Comparative Genomic and Metabolomic Analysis of Termitomyces Species Provides Insights into the Terpenome of the Fungal Cultivar and the Characteristic Odor of the Fungus Garden of Macrotermes natalensis Termites

mSystems

Dirk Hoffmeister¹  Almuth Hammerbacher²  Jan W. Schwitalla³  Janis Fricke³  Elena Seibel³  Christine Beemelmanns³  Nina B. Kreuzenbeck³  Tobias G. Köllner⁴  Suzanne Schmidt⁵  Benjamin H. Conlon⁵  Michael Poulsen⁵ 

[1] Associated Group of Pharmaceutical Microbiology, Leibniz Institute for Natural Product Research and Infection Biology–Hans-Knöll Institute (HKI), Jena, Germany;Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa;Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology–Hans-Knöll Institute (HKI), Jena, Germany;Max Planck Institute for Chemical Ecology, Department of Biochemistry, Jena, Germany;Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark;

关键词: Termitomyces;    secondary metabolism;    symbiosis;    terpenes;   

DOI  :  10.1128/msystems.01214-21

来源: DOAJ

【 摘 要 】

ABSTRACT Macrotermitinae termites have domesticated fungi of the genus Termitomyces as food for their colony, analogously to human farmers growing crops. Termites propagate the fungus by continuously blending foraged and predigested plant material with fungal mycelium and spores (fungus comb) within designated subterranean chambers. To test the hypothesis that the obligate fungal symbiont emits specific volatiles (odor) to orchestrate its life cycle and symbiotic relations, we determined the typical volatile emission of fungus comb biomass and Termitomyces nodules, revealing α-pinene, camphene, and d-limonene as the most abundant terpenes. Genome mining of Termitomyces followed by gene expression studies and phylogenetic analysis of putative enzymes related to secondary metabolite production encoded by the genomes uncovered a conserved and specific biosynthetic repertoire across strains. Finally, we proved by heterologous expression and in vitro enzymatic assays that a highly expressed gene sequence encodes a rare bifunctional mono-/sesquiterpene cyclase able to produce the abundant comb volatiles camphene and d-limonene. IMPORTANCE The symbiosis between macrotermitinae termites and Termitomyces is obligate for both partners and is one of the most important contributors to biomass conversion in the Old World tropic’s ecosystems. To date, research efforts have dominantly focused on acquiring a better understanding of the degradative capabilities of Termitomyces to sustain the obligate nutritional symbiosis, but our knowledge of the small-molecule repertoire of the fungal cultivar mediating interspecies and interkingdom interactions has remained fragmented. Our omics-driven chemical, genomic, and phylogenetic study provides new insights into the volatilome and biosynthetic capabilities of the evolutionarily conserved fungal genus Termitomyces, which allows matching metabolites to genes and enzymes and, thus, opens a new source of unique and rare enzymatic transformations.

【 授权许可】

Unknown