Written by Sara Gagliardi
Edited by Tim Bateman
All organisms, from microbes to plants and animals, produce biogenic volatile organic compounds (BVOCs). Most are considered secondary metabolites that mediate the ecological interactions of the organism, responsible for its odor, scents, perfumes, and pollutants. Furthermore, BVOCs function as osmolytes and antioxidants, aid in the dissipation of excess energy, and assist in thermotolerance. Terrestrial studies have demonstrated that the production of BVOCs plays a role in the ecophysiological response of organisms to abiotic stress, pathogen and grazing defences, inter- and intra-species communication, and climate regulation. The release of BVOCs is an indicator for the health of ecosystems because this production is regulated by biological processes intended to assist the physiological tolerance of organisms.
Despite their important function in regulating ecosystem health, the role of BVOCs in coral reefs remains largely unknown. However, the Great Barrier Reef (GBR, Australia) is one of the major sources of aerosols derived from BVOCs, which play a role in climate regulation by reacting with and influencing the presence of hydroxyl radicals, nitrogen oxides and ozone formation in the atmosphere (Fig. 1), as well as influencing cloud formation and albedo. Moreover, it is possible that the production of BVOCs in heat stressed corals plays a role as infochemicals for the attraction of pathogenic bacteria, further decreasing the health of corals.
At the University of Technology Sydney (Australia), Caitlin Lawson’s research shows that the corals produce an assortment of secondary metabolites, including BVOCs, to reduce the detrimental health impacts of heat stress. Indeed, elevated seawater temperature increases reactive oxygen species (ROS) production, and is the main driver of coral bleaching.
The species-specific assortment of BVOCs produced by a coral is called the volatilome, which remains largely uncharacterized and is influenced by environmental factors such as the seawater temperature. In her latest research (1), Lawson described the volatilome of two reef-building coral species of the GBR, Acropora intermedia and Pocillopora damicornis, in ambient and heat-stressed temperature conditions. Her aims were to identify a ‘core’ volatilome, that is shared by the two coral species and remained stable under the two different treatments, and to highlight the shift in the volatilome composition in response to seawater temperature increase.
Coral fragments (nubbins) of healthy colonies of A. intermedia and P. damicornis were collected from the GBR, and heat stress was induced by exposure to 32°C seawater. When heat-treated nubbins started to show severe signs of heat stress, volatilome BVOCs were sampled by placing nubbins in a gas tight chamber (Fig. 2). The samples were collected using thermal desorption (TD) tubes, treated to concentrate compounds, and analysed on a gas chromatography–mass spectrometry (GC-MS) machine for the detection and identification of compounds. Subsequently, each identified compound was classified into four categories: climate activity, stress response, signalling, and antimicrobial.
Results showed that A. intermedia and P. damicornis produced a total of 87 BVOCs. The ecophysiological functions of the coral volatilome under ambient temperature conditions were mostly assigned to the antimicrobial and climatic categories. However, the coral response to heat stress resulted in the decline of BVOC emissions’ diversity, abundance and functional potential. The diversity of the volatilomes decreased by 42% for A. intermedia and by 62% for P. damicornis, with all four functional categories (climatically active, stress response, signalling and antimicrobial) decreasing their potential to assist coral health. The reduced diversity can be explained by the downregulation of BVOC synthesis, their reactivity with other metabolites, or the increase in their metabolization within the holobiont.
The ‘core’ volatilome, shared by the two coral species and remaining stable during heat stress, was composed of two brominated compounds (bromoform and chlorodibromomethane), suggested to be produced by the coral or as a result of the interactions with its associated microbiome, and an unclassified halogenated hydrocarbon. Halogenated hydrocarbons were previously shown to be produced by Symbiodiniaceae (2) and their associated bacteria (3), and might play a role in the mitigation of oxidative stress and ROS production.
Among A. intermedia under heat stress, only three compounds increased their abundance, while five compounds, associated with signaling function and antioxidant activity, were only detected in these conditions. These patterns indicate increased communication within the holobiont and the need to prevent the production of ROS in response to elevated temperature.
Toluene emissions, likely produced as a byproduct of photosynthesis (4), decreased among P. damicornis under heat stress, correlating with the heat stress induced decline of photosynthetic algae. Furthermore, the species did not produce dimethyl sulfide (DMS) emissions, precluding its use as a suitable biomarker. Indeed, DMS has been used as a stress biomarker in coral reefs, as it is highly produced by corals and is known to play a role in the climate regulation and impact the tolerance of the coral holobiont to stress.
Finally, isoprene emissions did not vary with species, time or treatments, but its oxidized forms were detected in higher concentrations in P. damicornis grown under ambient temperature. Isoprene has an important role in the protection of the photosynthetic apparatus against ROS, observed in many plant species, and as a key metabolite of marine microbes. However, further investigations are needed to understand whether isoprene is oxidized by the corals, and sampling methods need to be improved —e.g., use of real-time analyses during heat stress.
In conclusion, the study of coral volatilomes opens up for important research in terms of climate change and coral reef resilience. Indeed, BVOC production could aid coral heat tolerance, and their emissions into the water and atmosphere could depict tropical coral reefs as a major hotspot for climate regulation.
References
- Lawson, C. A., Raina, J.-B., Deschaseaux, E., Hrebien, V., Possell, M., Seymour, J. R., & Suggett, D. J. (2021). Heat stress decreases the diversity, abundance and functional potential of coral gas emissions. Global Change Biology, 27(4), 879–891. https://doi.org/10.1111/gcb.15446
- Lawson, C. A., Possell, M., Seymour, J. R., Raina, J.-B., & Suggett, D. J. (2019). Coral endosymbionts (Symbiodiniaceae) emit species-specific volatilomes that shift when exposed to thermal stress. Scientific Reports, 9(1), 17395. https://doi.org/10.1038/s41598-019-53552-0
- Lawson, C. A., Seymour, J. R., Possell, M., Suggett, D. J., & Raina, J.-B. (2020). The Volatilomes of Symbiodiniaceae-Associated Bacteria Are Influenced by Chemicals Derived From Their Algal Partner. Frontiers in Marine Science, 7. https://doi.org/10.3389/fmars.2020.00106
- Misztal, P. K., Hewitt, C. N., Wildt, J., Blande, J. D., Eller, A. S. D., Fares, S., Gentner, D. R., Gilman, J. B., Graus, M., Greenberg, J., Guenther, A. B., Hansel, A., Harley, P., Huang, M., Jardine, K., Karl, T., Kaser, L., Keutsch, F. N., Kiendler-Scharr, A., … Goldstein, A. H. (2015). Atmospheric benzenoid emissions from plants rival those from fossil fuels. Scientific Reports, 5(1), 12064. https://doi.org/10.1038/srep12064
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