Comparative genomics unravels a rich set of biosynthetic gene clusters with distinct evolutionary trajectories across fungal species (Termitomyces) farmed by termites.
Suzanne Schmidt, Robert Murphy, Joel Vizueta, Signe Kjærsgaard Schierbech, Benjamin H Conlon, Nina B Kreuzenbeck, Sabine M E Vreeburg, Lennart J J van de Peppel, Duur K Aanen, Kolotchèlèma S Silué, N'Golo A Kone, Christine Beemelmanns, Tilmann Weber, Michael Poulsen
Author Information
Suzanne Schmidt: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark. Suzanne.schmidt@bio.ku.dk. ORCID
Robert Murphy: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark.
Joel Vizueta: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark. ORCID
Signe Kjærsgaard Schierbech: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark.
Benjamin H Conlon: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark.
Nina B Kreuzenbeck: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans-Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
Sabine M E Vreeburg: Laboratory of Genetics, Wageningen University, 6700 AA, Wageningen, The Netherlands.
Lennart J J van de Peppel: Laboratory of Genetics, Wageningen University, 6700 AA, Wageningen, The Netherlands. ORCID
Duur K Aanen: Laboratory of Genetics, Wageningen University, 6700 AA, Wageningen, The Netherlands.
Kolotchèlèma S Silué: Unité de Formation et de Recherche Sciences de la Nature (UFR-SN), Laboratoire d'Ecologie et de Développement Durable (UREB), Université Nangui Abrogoua, Abidjan, Côte d'Ivoire.
N'Golo A Kone: Unité de Formation et de Recherche Sciences de la Nature (UFR-SN), Laboratoire d'Ecologie et de Développement Durable (UREB), Université Nangui Abrogoua, Abidjan, Côte d'Ivoire.
Christine Beemelmanns: Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology - Hans-Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany. ORCID
Tilmann Weber: The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark. ORCID
Michael Poulsen: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark. ORCID
The use of compounds produced by hosts or symbionts for defence against antagonists has been identified in many organisms, including in fungus-farming termites (Macrotermitinae). The obligate mutualistic fungus Termitomyces plays a pivotal role in plant biomass decomposition and as the primary food source for these termites. Despite the isolation of various specialized metabolites from different Termitomyces species, our grasp of their natural product repertoire remains incomplete. To address this knowledge gap, we conducted a comprehensive analysis of 39 Termitomyces genomes, representing 21 species associated with members of five termite host genera. We identified 754 biosynthetic gene clusters (BGCs) coding for specialized metabolites and categorized 660 BGCs into 61 biosynthetic gene cluster families (GCFs) spanning five compound classes. Seven GCFs were shared by all 21 Termitomyces species and 21 GCFs were present in all genomes of subsets of species. Evolutionary constraint analyses on the 25 most abundant GCFs revealed distinctive evolutionary histories, signifying that millions of years of termite-fungus symbiosis have influenced diverse biosynthetic pathways. This study unveils a wealth of non-random and largely undiscovered chemical potential within Termitomyces and contributes to our understanding of the intricate evolutionary trajectories of biosynthetic gene clusters in the context of long-standing symbiosis.
References
Curr Biol. 2021 Oct 11;31(19):4413-4421.e5
[PMID: 34403645]
