The Termite Fungal Cultivar Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion.
Felix Schalk, Cene Gostinčar, Nina B Kreuzenbeck, Benjamin H Conlon, Elisabeth Sommerwerk, Patrick Rabe, Immo Burkhardt, Thomas Krüger, Olaf Kniemeyer, Axel A Brakhage, Nina Gunde-Cimerman, Z Wilhelm de Beer, Jeroen S Dickschat, Michael Poulsen, Christine Beemelmanns
Author Information
Felix Schalk: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Cene Gostinčar: Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
Nina B Kreuzenbeck: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Benjamin H Conlon: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
Elisabeth Sommerwerk: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Patrick Rabe: Kekulé Institute of Organic Chemistry and Biochemistry, University of Bonn, Bonn, Germany.
Immo Burkhardt: Kekulé Institute of Organic Chemistry and Biochemistry, University of Bonn, Bonn, Germany.
Thomas Krüger: Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Olaf Kniemeyer: Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Axel A Brakhage: Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Nina Gunde-Cimerman: Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
Z Wilhelm de Beer: Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Hatfield, Pretoria, South Africa.
Jeroen S Dickschat: Kekulé Institute of Organic Chemistry and Biochemistry, University of Bonn, Bonn, Germany.
Michael Poulsen: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
Christine Beemelmanns: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.
Macrotermitine termites have domesticated fungi in the genus 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 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 induces hydroquinone-mediated Fenton chemistry (Fe + HO + H → Fe + OH + HO) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MHQ, 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. Fungus-growing termites have optimized the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a codiversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here, we provide genomic, transcriptomic, and enzymatic evidence that also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistry-based hydroquinone-catalyzed lignin degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms reveal new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.
