A dynamic epibiont community associated with the bone eating worm Osedax

Abstract

Abstract 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.