Abstract
BackgroundNumerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals. Despite success in nearly all marine habitats and their well-known associations with photosynthetic symbionts, Cnidaria remain one of the only phyla present in the deep-sea without a clearly documented example of dependence on chemosynthetic symbionts.ResultsA new chemosynthetic symbiosis between the sea anemone Ostiactis pearseae 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 suggestive of a nutritional strategy distinct from the suspension feeding or prey capture conventionally employed by sea anemones. 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 (Thioglobaceae) dominated the O. pearseae bacterial community, but were not recovered from other nearby anemones, and were generally rare in the surrounding water. 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) appear to associate exclusively with O. pearseae and may play a role in symbiont sulfur cycling.ConclusionThe Cnidarian Ostiactis pearseae maintains a physical and nutritional alliance with chemosynthetic bacteria. The mixotrophic nature of this symbiosis is consistent with what is known about other cnidarians and the SUP05 bacterial group, in that they both form dynamic relationships to succeed in nature. 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.
Highlights
Numerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals
The white actiniarian morphotype was identified as Ostiactis pearseae [5], based on anatomical, cnidae, and DNA sequencing of preserved polyps
Despite 40+ years of appreciation for chemosynthetic symbioses and the continued search for their occurrence in the most well-known habitats, Cnidaria have only very recently been shown to associate with chemoautorophic bacteria
Summary
Numerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals. They are found in all marine habitats at most depths and latitudes [3] Their worldwide ecological success may best be attributed to an ability to form symbiotic relationships with other organisms, including microbial eukaryotes (e.g., dinoflagellates in the family Symbiodiniaceae; [4]), as in the case of shallow-water tropical species. Anthozoa such as sea anemones, octocorals, and zoanthids are found in deep-sea reducing environments, such as hydrothermal vents, seeps, and whalefalls [5,6,7,8]; they have been historically understudied, and most remain undescribed. A recent study demonstrated an affiliation between sulfide-oxidizing SUP05 bacteria and certain species of Anthozoa found near deep-sea seeps, and hypothesized a facultative symbiosis based on molecular and isotopic evidence [9]
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