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

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.

Development, Productivity, and Seasonality of Living Planktonic Foraminiferal Faunas and Limacina helicina in an Area of Intense Methane Seepage in the Barents Sea

“…It has also been hypothesized that CH 4 seepage can cause an increase in photosynthetic primary production (Pohlman et al, ), making CH 4 seepage areas CO 2 sinks. There have been several studies in the Arctic focusing on the effects of CH 4 seepage on the living benthic communities (Åström et al, , , ; Sen, Duperron, et al, , Sen et al, ), including living benthic foraminifera, although not exclusive to the Arctic region (Heinz et al, ; Herguera et al, ; Hill et al, ; Rathburn et al, ). However, no studies from the Arctic exist that examine the effects of CH 4 seepage on the pelagic ecosystem.…”

Frenulate siboglinids at high Arctic methane seeps and insight into high latitude frenulate distribution

“…Nodes with aLRT values greater than 0.8 are included or shown. Accession numbers: see Table and Sen, Duperron, et al, …”

“…The results of the molecular analyses demonstrate that the sampled pockmarks at Vestnesa Ridge contain two species of Oligobrachia . The presence of Oligobrachia overall is not surprising, since during sampling, the worms were seen to resemble this cryptic species complex based on overall body morphology (Sen, Duperron, et al, ). The more pertinent question was regarding the individual species itself.…”

“…This extends its distributional range to the high Arctic and shows it is not limited to the Norwegian Sea and that high latitude alone is not a barrier for dispersal and settlement. Instead, it appears to be a widespread species in northern regions, extending from the Nyegga/Storegga area in the Norwegian Sea (64°N) (Sen, Duperron, et al, ; Smirnov, ) to the Fram Strait (79°N) (Figure ). The specific sites that O. haakonmosbiensis is known from correspond exactly with northward flowing contour currents of Intermediate and Atlantic water (e.g., Hopkins, ).…”

“…It should further be noted that either of these species could correspond with the species Oligobrachia webbi found off the coast of Tromsø, northern Norway (Brattegard, ). This species is similar in morphology to both O. haakonmosbiensis and the CPL‐clade members, but the lack of both sequences and DNA‐extractable tissue has prevented molecular‐based identification (Sen, Duperron, et al, ). Therefore, high latitude seep frenulate species identifications presently exist for two distinct species: O. haakonmosbiensis and Oligobrachia sp.…”