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Abstract

Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for bacterial ecology and evolution. Vertical symbiont transmission leads to geographic isolation of the microbial population and consequently to genetic isolation of microbiotas from individual hosts. In contrast, the extent of geographic and genetic isolation of horizontally transmitted microbiota and its consequences in shaping population pangenomes is poorly characterized. Here we show that chemosynthetic symbionts (Sulfur-oxidizing or SOX and Methane-oxidizing or MOX) of individual Bathymodiolus brooksi mussels constitute genetically isolated subpopulations. The reconstruction of core genome-wide strain sequences from high-resolution metagenomes revealed distinct phylogenetic clades. Nucleotide diversity and strain composition vary along the mussel lifespan, and individual hosts show a high degree of genetic isolation. By additionally reconstructing population pan genomes, we reveal that gene content differences between mussel symbiont communities reflect the differences in strain composition; thus, strains belonging to the same monophyletic group share most of their genes. Furthermore, for both symbionts, the accessory gene content is over-represented in functions related to genome integrity. Compared to SOX, the MOX pan-genome is larger and has a smaller fraction of accessory genes. We find that MOX contains more genes related to cell motility and mobile genetic elements. Altogether, our results suggest that the uptake of environmental bacteria is a restricted process in B. brooksi, where self-infection of the gill tissue results in serial founder effects during symbiont evolution. We suggest that this geographic isolation among symbiont populations from individual mussels limits the exposure of symbionts to mobile genetic elements. In addition, the differences between both species suggest that the two symbionts have different ecological traits, where the association of MOX with the host occurred more recently and has a more facultative character that may involve an active free-living phase. We conclude that bacterial colonization dynamics over the host life cycle are an important determinant of population structure and genome evolution of horizontally transmitted symbionts.