Promiscuous endosymbionts in deep-sea corals and crinoids are shaped by nitrogen cycling

Abstract

Crinoids are commonly associated with corals, but whether they physiologically interact is unclear. Like corals, crinoids host symbiotic microorganisms but little is known about the crinoid microbiome. Here, we reveal the microbiomes of the deep-sea corals Desmophyllum pertusum and Solenosmilia variabilis and, notably, their associated feather star crinoid, Koehlermetra (of the family Thalassometridae) in the Campos Basin, Brazil. We showed that the same endosymbiotic members of the families Endozoicomonadaceae and Nitrosopumilaceae interchangeably inhabit the internal and external structures of the corals and crinoid, indicating promiscuity in symbioses. The metagenome-assembled genome of the novel and dominant Endozoicomonas promiscua sp. nov. suggest that these symbionts may drive dissimilatory nitrate reduction to ammonia, which could be a source of energy for ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae. Thus, nitrogen cycling may determine the microorganisms that are hosted by deep-sea corals, which may be provided by their associated crinoids. These findings provide important insight about the complex ecological interactions that could lead to promiscuous symbiosis. TeaserDeep-sea corals and crinoids share symbiotic microbes that cycle nitrogen, potentially supporting each other in the nutrient-poor deep sea.