Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis
As a changing climate threatens the persistence of terrestrial and marine ecosystems by altering community composition and function, differential performance of taxa highlights the need for predictive metrics and mechanistic understanding of the factors underlying positive performance in the face of environmental disturbances. Biochemical reactions within cells provide a snapshot of molecular regulation and flexibility during exposure to environmental stressors. However, because the organism is the unit of selection there is a need for the integration of metabolite data with organism physiology to understand mechanisms responsible for individual success under a changing climate.
Our study aims to characterize the molecular response of reef corals to simulated global climate change stressors. Furthermore, we seek to relate changes in the molecular physiology to observations in overall colony response.
To this end, we applied a non-targeted metabolomic approach to describe lipid and primary metabolite composition after exposure of the reef-building coral Pocillopora damicornis to ambient and elevated experimental climate change conditions. We compared these metabolite data to organism physiology, specifically the key processes of photosynthesis, respiration, and calcification.
Corals significantly altered their lipid and primary metabolite profiles in response to experimental treatments. Primary metabolite profiles predicted organisms’ net photosynthesis, but not calcification or respiration measures. Despite challenges in metabolome annotation, our data indicated corals alter carbohydrate composition, cell structural lipids, and signaling compounds in response to elevated treatment conditions.
The integration of metabolite and physiological data highlights the predictive power of metabolomics in defining organism performance and provides biomarkers for future studies. Here, we present a multivariate biomarker approach to assess climate change impacts and advance our mechanistic understanding of stress response in this keystone species.
KeywordsMetabolomics Lipidomics Pocillopora damicornis Ecological disturbance Ocean acidification Global climate change
- Al-Horani, F. A., Al-Moghrabi, S. M., & de Beer, D. (2003). The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Marine Biology, 142, 419–426.Google Scholar
- Allemand, D., Tambutté, É., Allemand, D., TambuttE, E., Girard, J., Jaubert, J., et al. (1998). Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. Journal of Experimental Biology, 201, 2001–2009.PubMedGoogle Scholar
- Banaszak, A. T., Barba Santos, M. G., LaJeunesse, T. C., & Lesser, M. P. (2006). The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. Journal of Experimental Marine Biology and Ecology, 337, 131–146.CrossRefGoogle Scholar
- Coelho, F. J. R. C., Cleary, D. F. R., Rocha, R. J. M., Calado, R., Castanheira, J. M., Rocha, S. M., et al. (2015). Unraveling the interactive effects of climate change and oil contamination on laboratory-simulated estuarine benthic communities. Global Change Biology, 21, 1871–1886.PubMedCrossRefGoogle Scholar
- Constantz, B., & Weiner, S. (1988). Acid macromolecules associated with the mineral phase of scleractinian coral skeletons. Comparative Biochemistry and Physiology, 248, 253–258.Google Scholar
- Dittami, S. M., Scornet, D., Petit, J.-L., Ségurens, B., Da Silva, C., Corre, E., et al. (2009). Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biology, 10, R66.PubMedPubMedCentralCrossRefGoogle Scholar
- Ellis, R. P., Spicer, J. I., Byrne, J. J., Sommer, U., Viant, M. R., White, D. A., & Widdicombe, S. (2014). 1H-NMR metabolomics reveals contrasting response by male and female mussels exposed to reduced seawater pH, increased temperature, and a pathogen. Environmental Technology, 48, 7044–7052.CrossRefGoogle Scholar
- Fitt, W. K., Gates, R. D., Hoegh-Guldberg, O., Bythell, J. C., Jatkar, A., Grottoli, A. G., et al. (2009). Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. Journal of Experimental Marine Biology and Ecology, 373, 102–110.CrossRefGoogle Scholar
- Gordon, B., Leggat, W., & Motti, C. (2013). Extraction protocol for nontargeted NMR and LC-MS metabolomics-based analysis of hard coral and their algal symbionts. In U. Roessner & D. A. Dias (Eds.), Metabolomics tools for natural product discovery (Vol. 1055, pp. 129–147). Dordrecht: Humana Press.CrossRefGoogle Scholar
- Hammer, K. M., Pedersen, S. A., & Størseth, T. R. (2012). Elevated seawater levels of CO2 change the metabolic fingerprint of tissues and hemolymph from the green shore crab Carcinus maenas. Comparative Biochemistry and Physiology Part D, 7, 292–302.Google Scholar
- IPCC. (2014). Climate Change 2014: Synthesis report. Contribution of working groups 1, II, and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC, Geneva, Switzerland.Google Scholar
- Jury, C. P., Robert, W. F., & Alina, S. M. (2010). Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (=Madracis mirabilis sensu Wells, 1973): bicarbonate concentrations best predict calcification rates. Global Change Biology, 16, 1632–1644.CrossRefGoogle Scholar
- Kaplan, F., Kopka, J., Sung, D. Y., Zhao, W., Popp, M., Porat, R., & Guy, C. L. (2007). Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. The Plant Journal, 50, 967–981.PubMedCrossRefGoogle Scholar
- Kind, T., & Fiehn, O. (2006). Metabolite profiling in blood plasma. Metabolomics: Methods and protocols (pp. 3–18). Totowa: Humana Press.Google Scholar
- Lardon, I., Eyckmans, M., Vu, T., Laukens, K., Boeck, G., & Dommisse, R. (2013). 1H-NMR study of the metabolome of a moderately hypoxia-tolerant fish, the common carp (Cyprinus carpio). Metabolomics, 9, 1216–1227.Google Scholar
- Lesser, M. P. (2011). Coral bleaching: causes and mechanisms. In Z. Dubinsky & N. Stambler (Eds.), Coral reefs: An ecosystem in transistion (pp. 405–419), Springer.Google Scholar
- Michal, G., & Schomburg, D. (Eds.). (1999). Biochemical Pathways: An atlas of biochemistry and molecular biology. New York: Wiley.Google Scholar
- Moya, A., Huisman, L., Ball, E. E., Hayward, D. C., Grasso, L. C., Chua, C. M., et al. (2012). Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Molecular Ecology, 21, 2440–2454.PubMedCrossRefGoogle Scholar
- Thurber, R. L., Barott, K. L., Hall, D., Liu, H., Rodriguez-Mueller, B., Desnues, C., et al. (2008). Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proceedings of the National Academy of Sciences USA, 105, 18413–18418.CrossRefGoogle Scholar
- Viant, M. R., Werner, I., Rosenblum, E. S., Gantner, A. S., Tjeerdema, R. S., & Johnson, M. L. (2003). Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiology and Biochemistry, 29, 159–171.CrossRefGoogle Scholar