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Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids
BACKGROUND: High latitude seeps are dominated by Oligobrachia siboglinid worms. Since these worms are often the sole chemosymbiotrophic taxon present (they host chemosynthetic bacteria within the trophosome organ in their trunk region), a key question in the study of high latitude seep ecology has b...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10236654/ https://www.ncbi.nlm.nih.gov/pubmed/37264469 http://dx.doi.org/10.1186/s42523-023-00251-x |
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author | Sen, Arunima Tanguy, Gwenn Galand, Pierre E. Andersen, Ann C. Hourdez, Stéphane |
author_facet | Sen, Arunima Tanguy, Gwenn Galand, Pierre E. Andersen, Ann C. Hourdez, Stéphane |
author_sort | Sen, Arunima |
collection | PubMed |
description | BACKGROUND: High latitude seeps are dominated by Oligobrachia siboglinid worms. Since these worms are often the sole chemosymbiotrophic taxon present (they host chemosynthetic bacteria within the trophosome organ in their trunk region), a key question in the study of high latitude seep ecology has been whether they harbor methanotrophic symbionts. This debate has manifested due to the mismatch between stable carbon isotope signatures of the worms (lower than -50‰ and usually indicative of methanotrophic symbioses) and the lack of molecular or microscopic evidence for methanotrophic symbionts. Two hypotheses have circulated to explain this paradox: (1) the uptake of sediment carbon compounds with depleted δC(13) values from the seep environment, and (2) a small, but significant and difficult to detect population of methanotrophic symbionts. We conducted 16S rRNA amplicon sequencing of the V3-V4 regions on two species of northern seep Oligobrachia (Oligobrachia webbi and Oligobrachia sp. CPL-clade), from four different high latitude sites, to investigate the latter hypothesis. We also visually checked the worms’ symbiotic bacteria within the symbiont-hosting organ, the trophosome, through transmission electron microscopy. RESULTS: The vast majority of the obtained reads corresponded to sulfide-oxidizers and only a very small proportion of the reads pertained to methane-oxidizers, which suggests a lack of methanotrophic symbionts. A number of sulfur oxidizing bacterial strains were recovered from the different worms, however, host individuals tended to possess a single strain, or sometimes two closely-related strains. However, strains did not correspond specifically with either of the two Oligobrachia species we investigated. Water depth could play a role in determining local sediment bacterial communities that were opportunistically taken up by the worms. Bacteria were abundant in non-trophosome (and thereby symbiont-free) tissue and are likely epibiotic or tube bacterial communities. CONCLUSIONS: The absence of methanotrophic bacterial sequences in the trophosome of Arctic and north Atlantic seep Oligobrachia likely indicates a lack of methanotrophic symbionts in these worms, which suggests that nutrition is sulfur-based. This is turn implies that sediment carbon uptake is responsible for the low δ(13)C values of these animals. Furthermore, endosymbiotic partners could be locally determined, and possibly only represent a fraction of all bacterial sequences obtained from tissues of these (and other) species of frenulates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00251-x. |
format | Online Article Text |
id | pubmed-10236654 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-102366542023-06-03 Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids Sen, Arunima Tanguy, Gwenn Galand, Pierre E. Andersen, Ann C. Hourdez, Stéphane Anim Microbiome Research BACKGROUND: High latitude seeps are dominated by Oligobrachia siboglinid worms. Since these worms are often the sole chemosymbiotrophic taxon present (they host chemosynthetic bacteria within the trophosome organ in their trunk region), a key question in the study of high latitude seep ecology has been whether they harbor methanotrophic symbionts. This debate has manifested due to the mismatch between stable carbon isotope signatures of the worms (lower than -50‰ and usually indicative of methanotrophic symbioses) and the lack of molecular or microscopic evidence for methanotrophic symbionts. Two hypotheses have circulated to explain this paradox: (1) the uptake of sediment carbon compounds with depleted δC(13) values from the seep environment, and (2) a small, but significant and difficult to detect population of methanotrophic symbionts. We conducted 16S rRNA amplicon sequencing of the V3-V4 regions on two species of northern seep Oligobrachia (Oligobrachia webbi and Oligobrachia sp. CPL-clade), from four different high latitude sites, to investigate the latter hypothesis. We also visually checked the worms’ symbiotic bacteria within the symbiont-hosting organ, the trophosome, through transmission electron microscopy. RESULTS: The vast majority of the obtained reads corresponded to sulfide-oxidizers and only a very small proportion of the reads pertained to methane-oxidizers, which suggests a lack of methanotrophic symbionts. A number of sulfur oxidizing bacterial strains were recovered from the different worms, however, host individuals tended to possess a single strain, or sometimes two closely-related strains. However, strains did not correspond specifically with either of the two Oligobrachia species we investigated. Water depth could play a role in determining local sediment bacterial communities that were opportunistically taken up by the worms. Bacteria were abundant in non-trophosome (and thereby symbiont-free) tissue and are likely epibiotic or tube bacterial communities. CONCLUSIONS: The absence of methanotrophic bacterial sequences in the trophosome of Arctic and north Atlantic seep Oligobrachia likely indicates a lack of methanotrophic symbionts in these worms, which suggests that nutrition is sulfur-based. This is turn implies that sediment carbon uptake is responsible for the low δ(13)C values of these animals. Furthermore, endosymbiotic partners could be locally determined, and possibly only represent a fraction of all bacterial sequences obtained from tissues of these (and other) species of frenulates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00251-x. BioMed Central 2023-06-01 /pmc/articles/PMC10236654/ /pubmed/37264469 http://dx.doi.org/10.1186/s42523-023-00251-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Sen, Arunima Tanguy, Gwenn Galand, Pierre E. Andersen, Ann C. Hourdez, Stéphane Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title | Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title_full | Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title_fullStr | Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title_full_unstemmed | Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title_short | Bacterial symbiont diversity in Arctic seep Oligobrachia siboglinids |
title_sort | bacterial symbiont diversity in arctic seep oligobrachia siboglinids |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10236654/ https://www.ncbi.nlm.nih.gov/pubmed/37264469 http://dx.doi.org/10.1186/s42523-023-00251-x |
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