Genome of ‘ Ca. Desulfovibrio trichonymphae', an H ₂-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut

Abstract

The cellulolytic protist Trichonympha agilis in the termite gut permanently hosts two symbiotic bacteria, ‘ Candidatus Endomicrobium trichonymphae' and ‘ Candidatus Desulfovibrio trichonymphae'. The former is an intracellular symbiont, and the latter is almost intracellular but still connected to the outside via a small pore. The complete genome of ‘ Ca. Endomicrobium trichonymphae' has previously been reported, and we here present the complete genome of ‘ Ca. Desulfovibrio trichonymphae'. The genome is small (1 410 056 bp), has many pseudogenes, and retains biosynthetic pathways for various amino acids and cofactors, which are partially complementary to those of ‘ Ca. Endomicrobium trichonymphae'. An amino acid permease gene has apparently been transferred between the ancestors of these two symbionts; a lateral gene transfer has affected their metabolic capacity. Notably, ‘ Ca. Desulfovibrio trichonymphae' retains the complex system to oxidize hydrogen by sulfate and/or fumarate, while genes for utilizing other substrates common in desulfovibrios are pseudogenized or missing. Thus, ‘ Ca. Desulfovibrio trichonymphae' is specialized to consume hydrogen that may otherwise inhibit fermentation processes in both T. agilis and ‘ Ca. Endomicrobium trichonymphae'. The small pore may be necessary to take up sulfate. This study depicts a genome-based model of a multipartite symbiotic system within a cellulolytic protist cell in the termite gut.