Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment.

Abstract

Previous studies have deciphered the genomic basis of host-symbiont metabolic complementarity in vestimentiferans, bathymodioline mussels, vesicomyid clams and Alviniconcha snails, yet little is known about the chemosynthetic symbiosis in Thyasiridae-a family of Bivalvia regarded as an excellent model in chemosymbiosis research due to their wide distribution in both deep-sea and shallow-water habitats. We report the first circular thyasirid symbiont genome, named Candidatus Ruthturnera sp. Tsphm01, with a size of 1.53 Mb, 1521 coding genes and 100% completeness. Compared to its free-living relatives, Ca. Ruthturnera sp. Tsphm01 genome is reduced, lacking components for chemotaxis, citric acid cycle and de novo biosynthesis of small molecules (e.g. amino acids and cofactors), indicating it is likely an obligate intracellular symbiont. Nevertheless, the symbiont retains complete genomic components of sulphur oxidation and assimilation of inorganic carbon, and these systems were highly and actively expressed. Moreover, the symbiont appears well-adapted to anoxic environment, including capable of anaerobic respiration (i.e. reductions of DMSO and nitrate) and possession of a low oxygen-adapted type of cytochrome c oxidase. Analysis of the host transcriptome revealed its metabolic complementarity to the incomplete metabolic pathways of the symbiont and the acquisition of nutrients from the symbiont via phagocytosis and exosome. By providing the first complete genome of reduced size in a thyasirid symbiont, this study enhances our understanding of the diversity of symbiosis that has enabled bivalves to thrive in chemosynthetic habitats. The resources will be widely used in phylogenetic, geographic and evolutionary studies of chemosynthetic bacteria and bivalves.