Tentacular team up: Deep partnerships between sea anemones and bacteria

With a newly discovered symbiosis between a hydrothermal vent anemone and chemosynthetic bacteria, deep in the Sea of Cortez, it is clear that we have much to learn about the sea around us
Published in Ecology & Evolution
Tentacular team up: Deep partnerships between sea anemones and bacteria
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BioMed Central
BioMed Central BioMed Central

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

Background 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. 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. Results A 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. Conclusion The 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.

The vast blue surface of the ocean… as far as the eye can see. Far away from the frenetic pace of humans. We have come to a place 80 miles off the coast of La Paz, Mexico to explore what lies beneath this thin ocean skin. In 2018, in collaboration with the Schmidt Ocean Institute (SOI), an interdisciplinary team of geologists, chemists, microbiologists and biologists embarked on a 21-day expedition aboard the R/V Falkor. The biologists on board hoped to witness a fascinating animal community in what is the largest habitat on Earth – the deep sea. Multibeam echosounders, magnetic instruments, and an autonomous underwater vehicle (AUV) equipped with sonars and seismic sensors were first deployed to gather broad information about the seafloor and form a big picture. Following, a remotely operated vehicle (ROV) named SuBastian, owned by SOI, conducted centimeter-scale resolution mapping using a low altitude survey system, employed for the first time at such deep depths, providing an unprecedented view of the geological and geochemical controls on animal communities at underwater volcanoes, known as hydrothermal vents. 

The biologists on our expedition aimed to investigate the density, distribution, diversity, and metabolism of organisms thriving at hydrothermal vents deep in the Pescadero Basin (3700 meters, or ~2.3 miles below). One of these vent fields was discovered in 2012 by scientists using drones that detected thermal anomalies and bottom features consistent with hydrothermal venting. These Pescadero Basin vents in the southernmost Gulf of California differ dramatically from nearby vent fields, most strikingly in their unusual animal communities, with many new species and numerous others found that were not expected to live in the area. Included in this group of unusual fauna was a very abundant white sea anemone that unexpectedly appeared to thrive very near to vigorously venting fluids.

This anemone species, named Ostiactis pearseae, was very abundant, living tucked in between 3-foot tall tubeworms and sulfide-oxidizing clams. Anemones normally capture either large prey using stinging harpoons or small particles suspended in seawater using sticky tentacles. Neither of these strategies appeared to be the primary mode of dining by O. pearseae. Further, we knew from past studies that animals in the areas of highest volcanic activity usually take advantage of chemical energy for their sustenance, rather than energy from the overlying sunlit ocean far above. Incredibly, as we detail in our recent paper published Jan 18, 2021 in BMC Biology, this anemone receives nutrition from bacteria living inside of their skin cells, that use the chemical compound hydrogen sulfide to fuel organic carbon production. This trick is all the more strange given that other related reef-building corals and anemones house symbionts in their digestive system, on the outside of their cells. Our understanding of this phenomenon was made possible by a collaboration among an international science team involving undergraduates and science faculty from both a small liberal arts college and several research universities, as well as scientists at the American Museum of Natural History in New York. We are very excited to revisit this site in October 2021 to explore unanswered questions about this extreme alliance between marine invertebrates and beneficial bacteria.

- Shana Goffredi (Occidental College) and Allison Miller (Schmidt Ocean Institute)

Photos copyright SOI. Contact sgoffredi at oxy.edu with questions or further inquiries about this work.

Goffredi, S.K., Motooka, C., Fike, D.A. et al. Mixotrophic chemosynthesis in a deep-sea anemone from hydrothermal vents in the Pescadero Basin, Gulf of California. BMC Biol 19, 8 (2021). https://doi.org/10.1186/s12915-020-00921-1

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