Shaping the tripartite symbiosis: are termite microbiome functions directed by the environmentally acquired fungal cultivar?
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Microbiome assembly critically impacts the ability of hosts to access beneficial symbiont functions. Fungus-farming termites have co-evolved with a fungal cultivar as a primary food source and complex gut microbiomes, which collectively perform complementary degradation of plant biomass. A large subset of the bacterial community residing within termite guts are inherited (vertically transmitted) from parental colonies, while the fungal symbiont is, in most termite species, acquired from the environment (horizontally transmitted). It has remained unknown how the gut microbiota sustains incipient colonies prior to the acquisition of the fungal cultivar, and how, if at all, bacterial contributions are modulated by fungus garden establishment. Here, we test the latter by determining the composition and predicted functions of the gut microbiome using metabarcoding and shotgun metagenomics, respectively. We focus our functional predictions on bacterial carbohydrate-active enzyme and nitrogen cycling genes and verify compositional patterns of the former through enzyme activity assays. Our findings reveal that the vast majority of microbial functions are encoded in the inherited microbiome, and that the establishment of fungal gardens incurs only minor modulations of predicted bacterial capacities for carbohydrate and nitrogen metabolism. While we cannot rule out that other symbiont functions are gained post-fungus garden establishment, our findings suggest that fungus-farming termite hosts are equipped with a near-complete set of gut microbiome functions at the earliest stages of colony life. This inherited, incipient bacterial microbiome likely contributes to the high extent of functional specificity and coevolution observed between termite hosts, gut microbiomes, and the fungal cultivar.
Originalsprog | Engelsk |
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Artikelnummer | 44 |
Tidsskrift | Animal Microbiome |
Vol/bind | 6 |
Antal sider | 17 |
ISSN | 2524-4671 |
DOI | |
Status | Udgivet - 2024 |
Bibliografisk note
Funding Information:
We thank members of the Social and Symbiotic Evolution Group at the University of Copenhagen for constructive comments on a draft of this manuscript. We thank Mireille Vasseur-Cognet, David Sillam-Dusses, Z. Wilhelm de Beer, and Alain Robert for assistance with termite collections and establishment of incipient colonies. We thank Asta R\u00F8dsgaard-J\u00F8rgensen, Malte Storm Lau Schlosser, and Nadja Vive Iv\u00F8 Beier for help with AZCL assays. We are grateful to Sylvia Mathiasen for laboratory support, and Rafael da Costa for line drawings that we adjusted and used in figures. This work was funded by a Ph.D. stipend from the Department of Biology, University of Copenhagen to V.M.S., the International Human Frontier Science Program RGP0060/2018 to Mireille Vasseur-Cognet, and a European Research Council Consolidator Grant (ERC-CoG 771349) to M.P. V.MS. and A.C-M. were further supported by the Danish National Research Foundation Center for Evolutionary Hologenomics (DNRF 143).
Publisher Copyright:
© The Author(s) 2024.
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