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Abstract BackgroundMarine symbioses are predominantly established through horizontal acquisition of microbial symbionts from the environment. However, genetic and functional comparisons of free-living populations of symbionts to their host-associated counterparts are sparse. Here, we assembled the first genomes of the chemoautotrophic gammaproteobacterial symbionts affiliated with the deep-sea snailAlviniconcha hesslerifrom two separate hydrothermal vent fields of the Mariana Back-Arc Basin. We used phylogenomic and population genomic methods to assess sequence and gene content variation between free-living and host-associated symbionts. ResultsOur phylogenomic analyses show that the free-living and host-associated symbionts ofA. hesslerifrom both vent fields are populations of monophyletic strains from a single species. Furthermore, genetic structure and gene content analyses indicate that these symbiont populations are differentiated by vent field rather than by lifestyle. ConclusionTogether, this work suggests that, despite the potential influence of host-mediated acquisition and release processes on horizontally transmitted symbionts, geographic isolation and/or adaptation to local habitat conditions are important determinants of symbiont population structure and intra-host composition. 

Abstract Mass mortality of marine animals due to volcanic ash deposition is present in the fossil record but has rarely been documented in real time. Here, using remotely-operated vehicle video footage and analysis of ash collected at the seafloor, we describe the devastating effect of the record-breaking 2022 Hunga submarine volcanic eruption on endangered and vulnerable snail and mussel species that previously thrived at nearby deep-sea hydrothermal vents. In contrast to grazing, scavenging, filter-feeding, and predatory vent taxa, we observed mass mortality, likely due to smothering during burial by thick ash deposits, of the foundation species, which rely on symbiotic chemosynthetic bacteria for the bulk of their nutrition. This is important for our broad understanding of the natural disturbance of marine ecosystems by volcanic eruptions and for predicting the effects of anthropogenic disturbance, like deep-sea mining, on these unique seafloor habitats. 

Abstract Chemosynthetic animal-microbe symbioses sustain hydrothermal vent communities in the global deep sea. In the Indo-Pacific Ocean, hydrothermal ecosystems are often dominated by gastropod species of the genus Alviniconcha, which live in association with chemosynthetic Gammaproteobacteria or Campylobacteria. While the symbiont genomes of most extant Alviniconcha species have been sequenced, no genome information is currently available for the gammaproteobacterial endosymbiont of Alviniconcha adamantis—a comparatively shallow living species that is thought to be the ancestor to all other present Alviniconcha lineages. Here, we report the first genome sequence for the symbiont of A. adamantis from the Chamorro Seamount at the Mariana Arc. Our phylogenomic analyses show that the A. adamantis symbiont is most closely related to Chromatiaceae endosymbionts of the hydrothermal vent snails Alviniconcha strummeri and Chrysomallon squamiferum, but represents a distinct bacterial species or possibly genus. Overall, the functional capacity of the A. adamantis symbiont appeared to be similar to other chemosynthetic Gammaproteobacteria, though several flagella and chemotaxis genes were detected, which are absent in other gammaproteobacterial Alviniconcha symbionts. These differences might suggest potential contrasts in symbiont transmission dynamics, host recognition, or nutrient transfer. Furthermore, an abundance of genes for ammonia transport and urea usage could indicate adaptations to the oligotrophic waters of the Mariana region, possibly via recycling of host- and environment-derived nitrogenous waste products. This genome assembly adds to the growing genomic resources for chemosynthetic bacteria from hydrothermal vents and will be valuable for future comparative genomic analyses assessing gene content evolution in relation to environment and symbiotic lifestyles.