Facultative chemosynthesis in a deep-sea anemone from hydrothermal vents in the Pescadero Basin, Gulf of California

Abstract

BackgroundNumerous deep-sea invertebrates have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to most animals. Despite success in nearly all marine habitats and their well-known associations with photosynthetic symbionts, Cnidaria remain one of the only phyla without a clear dependence on hydrothermal vents and reliance on chemosynthetic bacterial symbionts specifically. ResultsA new chemosynthetic symbiosis between the sea anemone Ostiactis pearseae (Daly & Gusmao, 2007) and intracellular bacteria was discovered at ~3700 m deep hydrothermal vents in the southern Pescadero Basin, Gulf of California. Unlike most sea anemones observed from chemically-reduced habitats, this species was observed in and amongst vigorously venting fluids, side-by-side with the chemosynthetic tubeworm Oasisia aff. alvinae. Individuals of O. pearseae displayed carbon, nitrogen, and sulfur tissue isotope values (average {delta}13C -29.1{per thousand}, {delta}15N 1.6{per thousand}, and {delta}34S -1.1{per thousand}) suggestive of a distinct nutritional strategy from conventional Actiniaria suspension feeding or prey capture. Molecular and microscopic evidence confirmed the presence of intracellular SUP05-related bacteria housed in the tentacle epidermis of O. pearseae specimens collected from 5 hydrothermally-active structures within two vent fields ~2 km apart. SUP05 bacteria dominated the O. pearseae bacterial community (64-96% of the total bacterial community based on 16S rRNA sequencing), but were not recovered from other nearby anemones, and were generally rare in the surrounding water (< 7% of the total community). Further, the specific Ostiactis-associated SUP05 phylotypes were not detected in the environment, indicating a specific association. Two unusual candidate bacterial phyla (the OD1 and BD1-5 groups) also appeared to associate exclusively with O. pearseae and may play a role in symbiont sulfur cycling. ConclusionOstiactis pearseae represents the first member of Cnidaria described to date to have a physical and nutritional alliance with chemosynthetic bacteria. The facultative nature of this symbiosis is consistent with the dynamic relationships formed by both the SUP05 bacterial group and Anthozoa. The advantages gained by appropriating metabolic and structural resources from each other presumably contribute to their striking abundance in the Pescadero Basin, at the deepest known hydrothermal vents in the Pacific Ocean.