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

• Published in: The ISME Journal
• Main Authors: 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
• Format: Article in Journal/Newspaper
• Language: unknown
• Published: 2019
• Subjects: 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; North Atlantic
• Online Access: https://zenodo.org/record/2587098; https://doi.org/10.1038/s41396-019-0346-7

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) ...