Summary Relationships fueled by sulfide between deep‐sea invertebrates and bacterial symbionts are well known, yet the diverse overlapping factors influencing symbiont specificity are complex. For animals that obtain their symbionts from the environment, both host identity and geographic location can impact the ultimate symbiont partner. Bacterial symbionts were analysed for three co‐occurring species each of Bathymodiolus mussels and vestimentiferan tubeworms, from three deep methane seeps off the west coast of Costa Rica. The bacterial internal transcribed spacer gene was analysed via direct and barcoded amplicon sequencing to reveal fine‐scale symbiont diversity. Each of the three mussel species (B. earlougheri, B. billschneideri and B. nancyschneideri) hosted genetically distinct thiotrophic endosymbionts, despite living nearly side‐by‐side in their habitat, suggesting that host identity is crucial in driving symbiont specificity. The dominant thiotrophic symbiont of co‐occurring tubeworms Escarpia spicata and Lamellibrachia (L. barhami and L. donwalshi), on the other hand, was identical regardless of host species or sample location, suggesting lack of influence by either factor on symbiont selectivity in this group of animals. These findings highlight the specific, yet distinct, influences on the environmental acquisition of symbionts in two foundational invertebrates with similar lifestyles, and provide a rapid, precise method of examining symbiont identities.

Osedax, the deep-sea annelid found at sunken whalefalls, is known to host Oceanospirillales bacterial endosymbionts intracellularly in specialized roots, that help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. During a 14-year study, we reveal a dynamic, yet persistent, succession of Campylobacterales integrated into the epidermis ofOsedax, that change over time as the whale carcass degrades on the sea floor. The Campylobacterales associated with seven species ofOsedax, which comprise 67% of the bacterial community on the trunk, are initially dominated by the genusArcobacter(at early time points < 24 months), theSulfurospirillumat intermediate stages (~ 50 months), and theSulfurimonasat later stages (>140 months) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests a transition from heterotrophy to autotrophy along the successional gradient, and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free living relatives, theOsedaxepibionts were highly enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with eukaryotic-like protein domains, suggesting a long evolutionary history with these enigmatic, yet widely distributed deep-sea worms.

Background Osedax, the deep-sea annelid found at sunken whalefalls, is known to host bacterial endosymbionts intracellularly in specialized roots, that help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. Here, we present an examination of the bacterial communities associated with the external surfaces of seven species of Osedax worms. Using molecular, metagenomic, and microscopy analyses we reveal a dynamic community of Campylobacterales epibionts associated with Osedax that are unique from close relatives and metabolically suited to different successional stages of whale decomposition. Results During this 14-year study, we reveal a dynamic, yet persistent, succession of Campylobacterales epibionts integrated into the epidermis of Osedax, that change over time as the whale carcass degrades on the sea floor. The epibionts associated with seven species of Osedax, which comprise 67% of the bacterial community on the trunk, are initially dominated by the genus Arcobacter (at early time points < 24 months), the Sulfurospirillum at intermediate stages (~ 50 months), and the Sulfurimonas at later stages (>140 months) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests a transition from heterotrophy to autotrophy along the successional gradient, and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free living relatives, the Osedax epibionts were highly enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with enriched effector proteins having eukaryotic-like domains. Conclusions Diverse bacteria form non-transient associations with the external surfaces of eukaryotes and can contribute to the health and physiology of their hosts. The recurrence of three Campylobacterales associated with diverse Osedaxspecies collected from multiple deep-sea locations suggests they are specific epibionts that share a long-evolutionary history with these enigmatic, yet widely distributed deep-sea worms. All three epibionts have an affinity for organic-rich and sulfide-rich habitats, however a successional shift in their composition reveals that they are a dynamic community that changes over time. These results provide evidence of a persistent yet dynamic relationship between Osedax and specific Campylobacterales epibionts that possess unique genomic features.

Osedax, the deep-sea annelid found at sunken whalefalls, is known to host Oceanospirillales bacterial endosymbionts intracellularly in specialized roots, which help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. During a 14-yr study, we reveal a dynamic, yet persistent, shift of Campylobacterales integrated into the epidermis of Osedax , which change over time as the whale carcass degrades on the sea floor. The Campylobacterales associated with seven species of Osedax , which comprise 67% of the bacterial community on the trunk, appear initially dominated by the genus Arcobacter (at early time points <24 mo), the Sulfurospirillum at intermediate stages (~50 mo), and the Sulfurimonas at later stages (>140 mo) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests potential for a transition from heterotrophy to autotrophy and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free-living relatives, the Osedax epibiont genomes were enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with eukaryotic-like protein (ELP) domains, suggesting a long evolutionary history with these enigmatic, yet widely distributed deep-sea worms. IMPORTANCE Symbiotic associations are widespread in nature and we can expect to find them in every type of ecological niche. In the last twenty years, the myriad of functions, interactions and species comprising microbe-host associations has fueled a surge of interest and appreciation for symbiosis. During this 14-year study, we reveal a dynamic population of bacterial epibionts, integrated into the epidermis of 7 species of a deep-sea worm group that feeds exclusively on the remains of marine mammals. The bacterial genomes provide clues of a long evolutionary history with these enigmatic worms. On the host surface, they exchange genes and appear to undergo ecological succession, as the whale carcass habitat degrades over time, similar to what is observed for some free-living communities. These, and other annelid worms are important keystone species for diverse deep-sea environments, yet the role of attached external bacteria in supporting host health has received relatively little attention.