TY - JOUR

T1 - The Termite Fungal Cultivar Termitomyces Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion

AU - Schalk, Felix

AU - Gostinčar, Cene

AU - Kreuzenbeck, Nina B.

AU - Conlon, Benjamin H.

AU - Sommerwerk, Elisabeth

AU - Rabe, Patrick

AU - Burkhardt, Immo

AU - Krüger, Thomas

AU - Kniemeyer, Olaf

AU - Brakhage, Axel A.

AU - Gunde-Cimerman, Nina

AU - de Beer, Z. Wilhelm

AU - Dickschat, Jeroen S.

AU - Poulsen, Michael

AU - Beemelmanns, Christine

N1 - Funding Information: This study was funded by the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation project ID 239748522-SFB 1127 [project A6] grant to C.B. and CRC/TR Funding Information: 124 FungiNet project no. 210879364 [projects A1 and Z2] grant to A.A.B. and O.K.), by the Danish Council for Independent Research (grant DFF-7014-00178), and by a European Research Council consolidator grant (771349) to M.P. C.G. and N.G.-C. acknowledge financial support from the state budget of the Slovenian Research Agency (research project J4-2549, research programs P1-0198 and P1-0170, Infrastructural Centre Mycosmo). Funding Information: This study was funded by the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation project ID 239748522-SFB 1127 [project A6] grant to C.B. and CRC/TR 124 FungiNet project no. 210879364 [projects A1 and Z2] grant to A.A.B. and O.K.), by the Danish Council for Independent Research (grant DFF-7014-00178), and by a European Research Council consolidator grant (771349) to M.P. C.G. and N.G.-C. acknowledge financial support from the state budget of the Slovenian Research Agency (research project J4-2549, research programs P1-0198 and P1-0170, Infrastructural Centre Mycosmo). Help with microscopy pictures by David Zopf is greatly appreciated (SFB 1127/2 ChemBioSys project no. 239748522 [project Z]). This paper was written with contributions from all authors. All authors have approved the final version. There are no conflicts of interest to declare. Publisher Copyright: © 2021 Schalk et al.

PY - 2021

Y1 - 2021

N2 - 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 termitefungus 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 (Fe21 1 H2O2 1 H1 ! Fe31 1OH 1 H2O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH2Q, 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. IMPORTANCE 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 Termitomyces also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistrybased 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.

AB - 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 termitefungus 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 (Fe21 1 H2O2 1 H1 ! Fe31 1OH 1 H2O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH2Q, 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. IMPORTANCE 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 Termitomyces also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistrybased 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.

KW - Biodegradation

KW - Lignin degradation

KW - Lignocellulose

KW - Metabolites

KW - Redox chemistry

KW - Redox proteins

KW - Secondary metabolism

KW - Symbiosis

KW - Termitomyces

U2 - 10.1128/mBio.03551-20

DO - 10.1128/mBio.03551-20

M3 - Journal article

C2 - 34126770

AN - SCOPUS:85109135733

VL - 12

JO - mBio

JF - mBio

SN - 2161-2129

IS - 3

M1 - e03551-20

ER -