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Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys

The environment around deep sea hydrothermal vents is characterized by an abundance of sulfur compounds, including toxic hydrogen sulfide. However, numerous communities of various invertebrates are found in it. It is suggested that invertebrates in the vicinity of hydrothermal vents detoxify sulfur...

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Autores principales: Koito, Tomoko, Ito, Yusuke, Suzuki, Akihiko, Tame, Akihiro, Ikuta, Tetsuro, Suzuki, Miwa, Mitsunobu, Satoshi, Sugimura, Makoto, Inoue, Koji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548688/
https://www.ncbi.nlm.nih.gov/pubmed/37789380
http://dx.doi.org/10.1186/s40851-023-00218-5
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author Koito, Tomoko
Ito, Yusuke
Suzuki, Akihiko
Tame, Akihiro
Ikuta, Tetsuro
Suzuki, Miwa
Mitsunobu, Satoshi
Sugimura, Makoto
Inoue, Koji
author_facet Koito, Tomoko
Ito, Yusuke
Suzuki, Akihiko
Tame, Akihiro
Ikuta, Tetsuro
Suzuki, Miwa
Mitsunobu, Satoshi
Sugimura, Makoto
Inoue, Koji
author_sort Koito, Tomoko
collection PubMed
description The environment around deep sea hydrothermal vents is characterized by an abundance of sulfur compounds, including toxic hydrogen sulfide. However, numerous communities of various invertebrates are found in it. It is suggested that invertebrates in the vicinity of hydrothermal vents detoxify sulfur compounds by biosynthesis of taurine-related compounds in the body. On the other hand, the vent endemic polychaete Alvinella pompejana has spherocrystals composed of sulfur and other metals in its digestive tract. It was considered that the spherocrystals contribute to the regulation of sulfur in body fluids. Paralvinella spp. and Polynoidae. gen. sp. live sympatrically and in areas most affected by vent fluid. In this study, we focused on the digestive tract of Paralvinella spp. and Polynoidae. gen. sp. to examine whether they have spherocrystals. We also investigated the possible involvement of bacteria in the digestive tract in spherulization. Examination with a scanning electron microscope (SEM) equipped with Energy Disperse X-ray Spectroscopy (EDS) detected spherocrystals containing sulfur and iron in the digestive tract of Paralvinella spp. In contrast, such spherocrystals were not observed in that of Polynoidae. gen. sp. although sulfur is detected there by inductively coupled plasma-optical emission spectrometry (ICP-OES). Meta-16S rRNA analysis indicated that the floras of the digestive tracts of the two species were very similar, suggesting that enteric bacteria are not responsible for spherocrystal formation. Analysis of taurine-related compounds indicated that the digestive tissues of Polynoidae. gen. sp. contain a higher amount of hypotaurine and thiotaurine than those of Paralvinella spp. Therefore, the two sympatric polychaetes use different strategies for controlling sulfur, i.e., Paralvinella spp. forms spherocrystals containing elemental sulfur and iron in the digestive tract, but Polynoidae. gen. sp. accumulates taurine-related compounds instead of spherocrystals. Such differences may be related to differences in their lifestyles, i.e., burrow-dweller or free-moving, or may have been acquired phylogenetically in the evolutionary process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-023-00218-5.
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spelling pubmed-105486882023-10-05 Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys Koito, Tomoko Ito, Yusuke Suzuki, Akihiko Tame, Akihiro Ikuta, Tetsuro Suzuki, Miwa Mitsunobu, Satoshi Sugimura, Makoto Inoue, Koji Zoological Lett Research Article The environment around deep sea hydrothermal vents is characterized by an abundance of sulfur compounds, including toxic hydrogen sulfide. However, numerous communities of various invertebrates are found in it. It is suggested that invertebrates in the vicinity of hydrothermal vents detoxify sulfur compounds by biosynthesis of taurine-related compounds in the body. On the other hand, the vent endemic polychaete Alvinella pompejana has spherocrystals composed of sulfur and other metals in its digestive tract. It was considered that the spherocrystals contribute to the regulation of sulfur in body fluids. Paralvinella spp. and Polynoidae. gen. sp. live sympatrically and in areas most affected by vent fluid. In this study, we focused on the digestive tract of Paralvinella spp. and Polynoidae. gen. sp. to examine whether they have spherocrystals. We also investigated the possible involvement of bacteria in the digestive tract in spherulization. Examination with a scanning electron microscope (SEM) equipped with Energy Disperse X-ray Spectroscopy (EDS) detected spherocrystals containing sulfur and iron in the digestive tract of Paralvinella spp. In contrast, such spherocrystals were not observed in that of Polynoidae. gen. sp. although sulfur is detected there by inductively coupled plasma-optical emission spectrometry (ICP-OES). Meta-16S rRNA analysis indicated that the floras of the digestive tracts of the two species were very similar, suggesting that enteric bacteria are not responsible for spherocrystal formation. Analysis of taurine-related compounds indicated that the digestive tissues of Polynoidae. gen. sp. contain a higher amount of hypotaurine and thiotaurine than those of Paralvinella spp. Therefore, the two sympatric polychaetes use different strategies for controlling sulfur, i.e., Paralvinella spp. forms spherocrystals containing elemental sulfur and iron in the digestive tract, but Polynoidae. gen. sp. accumulates taurine-related compounds instead of spherocrystals. Such differences may be related to differences in their lifestyles, i.e., burrow-dweller or free-moving, or may have been acquired phylogenetically in the evolutionary process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-023-00218-5. BioMed Central 2023-10-04 /pmc/articles/PMC10548688/ /pubmed/37789380 http://dx.doi.org/10.1186/s40851-023-00218-5 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Koito, Tomoko
Ito, Yusuke
Suzuki, Akihiko
Tame, Akihiro
Ikuta, Tetsuro
Suzuki, Miwa
Mitsunobu, Satoshi
Sugimura, Makoto
Inoue, Koji
Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title_full Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title_fullStr Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title_full_unstemmed Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title_short Difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
title_sort difference in sulfur regulation mechanism between tube-dwelling and free-moving polychaetes sympatrically inhabiting deep-sea hydrothermal chimneys
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548688/
https://www.ncbi.nlm.nih.gov/pubmed/37789380
http://dx.doi.org/10.1186/s40851-023-00218-5
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