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Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts

Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics an...

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Autores principales: Rubin-Blum, Maxim, Antony, Chakkiath Paul, Sayavedra, Lizbeth, Martínez-Pérez, Clara, Birgel, Daniel, Peckmann, Jörn, Wu, Yu-Chen, Cardenas, Paco, MacDonald, Ian, Marcon, Yann, Sahling, Heiko, Hentschel, Ute, Dubilier, Nicole
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6474228/
https://www.ncbi.nlm.nih.gov/pubmed/30647460
http://dx.doi.org/10.1038/s41396-019-0346-7
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author Rubin-Blum, Maxim
Antony, Chakkiath Paul
Sayavedra, Lizbeth
Martínez-Pérez, Clara
Birgel, Daniel
Peckmann, Jörn
Wu, Yu-Chen
Cardenas, Paco
MacDonald, Ian
Marcon, Yann
Sahling, Heiko
Hentschel, Ute
Dubilier, Nicole
author_facet Rubin-Blum, Maxim
Antony, Chakkiath Paul
Sayavedra, Lizbeth
Martínez-Pérez, Clara
Birgel, Daniel
Peckmann, Jörn
Wu, Yu-Chen
Cardenas, Paco
MacDonald, Ian
Marcon, Yann
Sahling, Heiko
Hentschel, Ute
Dubilier, Nicole
author_sort Rubin-Blum, Maxim
collection PubMed
description Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host–symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea.
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spelling pubmed-64742282019-10-04 Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts Rubin-Blum, Maxim Antony, Chakkiath Paul Sayavedra, Lizbeth Martínez-Pérez, Clara Birgel, Daniel Peckmann, Jörn Wu, Yu-Chen Cardenas, Paco MacDonald, Ian Marcon, Yann Sahling, Heiko Hentschel, Ute Dubilier, Nicole ISME J Article Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host–symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea. Nature Publishing Group UK 2019-01-15 2019-05 /pmc/articles/PMC6474228/ /pubmed/30647460 http://dx.doi.org/10.1038/s41396-019-0346-7 Text en © The Author(s) 2019 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Rubin-Blum, Maxim
Antony, Chakkiath Paul
Sayavedra, Lizbeth
Martínez-Pérez, Clara
Birgel, Daniel
Peckmann, Jörn
Wu, Yu-Chen
Cardenas, Paco
MacDonald, Ian
Marcon, Yann
Sahling, Heiko
Hentschel, Ute
Dubilier, Nicole
Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title_full Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title_fullStr Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title_full_unstemmed Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title_short Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
title_sort fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6474228/
https://www.ncbi.nlm.nih.gov/pubmed/30647460
http://dx.doi.org/10.1038/s41396-019-0346-7
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