Abstract
Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I–COI–), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. ‘mediterranea’) recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. ‘mediterranea’ to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.
Highlights
Osedax, commonly known as bone-eating worms, are a remarkable example of evolutionary adaptation to subsist on vertebrate bones [1]
Specimens (CRBA-33240–33245), preserved in glutaraldehyde/osmium tetroxide and dissected for TEM: CRBA-33240–33243, tubes with embryos inside; and CRBA-33244–33246, roots and transition between bone-roots
Our study confirms a broader range for Osedax deceptionensis in the shallow-waters of the Southern Ocean, by extending its current distribution to the Subantarctic waters of the South Georgia area
Summary
Commonly known as bone-eating worms, are a remarkable example of evolutionary adaptation to subsist on vertebrate bones [1]. Osedax females (and the males of O. priapus) live anchored to bones thanks to a ramified root system with an ovisac, obtaining nutrition via a unique symbiosis with Oceanospirillales gamma-proteobacteria [5,6,7]. These microorganisms, horizontally transmitted [7], are chemoorganoheterotrophic bacteria housed in bacteriocytes within the roots that degrade the organic compounds sequestered in the bone [5,6,7]. A recent analysis of the genome of two of the most dominant symbionts in Osedax has revealed their implication in degradation of proteins, likely originating from collagenous bone matrix [9]
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