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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

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.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 themore » fungus during fermentation and eight of them where tightly co-regulated with redox cycling enzymatic partners.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:
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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); French National Agency for Research; Spanish Ministry of Economy, Industry and Competitiveness
OSTI Identifier:
1618746
Alternate Identifier(s):
OSTI ID: 1544020; OSTI ID: 1619092
Grant/Contract Number:  
AC02-05CH11231; BIO2017-86559-R
Resource Type:
Published Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Name: Biotechnology for Biofuels Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
Netherlands
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. Netherlands: N. p., 2018. Web. doi:10.1186/s13068-018-1198-5.
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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. Netherlands. https://doi.org/10.1186/s13068-018-1198-5
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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". Netherlands. https://doi.org/10.1186/s13068-018-1198-5.
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@article{osti_1618746,
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 = {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.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.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 = {Netherlands},
year = {Mon Jul 23 00:00:00 EDT 2018},
month = {Mon Jul 23 00:00:00 EDT 2018}
}
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https://doi.org/10.1186/s13068-018-1198-5
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