Termites have several levels of defense measures to protect this obligate nutritional symbiosis, starting with lower individual levels of hygiene measures to a higher collective level, also called social immunity. To propagate the food fungus, younger workers ingest plant material alongside with Termitomyces biomass and use excreted lignocellulose and spore-enriched feces to craft new fungus comb on which Termitomyces is able to thrive (Fig. Termitomyces is cultivated by workers in cork-like structures termed “fungus combs”, which are maintained in chambers located within the subterranean colony and are also known as “fungal gardens”. The Macrotermitinae are the only termite lineage to have acquired fungal symbionts from the genus Termitomyces (family Lyophyllaceae) as their food source. 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. 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.
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. Capitalizing on viable Pseudoxylaria cultures from different termite colonies, we obtained genomes of seven and transcriptomes of two Pseudoxylaria isolates. Insights into the genomic and metabolic consequences of their association, however, have remained sparse. 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). 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.
Characterizing ancient clades of fungal symbionts is necessary for understanding the evolutionary process underlying symbiosis development.
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