AbstractMicrobes perform critical functions in corals yet most knowledge is derived from the photic zone. Here, we discovered two mollicutes that dominate the microbiome of the deep-sea octocoral,Callogorgia delta,and reside in the mesoglea. These symbionts were abundant across the host’s range, absent in the water, and rare in sediments. The symbionts lack all known fermentative capabilities including glycolysis and can only generate energy from arginine provided by the coral host. Their genomes feature extensive mechanisms to interact with foreign DNA which may be indicative of their role in symbiosis. We erect the novel family Oceanoplasmataceae which includes these symbionts and others associated with four marine invertebrate phyla. Its exceptionally broad host range suggests that the diversity of this enigmatic family remains largely undiscovered. Oceanoplasmataceae genomes are the most highly reduced among mollicutes providing new insight into their reductive evolution and the roles of coral symbionts.