Ecological differences among hydrothermal vent symbioses may drive contrasting patterns of symbiont population differentiation

ABSTRACT The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental, and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains, it is unknown how differences in ecological characteristics among host-symbiont associations influence the genomic structure of symbiont populations. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses. Bathymodiolus septemdierum lives in close symbiotic relationship with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with little exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum show structuring by geographic location, but that the dominant symbiont strain is uncorrelated with vent site. These patterns are in contrast to co-occurring Alviniconcha and Ifremeria gastropod symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. Our results suggest that relative habitat homogeneity combined with sufficient symbiont dispersal and genomic mixing might promote persistence of similar symbiont strains across geographic locations, while mixotrophy might decrease selective pressures on the host to affiliate with locally adapted symbiont strains. Overall, these data contribute to our understanding of the potential mechanisms influencing symbiont population structure across a spectrum of marine microbial symbioses that occupy contrasting ecological niches. IMPORTANCE Beneficial relationships between animals and microbial organisms (symbionts) are ubiquitous in nature. In the ocean, microbial symbionts are typically acquired from the environment and their composition across geographic locations is often shaped by adaptation to local habitat conditions. However, it is currently unknown how generalizable these patterns are across symbiotic systems that have contrasting ecological characteristics. To address this question, we compared symbiont population structure between deep-sea hydrothermal vent mussels and co-occurring but ecologically distinct snail species. Our analyses show that mussel symbiont populations are less partitioned by geography and do not demonstrate evidence for environmental adaptation. We posit that the mussel's mixotrophic feeding mode may lower its need to affiliate with locally adapted symbiont strains, while microhabitat stability and symbiont genomic mixing likely favors persistence of symbiont strains across geographic locations. Altogether, these findings further our understanding of the mechanisms shaping symbiont population structure in marine environmentally transmitted symbioses.