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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Online Access: | https://doi.org/10.1038/s41396-019-0346-7 |
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ftzenodo:oai:zenodo.org:2587098 2024-09-15T18:24:26+00:00 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 Mac Donald, Ian Macron, Yann Sahling, Heiko Hentschel, Ute Dubilier, Nicole 2019-01-15 https://doi.org/10.1038/s41396-019-0346-7 unknown Zenodo https://www.nature.com/articles/s41396-019-0346-7?WT.feed_name=subjects_bacteria https://zenodo.org/communities/sponges https://zenodo.org/communities/eu https://doi.org/10.1038/s41396-019-0346-7 oai:zenodo.org:2587098 info:eu-repo/semantics/openAccess Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode The ISME Journal, (2019-01-15) deep-sea sponges asphalt seeps methane-oxidizing bacteria symbiosis European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES Grant Agreement No 340535 The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From Genome to the Environment BathyBiome 340535 info:eu-repo/semantics/article 2019 ftzenodo https://doi.org/10.1038/s41396-019-0346-7 2024-07-25T15:05:00Z 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. ACKNOWLEDGEMENTS The authors thank all individuals who helped during the R/V Meteor research cruise M114, including onboard technical and scientific personnel, the captain and crew, and the ROV MARUM-Quest team. We thank the Max Planck-Genome-Centre Cologne (http://mpgc.mpipz.mpg.de/home/) for generating the meta- genomic and the metatranscriptomic data used in this study, the Imaging Core Facility at the University of Würzburg, Germany for embedding of the TEM samples, the Central Microscopy unit at the University of Kiel, Germany for access to their electron microscope facilities, and Ralf Lendt (University of Hamburg) ... Article in Journal/Newspaper North Atlantic Zenodo The ISME Journal 13 5 1209 1225 |
institution |
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Zenodo |
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ftzenodo |
language |
unknown |
topic |
deep-sea sponges asphalt seeps methane-oxidizing bacteria symbiosis European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES Grant Agreement No 340535 The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From Genome to the Environment BathyBiome 340535 |
spellingShingle |
deep-sea sponges asphalt seeps methane-oxidizing bacteria symbiosis European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES Grant Agreement No 340535 The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From Genome to the Environment BathyBiome 340535 Rubin-Blum, Maxim Antony, Chakkiath Paul Sayavedra, Lizbeth Martínez-Pérez, Clara Birgel, Daniel Peckmann, Jörn Wu, Yu-Chen Cardenas, Paco Mac Donald, Ian Macron, Yann Sahling, Heiko Hentschel, Ute Dubilier, Nicole Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts |
topic_facet |
deep-sea sponges asphalt seeps methane-oxidizing bacteria symbiosis European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES Grant Agreement No 340535 The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From Genome to the Environment BathyBiome 340535 |
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. ACKNOWLEDGEMENTS The authors thank all individuals who helped during the R/V Meteor research cruise M114, including onboard technical and scientific personnel, the captain and crew, and the ROV MARUM-Quest team. We thank the Max Planck-Genome-Centre Cologne (http://mpgc.mpipz.mpg.de/home/) for generating the meta- genomic and the metatranscriptomic data used in this study, the Imaging Core Facility at the University of Würzburg, Germany for embedding of the TEM samples, the Central Microscopy unit at the University of Kiel, Germany for access to their electron microscope facilities, and Ralf Lendt (University of Hamburg) ... |
format |
Article in Journal/Newspaper |
author |
Rubin-Blum, Maxim Antony, Chakkiath Paul Sayavedra, Lizbeth Martínez-Pérez, Clara Birgel, Daniel Peckmann, Jörn Wu, Yu-Chen Cardenas, Paco Mac Donald, Ian Macron, 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 Mac Donald, Ian Macron, Yann Sahling, Heiko Hentschel, Ute Dubilier, Nicole |
author_sort |
Rubin-Blum, Maxim |
title |
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_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_sort |
fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts |
publisher |
Zenodo |
publishDate |
2019 |
url |
https://doi.org/10.1038/s41396-019-0346-7 |
genre |
North Atlantic |
genre_facet |
North Atlantic |
op_source |
The ISME Journal, (2019-01-15) |
op_relation |
https://www.nature.com/articles/s41396-019-0346-7?WT.feed_name=subjects_bacteria https://zenodo.org/communities/sponges https://zenodo.org/communities/eu https://doi.org/10.1038/s41396-019-0346-7 oai:zenodo.org:2587098 |
op_rights |
info:eu-repo/semantics/openAccess Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode |
op_doi |
https://doi.org/10.1038/s41396-019-0346-7 |
container_title |
The ISME Journal |
container_volume |
13 |
container_issue |
5 |
container_start_page |
1209 |
op_container_end_page |
1225 |
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1810464779701059584 |