Acetogenesis from H2plus CO2and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist

Abstract

Symbiotic associations of cellulolytic eukaryotic protists and diverse bacteria are common in the gut microbial communities of termites. Besides cellulose degradation by the gut protists, reductive acetogenesis from H2plus CO2and nitrogen fixation by gut bacteria play crucial roles in the host termites’ nutrition by contributing to the energy demand of termites and supplying nitrogen poor in their diet, respectively. Fractionation of these activities and the identification of key genes from the gut community of the wood-feeding termiteHodotermopsis sjoestedtirevealed that substantial activities in the gut—nearly 60% of reductive acetogenesis and almost exclusively for nitrogen fixation—were uniquely attributed to the endosymbiotic bacteria of the cellulolytic protist in the genusEucomonympha. The rod-shaped endosymbionts were surprisingly identified as a spirochete species in the genusTreponema, which usually exhibits a characteristic spiral morphology. The endosymbionts likely use H2produced by the protist for these dual functions. Although H2is known to inhibit nitrogen fixation in some bacteria, it seemed to rather stimulate this important mutualistic process. In addition, the single-cell genome analyses revealed the endosymbiont's potentials of the utilization of sugars for its energy requirement, and of the biosynthesis of valuable nutrients such as amino acids from the fixed nitrogen. These metabolic interactions are suitable for the dual functions of the endosymbiont and reconcile its substantial contributions in the gut.