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

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...

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Published in:PLOS ONE
Main Authors: Sen, Arunima, Duperron, Sebastien, Hourdez, Stephane, Piquet, Berenice, Leger, Nelly, Gebruk, Andrey, Le Port, Anne-sophie, Svenning, Mette Marianne, Andersen, Ann C.
Format: Article in Journal/Newspaper
Language:English
Published: Public Library Science 2018
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Online Access:https://archimer.ifremer.fr/doc/00474/58537/61088.pdf
https://archimer.ifremer.fr/doc/00474/58537/61089.zip
https://doi.org/10.1371/journal.pone.0209273
https://archimer.ifremer.fr/doc/00474/58537/
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spelling ftarchimer:oai:archimer.ifremer.fr:58537 2023-05-15T14:55:45+02:00 Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps Sen, Arunima Duperron, Sebastien Hourdez, Stephane Piquet, Berenice Leger, Nelly Gebruk, Andrey Le Port, Anne-sophie Svenning, Mette Marianne Andersen, Ann C. 2018-12 application/pdf https://archimer.ifremer.fr/doc/00474/58537/61088.pdf https://archimer.ifremer.fr/doc/00474/58537/61089.zip https://doi.org/10.1371/journal.pone.0209273 https://archimer.ifremer.fr/doc/00474/58537/ eng eng Public Library Science https://archimer.ifremer.fr/doc/00474/58537/61088.pdf https://archimer.ifremer.fr/doc/00474/58537/61089.zip doi:10.1371/journal.pone.0209273 https://archimer.ifremer.fr/doc/00474/58537/ info:eu-repo/semantics/openAccess restricted use Plos One (1932-6203) (Public Library Science), 2018-12 , Vol. 13 , N. 12 , P. e0209273 (29p.) text Publication info:eu-repo/semantics/article 2018 ftarchimer https://doi.org/10.1371/journal.pone.0209273 2021-09-23T20:31:56Z 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. Article in Journal/Newspaper Arctic Barents Sea Norwegian Sea Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Arctic Barents Sea Norwegian Sea PLOS ONE 13 12 e0209273
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
description 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.
format Article in Journal/Newspaper
author Sen, Arunima
Duperron, Sebastien
Hourdez, Stephane
Piquet, Berenice
Leger, Nelly
Gebruk, Andrey
Le Port, Anne-sophie
Svenning, Mette Marianne
Andersen, Ann C.
spellingShingle Sen, Arunima
Duperron, Sebastien
Hourdez, Stephane
Piquet, Berenice
Leger, Nelly
Gebruk, Andrey
Le Port, Anne-sophie
Svenning, Mette Marianne
Andersen, Ann C.
Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
author_facet Sen, Arunima
Duperron, Sebastien
Hourdez, Stephane
Piquet, Berenice
Leger, Nelly
Gebruk, Andrey
Le Port, Anne-sophie
Svenning, Mette Marianne
Andersen, Ann C.
author_sort Sen, Arunima
title Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
title_short Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
title_full Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
title_fullStr Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
title_full_unstemmed Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps
title_sort cryptic frenulates are the dominant chemosymbiotrophic fauna at arctic and high latitude atlantic cold seeps
publisher Public Library Science
publishDate 2018
url https://archimer.ifremer.fr/doc/00474/58537/61088.pdf
https://archimer.ifremer.fr/doc/00474/58537/61089.zip
https://doi.org/10.1371/journal.pone.0209273
https://archimer.ifremer.fr/doc/00474/58537/
geographic Arctic
Barents Sea
Norwegian Sea
geographic_facet Arctic
Barents Sea
Norwegian Sea
genre Arctic
Barents Sea
Norwegian Sea
genre_facet Arctic
Barents Sea
Norwegian Sea
op_source Plos One (1932-6203) (Public Library Science), 2018-12 , Vol. 13 , N. 12 , P. e0209273 (29p.)
op_relation https://archimer.ifremer.fr/doc/00474/58537/61088.pdf
https://archimer.ifremer.fr/doc/00474/58537/61089.zip
doi:10.1371/journal.pone.0209273
https://archimer.ifremer.fr/doc/00474/58537/
op_rights info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1371/journal.pone.0209273
container_title PLOS ONE
container_volume 13
container_issue 12
container_start_page e0209273
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