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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, 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

The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones.TeaserGenome reduction and adaptations for collagen digestion underpin the symbiosis of Osedax worms to exploit decaying bones.

Indirect development with an intermediate larva exists in all major animal lineages1, which makes larvae central to most scenarios of animal evolution2–11. Yet how larvae evolved remains disputed. Here we show that temporal shifts (that is, heterochronies) in trunk formation underpin the diversification of larvae and bilaterian life cycles. We performed chromosome-scale genome sequencing in the annelid Owenia fusiformis with transcriptomic and epigenomic profiling during the life cycles of this and two other annelids. We found that trunk development is deferred to pre-metamorphic stages in the feeding larva of O. fusiformis but starts after gastrulation in the non-feeding larva with gradual metamorphosis of Capitella teleta and the direct developing embryo of Dimorphilus gyrociliatus. Accordingly, the embryos of O. fusiformis develop first into an enlarged anterior domain that forms larval tissues and the adult head12. Notably, this also occurs in the so-called ‘head larvae’ of other bilaterians13–17, with which the O. fusiformis larva shows extensive transcriptomic similarities. Together, our findings suggest that the temporal decoupling of head and trunk formation, as maximally observed in head larvae, facilitated larval evolution in Bilateria. This diverges from prevailing scenarios that propose either co-option9,10 or innovation11 of gene regulatory programmes to explain larva and adult origins.