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The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion

Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer....

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Autores principales: Schalk, Felix, Gostinčar, Cene, Kreuzenbeck, Nina B., Conlon, Benjamin H., Sommerwerk, Elisabeth, Rabe, Patrick, Burkhardt, Immo, Krüger, Thomas, Kniemeyer, Olaf, Brakhage, Axel A., Gunde-Cimerman, Nina, de Beer, Z. Wilhelm, Dickschat, Jeroen S., Poulsen, Michael, Beemelmanns, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262964/
https://www.ncbi.nlm.nih.gov/pubmed/34126770
http://dx.doi.org/10.1128/mBio.03551-20
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author Schalk, Felix
Gostinčar, Cene
Kreuzenbeck, Nina B.
Conlon, Benjamin H.
Sommerwerk, Elisabeth
Rabe, Patrick
Burkhardt, Immo
Krüger, Thomas
Kniemeyer, Olaf
Brakhage, Axel A.
Gunde-Cimerman, Nina
de Beer, Z. Wilhelm
Dickschat, Jeroen S.
Poulsen, Michael
Beemelmanns, Christine
author_facet Schalk, Felix
Gostinčar, Cene
Kreuzenbeck, Nina B.
Conlon, Benjamin H.
Sommerwerk, Elisabeth
Rabe, Patrick
Burkhardt, Immo
Krüger, Thomas
Kniemeyer, Olaf
Brakhage, Axel A.
Gunde-Cimerman, Nina
de Beer, Z. Wilhelm
Dickschat, Jeroen S.
Poulsen, Michael
Beemelmanns, Christine
author_sort Schalk, Felix
collection PubMed
description Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that Termitomyces employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that Termitomyces induces hydroquinone-mediated Fenton chemistry (Fe(2+) + H(2)O(2) + H(+) → Fe(3+) + (•)OH + H(2)O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH(2)Q, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect’s agricultural symbiosis is accomplished.
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spelling pubmed-82629642021-07-23 The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion Schalk, Felix Gostinčar, Cene Kreuzenbeck, Nina B. Conlon, Benjamin H. Sommerwerk, Elisabeth Rabe, Patrick Burkhardt, Immo Krüger, Thomas Kniemeyer, Olaf Brakhage, Axel A. Gunde-Cimerman, Nina de Beer, Z. Wilhelm Dickschat, Jeroen S. Poulsen, Michael Beemelmanns, Christine mBio Research Article Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that Termitomyces employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that Termitomyces induces hydroquinone-mediated Fenton chemistry (Fe(2+) + H(2)O(2) + H(+) → Fe(3+) + (•)OH + H(2)O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH(2)Q, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect’s agricultural symbiosis is accomplished. American Society for Microbiology 2021-06-15 /pmc/articles/PMC8262964/ /pubmed/34126770 http://dx.doi.org/10.1128/mBio.03551-20 Text en Copyright © 2021 Schalk et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Schalk, Felix
Gostinčar, Cene
Kreuzenbeck, Nina B.
Conlon, Benjamin H.
Sommerwerk, Elisabeth
Rabe, Patrick
Burkhardt, Immo
Krüger, Thomas
Kniemeyer, Olaf
Brakhage, Axel A.
Gunde-Cimerman, Nina
de Beer, Z. Wilhelm
Dickschat, Jeroen S.
Poulsen, Michael
Beemelmanns, Christine
The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title_full The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title_fullStr The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title_full_unstemmed The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title_short The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion
title_sort termite fungal cultivar termitomyces combines diverse enzymes and oxidative reactions for plant biomass conversion
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262964/
https://www.ncbi.nlm.nih.gov/pubmed/34126770
http://dx.doi.org/10.1128/mBio.03551-20
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