Differences in cofactor, oxygen and sulfur requirements influence niche adaptation in deep-sea vesicomyid clam symbioses

Vertical transmission of bacterial endosymbionts is accompanied by virtually irreversible gene loss that can provide insights into adaptation to divergent ecological niches. While patterns of genome reduction have been well described in some terrestrial symbioses, they are less understood in marine systems where vertical transmission is relatively rare. The association between deep-sea vesicomyid clams and chemosynthetic Gammaproteobacteria is one example of maternally inherited symbioses in the ocean. Differences in nitrogen and sulfur physiology between the two dominant symbiont groups, Ca. Ruthia and Ca. Vesicomyosocius, have been hypothesized to influence niche exploitation, which likely affects gene content evolution in these symbionts. However, genomic data are currently limited to confirm this assumption. In the present study we sequenced and compared 11 vesicomyid symbiont genomes with existing assemblies for Ca. Vesicomyosocius okutanii and Ca. Ruthia magnifica. Our analyses indicate that the two vesicomyid symbiont groups have a common core genome related to chemosynthetic metabolism, but differ in their potential for nitrate respiration and flexibility to environmental sulfide concentrations. Moreover, Ca. Vesicomyosocius and Ca. Ruthia have different enzymatic requirements for cobalamin and nickel and show contrasting capacities to acquire foreign genetic material. Tests for site-specific positive selection in metabolic candidate genes imply that the observed physiological differences are adaptive and thus likely correspond to ecological niches available to each symbiont group. These findings highlight the role of niche differentiation in creating divergent paths of reductive genome evolution in vertically transmitted symbionts.