • Moktali, Venkatesh; Park, Jongsun; Fedorova-Abrams, Natalie D.
  • BMC Genomics, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2164-13-525

Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus
journal, December 2015

  • Couturier, Marie; Navarro, David; Chevret, Didier
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0407-8

The COG database: an updated version includes eukaryotes
journal, January 2003

  • Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D.
  • BMC Bioinformatics, Vol. 4, Article No. 41
  • DOI: 10.1186/1471-2105-4-41

HMMER web server: interactive sequence similarity searching
journal, May 2011

  • Finn, R. D.; Clements, J.; Eddy, S. R.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr367

Independent evolution of four heme peroxidase superfamilies
journal, May 2015

  • Zámocký, Marcel; Hofbauer, Stefan; Schaffner, Irene
  • Archives of Biochemistry and Biophysics, Vol. 574
  • DOI: 10.1016/j.abb.2014.12.025

Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads
journal, January 2010


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
  • DOI: 10.1093/nar/gkt1183

The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown
journal, January 2014


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
  • DOI: 10.1073/pnas.1400592111

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

  • Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
  • Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
  • DOI: 10.1186/1754-6834-6-41

Transcriptional and Enzymatic Profiling of Pleurotus ostreatus Laccase Genes in Submerged and Solid-State Fermentation Cultures
journal, March 2012

  • Castanera, Raúl; Pérez, Gúmer; Omarini, Alejandra
  • Applied and Environmental Microbiology, Vol. 78, Issue 11
  • DOI: 10.1128/AEM.07880-11

    Works referencing / citing this record:

    The amazing potential of fungi: 50 ways we can exploit fungi industrially
    journal, July 2019