Species- and Caste-Specific Gut Metabolomes in Fungus-Farming Termites.

Nanna Hjort Vidkjær,Michael Poulsen,Christine Beemelmanns,Suzanne Schmidt,Kasun H Bodawatta,Haofu Hu

doi:10.3390/metabo11120839

Nanna Hjort Vidkjær, Michael Poulsen + Show 4 more

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https://doi.org/10.3390/metabo11120839

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Abstract

Fungus-farming termites host gut microbial communities that contribute to the pre-digestion of plant biomass for manuring the fungal mutualist, and potentially to the production of defensive compounds that suppress antagonists. Termite colonies are characterized by complex division of labor and differences in diet between termite size (minor and major) and morphological (worker and soldier) castes, and this extends to the composition of their gut microbial communities. We hypothesized that gut metabolomes should mirror these differences and tested this through untargeted LC-MS/MS analyses of three South African species of fungus-farming termites. We found distinct metabolomes between species and across castes, especially between soldiers and workers. Primary metabolites dominate the metabolomes and the high number of overlapping features with the mutualistic fungus and plant material show distinct impacts of diet and the environment. The identification of a few bioactive compounds of likely microbial origin underlines the potential for compound discovery among the many unannotated features. Our untargeted approach provides a first glimpse into the complex gut metabolomes and our dereplication suggests the presence of bioactive compounds with potential defensive roles to be targeted in future studies.

Highlights

Symbioses often include complex assemblies of organisms that affect each other’s ecology and evolution, potentially coevolve, and often encompass the production of chemical compounds that mediate signaling, digestive, or defensive roles [1,2,3]
To evaluate which chemical features contributed the most to the difference between termite species and castes, we used the variable importance in projections (VIP) acquired from the partial least squares discriminant analyses (PLS-DA) and one-way analyses of variance (ANOVA) performed in MetaboAnalyst 5.0
Due to the species-level differences, we investigated the significant differences between castes for each species separately in additional PLS-DAs and PERMANOVAs

Summary

Introduction

Symbioses often include complex assemblies of organisms that affect each other’s ecology and evolution, potentially coevolve, and often encompass the production of chemical compounds that mediate signaling, digestive, or defensive roles [1,2,3]. The most prominent community differences are associated with the termite host diet and primarily differ between soil-, wood-, and fungus-feeding termites [8,9]. The fungus-farming termite sub-family Macrotermitinae has engaged in a co-evolved obligate symbiosis with species in the fungal genus Termitomyces (Agari2caolfe1s9: Lyophyllaceae) for ca. The adoption of a primarily fungal diet remodeled farming termite gut bacterial community compositions [9,10,11], shifting the prominent role of plant

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