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

Abstract

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.

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

“…holobiont systems in which microbiome composition is not or only partially controlled: radiolarians and foraminiferans (both heterotrophic protist dwellers harboring endosymbiotic microalgae) are emerging as ecological models for unicellular photosymbiosis due to their ubiquitous presence in the world's oceans (Decelle et al 2015;. The discovery of deep-sea hydrothermal vents revealed symbioses of animals with chemosynthetic bacteria that have later been found in many other marine ecosystems (Dubilier et al 2008;Rubin-Blum et al 2019) and frequently exhibit high levels of metabolic and taxonomic diversity (Duperron et al 2008;Petersen et al 2016;Ponnudurai et al 2017). The cosmopolitan haptophyte Emiliania huxleyi, promoted by associated bacteria (Seyedsayamdost et al 2011;Segev et al 2016), produces key intermediates in the carbon and sulfur biogeochemical cycles, making it an important model phytoplankton species.…”

Oil seepage and carbonate formation: A case study from the southern Gulf of Mexico

“…Initial direct investigations of these phenomena in the southern Gulf of Mexico (GoM) were conducted in 2003 with the German research vessel R/V Sonne in the Bay of Campeche and along the Yucatan Shelf (Bohrmann & Schenck, ). The Bay of Campeche hosts the ‘Chapopote Asphalt Volcano’, characterized by extensive eruptions of liquid heavy hydrocarbons, widespread asphalt flows, sea floor gas hydrate deposits and diverse macrofaunal communities able to defy this putatively hostile environment (MacDonald et al ., ; Sahling et al ., ; Rubin‐Blum et al ., , ). Further investigation of this oil seep province during R/V Meteor Cruise 67 in 2006 (Bohrmann & Spieß, ) included detailed surveying and mapping of asphalt flows and seismic studies, as well as biogeochemical studies (Ding et al ., , ; Naehr et al ., ; Brüning et al ., ; Schubotz et al ., ,b; Marcon et al ., ).…”

“…Initial direct investigations of these phenomena in the southern Gulf of Mexico (GoM) were conducted in 2003 with the German research vessel R/V Sonne in the Bay of Campeche and along the Yucatan Shelf (Bohrmann & Schenck, 2004). The Bay of Campeche hosts the 'Chapopote Asphalt Volcano', characterized by extensive eruptions of liquid heavy hydrocarbons, widespread asphalt flows, sea floor gas hydrate deposits and diverse macrofaunal communities able to defy this putatively hostile environment (MacDonald et al, 2004;Sahling et al, 2016;Rubin-Blum et al, 2017, 2019.…”

Methylotrophy, alkane-degradation, and pigment production as defining features of the globally distributed yet-uncultured phylum Binatota

“…Finally, the occurrence and apparent wide distribution of members of the Binatota in sponges, particularly by the order Bin18, is notable, and could be attributed to the recognized nutritional-based symbiosis between sponges and hydrocarbon-degraders 77,78 , including methanotrophs 79 . This is especially true in deep-water sponges, where low levels of planktonic biomass restrict the amount of food readily acquired via lter feeding and hence biomass acquisition via methane and alkane oxidation is especially valuable.…”