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 genetic, environmental and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains in autotrophic symbioses, little is known about the processes shaping symbiont population structure in mixotrophic host-microbe associations where hosts are less dependent on symbiont function and fitness. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which belongs to the foundation fauna at deep-sea hydrothermal vents in the Western Pacific Ocean. Bathymodiolus septemdierum lives in close symbiotic association with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with less exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum are only weakly structured by geochemical habitat or geography and show elevated rates of homologous recombination, in contrast to co-occurring gastropod symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. These results suggest that relative habitat stability 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 the spectrum of obligate to facultative marine microbial symbioses.

Extracellular chemosymbiont populations in a shallow-water thyasirid clam potentially shaped by priority effect

“…The population structure of horizontally transmitted symbionts could be shaped by a series of factors, including host genetics, environmental factors, and geographic factors [98]. Based on the symbiont population variant data, we revealed almost no correlation between the mean fixation index F ST of pairwise symbiont population from each sampling site and environmental factors (i.e.…”