Revealing the metabolic capacity ofStreblomastix strixand its bacterial symbionts using single-cell metagenomics

Abstract

Lower termites harbor in their hindgut complex microbial communities that are involved in the digestion of cellulose. Among these are protists, which are usually associated with specific bacterial symbionts found on their surface or inside their cells. While these form the foundations of a classic system in symbiosis research, we still know little about the functional basis for most of these relationships. Here, we describe the complex functional relationship between one protist, the oxymonadStreblomastix strix, and its ectosymbiotic bacterial community using single-cell genomics. We generated partial assemblies of the hostS. strixgenome andCandidatusOrdinivivax streblomastigis, as well as a complex metagenome assembly of at least 8 other Bacteroidetes bacteria confirmed by ribosomal (r)RNA fluorescence in situ hybridization (FISH) to be associated withS. strix.Our data suggest thatS. strixis probably not involved in the cellulose digestion, but the bacterial community on its surface secretes a complex array of glycosyl hydrolases, providing them with the ability to degrade cellulose to monomers and fueling the metabolism ofS. strix. In addition, some of the bacteria can fix nitrogen and can theoretically provideS. strixwith essential amino acids and cofactors, which the protist cannot synthesize. On the contrary, most of the bacterial symbionts lack the essential glycolytic enzyme enolase, which may be overcome by the exchange of intermediates withS. strix. This study demonstrates the value of the combined single-cell (meta)genomic and FISH approach for studies of complicated symbiotic systems.