Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

Abstract

Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for the 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 is poorly characterized.Here we show that chemosynthetic symbionts of individual Bathymodiolus brooksi mussels constitute genetically isolated populations. 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. 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 conclude that bacterial colonization dynamics over the host life-cycle is thus an important determinant of population structure and genome evolution of horizontally transmitted symbionts.

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

“…In this study, we focused on selection on vertical transmission fidelity, and defined horizontal transmission as the process of picking up random microbes from the environment. However, we note that heritable control over horizontal transmission (Picazo et al 2019) (with variation among host genotypes in how faithfully they pick up the same microbes as their parent), results in essentially the same population-level outcomes as heritable control over vertical transmission. We thus expect selection on heritable horizontal transmission to be consistent with the presented results here.…”

“…C) Hosts may exert strong control over which microbes may infect, but maintain flexible associations with broader diversity of microbes than in scenarios illustrated in A or B. For example, deep sea mussels restrict acquisition to single bacterial species, but this bacterial species may vary across individuals and populations (Picazo et al 2019). Bacterial diversity is reduced within hosts, but variable across hosts.…”

The hidden pangenome: comparative genomics reveals pervasive diversity in symbiotic and free-living sulfur-oxidizing bacteria

“…Accumulating evidence suggests that there can be substantial subspecies diversity affecting function within environmental bacterial populations and microbiomes [6][7][8]. For example, populations of intracellular sulfuroxidizing symbionts of bathymodiolin mussels harbor extensive gene content diversity within single host individuals [9][10][11]. These and other observations suggest that subspecies variation in symbiotic populations may be far more widespread than currently known [9].…”

“…The metabolic diversity among free-living lineages [22,15,16,24], the intraspecific gene content variation within the mussel symbionts [9][10][11], and the range of different lifestyles observed within the Thioglobaceae family indicate an impressive versatility and genomic plasticity. However, to date, a comprehensive understanding of this variability is lacking, as most studies focus on either symbiotic lineages or the free-living.…”

Currency, Exchange, and Inheritance in the Evolution of Symbiosis

“…Thus, in symbiotic interactions with a mixed microbial community, where multiple strains harbor the core symbiont currency exchange mechanisms (e.g., [52]), functional redundancy may lead to a transient interaction rather than stable inheritance. In such symbioses, colonization history can result in alternative symbiont community composition that nonetheless secures the host requirements (e.g., [53]). From a hostcentric point of view, it is likely more informative to study the mechanisms and role of currency exchange rather than the specific symbiont strain identity.…”