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

Shana K Goffredi, Cambrie Motooka, David A. Fike, Luciana C Gusmão, Ekin Tilic, Greg W Rouse, Estefanía Rodríguez

Preprint posted on August 11, 2020 https://www.biorxiv.org/content/10.1101/2020.08.10.245456v1

Article now published in BMC Biology at http://dx.doi.org/10.1186/s12915-020-00921-1

Tentacular team-up: the first known symbiosis between chemotrophic bacteria and cnidarians allows this deep-sea duo to thrive at hydrothermal vents.

Selected by Sophia Friesen

Categories: ecology, zoology

Background and context:

To survive on the deep ocean floor, far from the sunlight that powers most of Earth’s food web, many organisms have adapted to use an alternate energy source: oxidization of electron donors, such as sulfides or hydrogen, which can be abundant at deep ocean thermal vents. Many marine invertebrates, including tube worms [1], mussels [2], and crabs [3], have taken advantage of this energy source via symbiosis with chemotrophic bacteria, which have the metabolic pathways required to use such unusual fuels. Given the number of times chemotrophic symbiosis has arisen, it is surprising that until now, there were no known instances within Cnidaria, a widespread and successful phylum of marine invertebrates which often symbiose with photosynthetic bacteria [4].

When the authors of this preprint observed dense crowds of the sea anemone Ostiactis pearseae in the newly discovered Pescadero Basin hydrothermal vent fields, they suspected that these cnidarians might partner with chemotrophic bacteria to derive nutrients from the vents. The researchers conducted isotope analysis of anemone tissues to confirm that they receive nutrients from a different source than their non-chemotrophic neighbors. They analyzed the bacterial DNA associated with the anemones, finding that unique types of sulfur-metabolizing bacteria are abundant in the anemone tissue. TEM of anemone tentacles showed that the bacteria are present inside specific cell types. The authors conclude that the anemones and bacteria are in a symbiotic relationship in which the bacteria provide nutrients derived from thermal vent chemicals, the first chemotrophic symbiosis identified in Cnidaria.

 

Key findings:

  1. Pescadero Basin O. pearseae have unusual isotope ratios, consistent with symbiosis with chemotrophs

In order to determine where the anemones gained nutrients from, the researchers analyzed the ratios of isotopes of carbon, nitrogen, and sulfur in the anemones’ tissues. Individual anemones had variable isotope ratios, but they generally contained much lower ratios of 13C, 15N, and 34S than nearby, non-chemotrophic anthozoans, which indicates that the O. pearseae anemones had a different strategy of gaining nutrients than their neighbors. Specifically, lower amounts of 34S suggest that the anemones might be receiving sulfur from sulfur-metabolizing bacteria, which preferentially use 32S rather than 34S. Organisms preferentially retain 15N, so this isotope tends to increase with increasing trophic level. Lower levels of 15N in the anemones are consistent with a nitrogen source lower on the food chain, such as chemotrophic bacteria, rather than the animal prey that nearby anthozoans feed upon.

 

  1. The anemones are associated with a unique bacterial community, mostly thiotrophic

Isotope analysis showed that the anemones received nutrients from an unusual source, potentially chemotrophic bacteria. The authors therefore analyzed the bacterial DNA present in anemone tissue to determine which clades of bacteria were associated with the anemones. They found that one clade of sulfide-oxidizing bacteria, the SUP05 clade within the family Thioglobaceae, consistently made up a majority of the bacterial community associated with the anemones, despite making up only about 6% of the bacterial community in the surrounding water. Additionally, the specific SUP05 phylotypes found in anemone tissue are unique to the anemones and absent from the surrounding environment, suggesting a symbiotic relationship. The researchers confirmed that the SUP05 bacteria in the anemones have a number of genes involved in sulfur metabolism, as well as nitrate reduction, which means that the bacteria are most likely thiotrophic and could potentially transfer sulfur, nitrogen, and carbon to the anemones.

 

  1. Anemones harbor SUP05 bacteria within tentacle epithelial cells

To identify how the bacteria were physically associated with the anemones, bacteria were labeled using hybridization chain reaction-FISH to strongly mark SUP05 rRNA, and anemone tissue was visualized using TEM. The bacteria were present in large numbers specifically inside the cells of the tentacle epidermis, and some were even seen in the process of being endocytosed, indicating that the bacteria do not simply passively accumulate on the surface of the anemones, but are actively and specifically transported into the tissue.

