Bone-Eating Worms Spread: Insights into Shallow-Water Osedax (Annelida, Siboglinidae) from Antarctic, Subantarctic, and Mediterranean Waters

PLoS One. 2015 Nov 18;10(11):e0140341. doi: 10.1371/journal.pone.0140341. eCollection 2015.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Annelida / classification
  • Annelida / genetics*
  • Annelida / microbiology
  • Aquatic Organisms
  • Bayes Theorem
  • Biological Evolution*
  • Bone and Bones / chemistry
  • Ecosystem
  • Electron Transport Complex IV / genetics
  • Female
  • Gammaproteobacteria / physiology
  • Histones / genetics
  • Male
  • Oceans and Seas
  • Phylogeny*
  • RNA, Ribosomal, 16S / genetics
  • RNA, Ribosomal, 18S / genetics
  • RNA, Ribosomal, 28S / genetics
  • Symbiosis
  • Vertebrates

Substances

  • Histones
  • RNA, Ribosomal, 16S
  • RNA, Ribosomal, 18S
  • RNA, Ribosomal, 28S
  • Electron Transport Complex IV

Grants and funding

This research received support from the Spanish Government, through the research project ACTIQUIM-II (CTM2010-17415/ANT) and through the environmental association S’Agulla Educació Mediambiental. G.W. Rouse thanks the captain and crew of RVIB Nathaniel B. Palmer Chief Scientist N.G. Wilson and the science participants during the cruise NBP13-03. This work was supported by award #1043749 from the National Science Foundation Office of Polar Programs to N.G. Wilson, G.W. Rouse and R.S. Burton.