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, Sébastien, Hourdez, Stéphane, Piquet, Bérénice, Léger, Nelly, Gebruk, Andrey, Le Port, Anne-Sophie, Svenning, Mette Marianne, Andersen, Ann C.
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Language:English
Published: Public Library of Science 2018
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310283/
http://www.ncbi.nlm.nih.gov/pubmed/30592732
https://doi.org/10.1371/journal.pone.0209273
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spelling ftpubmed:oai:pubmedcentral.nih.gov:6310283 2023-05-15T14:55:50+02:00 Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps Sen, Arunima Duperron, Sébastien Hourdez, Stéphane Piquet, Bérénice Léger, Nelly Gebruk, Andrey Le Port, Anne-Sophie Svenning, Mette Marianne Andersen, Ann C. 2018-12-28 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310283/ http://www.ncbi.nlm.nih.gov/pubmed/30592732 https://doi.org/10.1371/journal.pone.0209273 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310283/ http://www.ncbi.nlm.nih.gov/pubmed/30592732 http://dx.doi.org/10.1371/journal.pone.0209273 © 2018 Sen et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. CC-BY Research Article Text 2018 ftpubmed https://doi.org/10.1371/journal.pone.0209273 2019-01-13T01:20:38Z 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. ... Text Arctic Barents Sea Norwegian Sea PubMed Central (PMC) Arctic Barents Sea Norwegian Sea PLOS ONE 13 12 e0209273
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Sen, Arunima
Duperron, Sébastien
Hourdez, Stéphane
Piquet, Bérénice
Léger, 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
topic_facet Research Article
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. ...
format Text
author Sen, Arunima
Duperron, Sébastien
Hourdez, Stéphane
Piquet, Bérénice
Léger, Nelly
Gebruk, Andrey
Le Port, Anne-Sophie
Svenning, Mette Marianne
Andersen, Ann C.
author_facet Sen, Arunima
Duperron, Sébastien
Hourdez, Stéphane
Piquet, Bérénice
Léger, 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 of Science
publishDate 2018
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310283/
http://www.ncbi.nlm.nih.gov/pubmed/30592732
https://doi.org/10.1371/journal.pone.0209273
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_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310283/
http://www.ncbi.nlm.nih.gov/pubmed/30592732
http://dx.doi.org/10.1371/journal.pone.0209273
op_rights © 2018 Sen et al
http://creativecommons.org/licenses/by/4.0/
This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1371/journal.pone.0209273
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