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The production of secondary metabolites, such as dipeptides, in certain coral species increases greatly under thermal stress and may serve as indications for coral bleaching.
Coral reefs cover over 255,000 km of the earth’s surface area and are crucial to the survival of millions of species (Williams et al. 2021). However, the increase in water temperatures due to global warming has placed these ecosystems in great danger due to a problem known as “coral bleaching”. Coral bleaching refers to when corals expel their symbionts under stress and take on a pale, white color in the process. The term symbiont refers to organisms that have a close physical association with one another that typically serves to benefit both species. Under normal, ambient, conditions, these algal symbiotic cells provide between 90 and 95% of the energetic requirements for their host corals (Williams et al. 2021). Together, these algal symbionts and the corals themselves are known as halobionts. During bleaching events, corals experience increased susceptibility to disease and decreases in growth and production rates since they are no longer receiving all the necessary metabolites from their symbiotic algal cells (Brown 1997). With these ideas in mind, researchers set out to identify diagnostic markers that might be used to predict coral bleaching events early on and be used to inform conservationists. Researchers were interested in changes in the amounts of metabolites produced by the holobiont since the exchange of metabolites is so crucial to the survivability of the corals. The researchers selected two specific species of coral, Montipora capitata and Pocivillopora acuta, because they display very different responses to thermal stress.
Nubbins from the two species were sampled from wild corals and subjected to heat stress for five weeks under the experimental condition. At the end of these experiments, more nubbins were taken from the same wild colonies to serve as the control. However, the bay from which the samples were taken experienced an unexpected warming even which led to thermal stress in the ambient, control condition as well. M. capitata visually appeared to be much less affected by this warming event compared to the other species, P. acuta, so the data from the M. capitata samples were given priority.
The experimenters first used hydrophilic interaction liquid chromatography (HILIC)-mass spectrometry (LC-MS) to identify thousands of polar metabolic features in the coral samples. The researchers also utilized a similar technique known as high-resolution LC-tandem MS (LC-MS2) to detect, quantify, and elucidate the structure of many secondary polar metabolites (Williams et al. 2021). One group of metabolites that were of particular interest to the researchers were montiporic acids (MAs) these compounds have many beneficial properties such as cytotoxicity, antimicrobial properties, and the ability to reduce photosynthetic competency of coral symbionts (Williams et al 2021). These were found in high abundance in the M. capitata which suggests that corals divert excessive amounts of resources to the production of secondary metabolites.
The polar metabolomic analysis mentioned above also revealed a handful of features that showed differential accumulation in the two species. Through further analysis, the researchers were able to determine that these features were dipeptides. Dipeptides are small molecules composed of two amino acids attached to one another and are given names based on the two amino acids that they are made of. The four dipeptides that were identified by the researchers included arginine-glutamine (RQ), lysine-glutamine (KQ), arginine-valine (RV), and arginine-alanine (RA). The accumulation of these dipeptides under heat stress was a robust result among all four colonies of corals that were sampled from (Williams et al. 2021).
After determining that these dipeptides accumulate under heat stress, the researchers developed a secondary hypothesis that the production of these dipeptides was co-regulated by the coral and symbiotic algal species and that they cluster under thermal stress. Using an average dipeptide by community (ADPC) score, the researchers were able to determine that these dipeptides were indeed co-regulated and that they increase in abundance in the coral holobiont under thermal stress compared to those in the ambient, control condition (Williams et al. 2021). These results indicate that the holobiont diverts an increased number of resources to create these dipeptides. Possible explanations for the accumulation in the thermally stressed corals is the fact that dipeptides are important sources of nitrogen for the algal symbiont that can be to generate energy via the tricarboxylic acid (TCA) cycle or metabolized in the purine pathway, as well as the fact that they serve as a potential response to oxygen stress (Williams et al. 2021).
Finally, the researchers investigated whether differences in dipeptides would be observed based on the presence of symbionts. Since it is difficult to obtain aposymbiotic corals, researchers used the sea anemone model Aiptasia. The results from these experiments showed differential accumulation in symbiotic populations compared to the aposymbiotic populations. These data suggest that these dipeptides played an important role in the evolution of the symbiotic relationship between these corals and their algal symbionts (Williams et al. 2021).
The identification of these metabolomic changes linked with thermal stress in coral holobionts is promising in the fact that they may be used in the future by conservationists to predict coral bleaching. However, much more research is required to identify whether these data can be extrapolated to other species of coral as the samples used in this experiment represent only two coral species from a handful of colonies. Another area of particular interest would be whether future findings and greater knowledge about the metabolite exchange between corals and their symbionts could be used to intervene and prevent or delay coral bleaching events.
Callen Davidson is currently enrolled at Davidson College. Contact him at cadavidson@davidson.edu.
References
Brown, B.E., 1997. Coral bleaching: causes and consequences. Coral Reefs 16, S129–S138. https://doi.org/10.1007/s003380050249
Smit, Nico. 2021. Coral Sea Life on the Great Barrier Reef [Photo] https://unsplash.com/photos/pD8F9ATnQD0
Williams, A., Chiles, E.N., Conetta, D., Pathmanathan, J.S., Cleves, P.A., Putnam, H.M., Su, X., Bhattacharya, D., 2021. Metabolomic shifts associated with heat stress in coral holobionts. Science Advances 7, eabd4210. https://doi.org/10.1126/sciadv.abd4210
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