Deep-sea corals near cold seeps associate with chemoautotrophic bacteria that are related to the symbionts of cold seep and hydrothermal vent mussels

Cnidarians are known for their symbiotic relationships, yet no known association exists between corals and chemoautotrophic microbes. Deep-sea corals, which support diverse animal communities in the Gulf of Mexico, are often found on authigenic carbonate in association with cold seeps. Sulfur-oxidizing chemoautotrophic bacteria of the SUP05 cluster are dominant symbionts of bathymodiolin mussels at cold seeps and hydrothermal vents around the world and have also been found in association with sponges. Therefore, we investigated whether other basal metazoans, corals, also associate with bacteria of the SUP05 cluster and report here that such associations are widespread. This was unexpected because it has been proposed that cnidarians would not form symbioses with chemoautotrophic bacteria due to their high oxygen demand and their lack of specialized respiratory structures. We screened corals, water, and sediment for SUP05 using 16S metabarcoding and found SUP05 phylotypes associated with corals at high relative abundance (10 – 91%). These coral-associated SUP05 phylotypes were coral host specific, absent in water samples, and rare or not detected in sediment samples. The genome of one SUP05 phylotype associated with sp. type B3, contained the genetic potential to oxidize reduced sulfur compounds and fix carbon and these pathways were transcriptionally active. Finally, the relative abundance of this SUP05 phylotype was positively correlated with chemoautotrophically-derived carbon and nitrogen input into the coral holobiont based on stable carbon and nitrogen isotopic compositions. We propose that SUP05 may supplement the diet of its host coral through chemoautotrophy or may provide nitrogen, essential amino acids, or vitamins. This is the first documented association between a chemoautotrophic symbiont and a cnidarian, broadening the known symbioses of corals and may represent a novel interaction between coral communities and cold seeps.