 

Why I liked this paper:

Deep sea vent communities provide insights into ecosystems that are so far removed from our own as to seem almost alien. They expand our views on what life can be. But they are also incredibly hard to study. Due to their remoteness and the difficulties of replicating such environmental conditions in the lab, researchers of such ecosystems cannot rely on the surfeit of tools available to model-organism researchers. However, the strategies used by the researchers here are powerful – for instance, isotope analysis of the anemones’ tissue clearly shows that they are receiving nutrients from an unusual source.

This paper also demonstrates the adaptability of life, not only between organisms but also within a single species. The anemone in this study, Ostiactis pearseae, varies considerably in tissue isotope ratios between individuals, indicating that some anemones are getting many of their nutrients through more traditional predation. Consistent with this, the anemones still have functional stinging cells with which to capture prey. Within this single species, there are incredibly different strategies to obtain resources, even in the extreme environment of the deep ocean.

 

Questions for the authors:

  1. You noted substantial variation in the percent of SUP05 bacteria in the bacterial communities of individual anemones, as well as differences in tissue isotope ratios between individuals. Were you able to run those two analyses on the same individual anemones, and if so, did you see any correlation between SUP05 prevalence and isotope lightness?
  2. The benefit the anemone gains from hosting thiotrophic bacteria is intuitive, but would you speculate on what advantage the bacteria gains from its association with the anemone?
  3. Studying such a remote ecosystem must present unusual difficulties. What unexpected challenges did you encounter in the course of this project?

 

References:

  1. López-García P, Gaill F, Moreira D (2002). “Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila.” Environmental Microbiology 4(4): 204-215. doi:10.1046/j.1462-2920.2002.00286.x
  2. Duperron S, Bergin C, Zielinski F, et al (2006). “A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environmental Microbiology 8(8): 1441-1447. https://doi.org/10.1111/j.1462-2920.2006.01038.x
  3. Goffredi SK, Jones WJ, Erhlich H, et al (2008). “Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta.” Environmental Microbiology 10(10): 2623-2634. https://doi.org/10.1111/j.1462-2920.2008.01684.x
  4. Muscatine L (1990). “The role of symbiotic algae in carbon and energy flux in reef corals.” Coral Reefs 25: 1-29.

Tags: anemone, chemotroph, hydrothermal vent, symbiosis

Posted on: 21st August 2020 , updated on: 24th August 2020

doi: https://doi.org/10.1242/prelights.24159

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Author's response

Shana Goffredi shared

You noted substantial variation in the percent of SUP05 bacteria in the bacterial communities of individual anemones, as well as differences in tissue isotope ratios between individuals. Were you able to run those two analyses on the same individual anemones, and if so, did you see any correlation between SUP05 prevalence and isotope lightness?

That is a great question. We did run the 2 analyses on the same animals, however since only a few tentacles were used to assess the presence and structure of the bacterial community, we cannot know for sure the ratio of host to symbiont, and therefore symbiont impact on nutrition.  In order to detect a correlation between SUP05 prevalence and isotope lightness, we would need to survey an entire anemone. This is a great idea, however, and since we are visiting these vents again in October 2021 we could certainly target the smaller specimens to do such a comparison.

The benefit the anemone gains from hosting thiotrophic bacteria is intuitive, but would you speculate on what advantage the bacteria gains from its association with the anemone?

This is also a very good question. The default is usually that the host provides a stable source of all metabolites required by the symbiont. Imagine being a tiny single-celled bacterium that needs both oxygen and sulfide, which don’t usually co-exist in the same parcel of water. Therefore, it might be advantageous to associate with a larger, more mobile animal surface, even if internal, in order to have a steady supply of both.

Studying such a remote ecosystem must present unusual difficulties. What unexpected challenges did you encounter in the course of this project?

So many challenges. The biggest is that we never know what we will discover and, thus, can’t realistically prepare for all sampling protocols and experimental set-ups. Based on our findings, which were not confirmed until we got back to our landlocked laboratories, we have new ideas for live animal-bacteria experiments to be conducted next year. Thankfully, albeit rarely, we will be able to revisit these amazing sites and these unique animals again. I’m so glad you mentioned the comparison to model-systems research. We are always jealous of the beautifully orchestrated experiments that one can perform when not onboard a moving research ship.

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