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05, 2023;17 (5): 733-747.

Adaptations of Pseudoxylaria towards a comb-associated lifestyle in fungus-farming termite colonies.

Janis Fricke, Felix Schalk, Nina B Kreuzenbeck, Elena Seibel, Judith Hoffmann, Georg Dittmann, Benjamin H Conlon, Huijuan Guo, Z Wilhelm de Beer, Daniel Giddings Vassão, Gerd Gleixner, Michael Poulsen, Christine Beemelmanns
Author Information
  1. Janis Fricke: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  2. Felix Schalk: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  3. Nina B Kreuzenbeck: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  4. Elena Seibel: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  5. Judith Hoffmann: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  6. Georg Dittmann: Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Hans-Knöll-Straße 10, 07745, Jena, Germany.
  7. Benjamin H Conlon: Department of Biology, Section for Ecology and Evolution, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark. ORCID
  8. Huijuan Guo: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany.
  9. Z Wilhelm de Beer: Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Hatfield, 0028, Pretoria, South Africa.
  10. Daniel Giddings Vassão: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany. ORCID
  11. Gerd Gleixner: Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Hans-Knöll-Straße 10, 07745, Jena, Germany. ORCID
  12. Michael Poulsen: Department of Biology, Section for Ecology and Evolution, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark. ORCID
  13. Christine Beemelmanns: Group Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology-Hans Knöll Institute (HKI), Beutenbergstraße 11a, 07745, Jena, Germany. Christine.Beemelmanns@helmholtz-hips.de. ORCID
PMID: 36841903 DOI: 10.1038/s41396-023-01374-4

Abstract

Characterizing ancient clades of fungal symbionts is necessary for understanding the evolutionary process underlying symbiosis development. In this study, we investigated a distinct subgeneric taxon of Xylaria (Xylariaceae), named Pseudoxylaria, whose members have solely been isolated from the fungus garden of farming termites. Pseudoxylaria are inconspicuously present in active fungus gardens of termite colonies and only emerge in the form of vegetative stromata, when the fungus comb is no longer attended ("sit and wait" strategy). Insights into the genomic and metabolic consequences of their association, however, have remained sparse. Capitalizing on viable Pseudoxylaria cultures from different termite colonies, we obtained genomes of seven and transcriptomes of two Pseudoxylaria isolates. Using a whole-genome-based comparison with free-living members of the genus Xylaria, we document that the association has been accompanied by significant reductions in genome size, protein-coding gene content, and reduced functional capacities related to oxidative lignin degradation, oxidative stress responses and secondary metabolite production. Functional studies based on growth assays and fungus-fungus co-cultivations, coupled with isotope fractionation analysis, showed that Pseudoxylaria only moderately antagonizes growth of the termite food fungus Termitomyces, and instead extracts nutrients from the food fungus biomass for its own growth. We also uncovered that Pseudoxylaria is still capable of producing structurally unique metabolites, which was exemplified by the isolation of two novel metabolites, and that the natural product repertoire correlated with antimicrobial and insect antifeedant activity.

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MeSH Term

Animals
Isoptera
Biological Evolution
Acclimatization
Symbiosis
Fungi
Agriculture
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 14

Word Cloud

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