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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

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) for compound- specific carbon isotope measurements. We thank Bram Vekeman for providing the genomes from the MMG2 North Sea enrichments. The Campeche Knoll cruise was funded by the German Research Foun- dation (DFG – Deutsche Forschungsgemeinschaft). Additional support was provided through the MARUM DFG-Research Center/Excellence Cluster "The Ocean in the Earth System" at the University of Bremen. We are grateful to the Mexican authorities for granting permission to conduct this research in the southern Gulf of Mexico (permission of DGOPA: 02540/14 from 5 November 2014). This study was funded by the Max Planck Society, the MARUM DFG-Research Center/ Excellence Cluster "The Ocean in the Earth System" at the University of Bremen, an ERC Advanced Grant (BathyBiome, 340535) and a Gordon and Betty Moore Foundation Marine Microbial Initiative Investigator Award to ND (Grant GBMF3811), the DFG Collaborative Research Center 1182 'Origin and Function of Metaorganisms to UH and ND, and the European Union's Horizon 2020 research and innovation program to PC and UH under Grant Agreement No. 679849 ('SponGES'). CPA was supported by a postdoctoral fellow- ship from the Alexander von Humboldt Foundation. 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/. SUPPLEMENTARY INFORMATION The online version of this article (https:// doi.org/10.1038/s41396-019-0346-7) contains supplementary material, which is available to authorized users.
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