Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps

PLoS One. 2018 Dec 28;13(12):e0209273. doi: 10.1371/journal.pone.0209273. eCollection 2018.

Abstract

We provide the first detailed identification of Barents Sea cold seep frenulate hosts and their symbionts. Mitochondrial COI sequence analysis, in combination with detailed morphological investigations through both light and electron microscopy was used for identifying frenulate hosts, and comparing them to Oligobrachia haakonmosbiensis and Oligobrachia webbi, two morphologically similar species known from the Norwegian Sea. Specimens from sites previously assumed to host O. haakonmosbiensis were included in our molecular analysis, which allowed us to provide new insight on the debate regarding species identity of these Oligobrachia worms. Our results indicate that high Arctic seeps are inhabited by a species that though closely related to Oligobrachia haakonmosbiensis, is nonetheless distinct. We refer to this group as the Oligobrachia sp. CPL-clade, based on the colloquial names of the sites they are currently known to inhabit. Since members of the Oligobrachia sp. CPL-clade cannot be distinguished from O. haakonmosbiensis or O. webbi based on morphology, we suggest that a complex of cryptic Oligobrachia species inhabit seeps in the Norwegian Sea and the Arctic. The symbionts of the Oligobrachia sp. CPL-clade were also found to be closely related to O. haakonmosbiensis symbionts, but genetically distinct. Fluorescent in situ hybridization and transmission electron micrographs revealed extremely dense populations of bacteria within the trophosome of members of the Oligobrachia sp. CPL-clade, which is unusual for frenulates. Bacterial genes for sulfur oxidation were detected and small rod shaped bacteria (round in cross section), typical of siboglinid-associated sulfur-oxidizing bacteria, were seen on electron micrographs of trophosome bacteriocytes, suggesting that sulfide constitutes the main energy source. We hypothesize that specific, local geochemical conditions, in particular, high sulfide fluxes and concentrations could account for the unusually high symbiont densities in members of the Oligrobrachia sp. CPL-clade.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arctic Regions
  • Bacteria* / genetics
  • Cold Temperature
  • DNA, Mitochondrial
  • Norway
  • Oceans and Seas
  • Phylogeny
  • Polychaeta / anatomy & histology
  • Polychaeta / microbiology*
  • Polychaeta / ultrastructure
  • RNA, Bacterial
  • RNA, Ribosomal, 16S
  • Symbiosis

Substances

  • DNA, Mitochondrial
  • RNA, Bacterial
  • RNA, Ribosomal, 16S

Grants and funding

This study was funded through the Centre for Arctic Gas Hydrate, Environment and Climate (CAGE) and the Research Council of Norway through its Centres of Excellence scheme, project number 223259, and an Aurora grant from the Research Council of Norway and Government of France to AS and AA. Processing of material from the Laptev Sea was partly funded by the RSF Grant 14-50-00095 and the RFBR Grant 18-05-60228. The publication charges for this article have been funded by a grant from the publication fund of UiT The Arctic University of Norway.