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Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis

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Abstract

Introduction

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.

Objectives

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.

Methods

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.

Results

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.

Conclusions

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.

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References

  • Ainsworth, T. D., Thurber, R. V., & Gates, R. D. (2010). The future of coral reefs: A microbial perspective. Trends in Ecology & Evolution, 25, 233–240.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Allemand, D., Ferrier-Pagès, C., Furla, P., Houlbrèque, F., Puverel, S., Reynaud, S., et al. (2004). Biomineralisation in reef-building corals: From molecular mechanisms to environmental control. Comptes Renduls Palevol, 3, 453–467.

    Article  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.

    CAS  PubMed  Google Scholar 

  • Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S., & Hoegh-Guldberg, O. (2008). Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences USA, 105, 17442–17446.

    Article  CAS  Google Scholar 

  • Aslund, M. W., Celejewski, M., Lankadurai, B. P., Simpson, A. J., & Simpson, M. J. (2011). Natural variability and correlations in the metabolic profile of healthy Eisenia fetida earthworms observed using 1H NMR metabolomics. Chemosphere, 8, 1096–1101.

    Article  CAS  Google Scholar 

  • Baird, A. H., & Marshall, P. A. (2002). Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series, 237, 133–141.

    Article  Google 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.

    Article  CAS  Google Scholar 

  • Banaszak, A. T., LaJeunesse, T. C., & Trench, R. K. (2000). The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. Journal of Experimental Marine Biology and Ecology, 249, 219–233.

    Article  CAS  Google Scholar 

  • Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor-Knowles, N., & Palumbi, S. R. (2013). Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences USA, 110, 1387–1392.

    Article  CAS  Google Scholar 

  • Bolling, C., & Fiehn, O. (2005). Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiology, 139, 1995–2005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouslimani, A., Porto, C., Rath, C. M., Wang, M., Guo, Y., Gonzalez, A., et al. (2015). Molecular cartography of the human skin surface in 3D. Proceedings of the National Academy of Sciences USA, 122, E2120–E2129.

    Article  CAS  Google Scholar 

  • Brown, B. (1997). Coral bleaching: Causes and consequences. Coral Reefs, 16, S129–S138.

    Article  Google Scholar 

  • Bruno, J. F., & Selig, E. R. (2007). Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS One, 2, e711.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bundy, J. G., Davey, M. P., & Viant, M. R. (2009). Environmental metabolomics: a critical review and future perspectives. Metabolomics, 5, 3–21.

    Article  CAS  Google Scholar 

  • Burriesci, M. S., Raab, T. K., & Pringle, J. R. (2012). Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. Journal of Experimental Marine Biology and Ecology, 215, 3467–3477.

    Article  CAS  Google 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.

    Article  PubMed  Google Scholar 

  • Constantz, B., & Weiner, S. (1988). Acid macromolecules associated with the mineral phase of scleractinian coral skeletons. Comparative Biochemistry and Physiology, 248, 253–258.

    CAS  Google Scholar 

  • Crawley, A., Kline, D., Dunn, S., Anthony, K., & Dove, S. (2010). The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biology, 16, 851–863.

    Article  Google Scholar 

  • Davy, S. K., Allemand, D., & Weis, V. M. (2012). Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews, 76, 229–261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De’ath, G., Fabricius, K. E., Sweatman, H., & Puotinen, M. (2012). The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences USA, 109, 17995–17999.

    Article  Google Scholar 

  • DeSalvo, M., Sunagawa, S., Voolstra, C., & Medina, M. (2010). Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Marine Ecology Progress Series, 402, 97–113.

    Article  CAS  Google Scholar 

  • Dickinson, G. H., Ivanina, A. V., Matoo, O. B., Pörtner, H. O., Lannig, G., Bock, C., et al. (2012). Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. Journal of Experimental Marine Biology and Ecology, 215, 29–43.

    Article  CAS  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doney, S. C., Fabry, V. J., Feely, R. A., & Kleypas, J. A. (2009). Ocean acidification: The other CO2 problem. Annual Review of Marine Science, 1, 169–192.

    Article  PubMed  Google Scholar 

  • Doney, S. C., Ruckelshaus, M., Duffy, J. E., Barry, J. P., Chan, F., English, C. A., et al. (2012). Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4, 11–37.

    Article  PubMed  Google Scholar 

  • Downs, C. A., Ostrander, G. K., Rougee, L., Rongo, T., Knutson, S., Williams, D. E., et al. (2012). The use of cellular diagnostics for identifying sub-lethal stress in reef corals. Ecotoxicology, 21, 768–782.

    Article  CAS  PubMed  Google Scholar 

  • Downs, C. A., Woodley, C. M., Richmond, R. H., Lanning, L. L., & Owen, R. (2005). Shifting the paradigm of coral-reef “health” assessment. Marine Pollution, 51, 486–494.

    Article  CAS  Google Scholar 

  • Drupp, P., De Carlo, E. H., Machkenzie, F. T., Bienfang, P., & Sabine, C. (2011). Nutrient inputs, phytoplankton response, and CO2 variations in a semi-enclosed subtropical embayment, Kaneohe bay, Hawaii. Aquatic Geochemistry, 17, 473–498.

    Article  CAS  Google Scholar 

  • Dunn, S. R., Thomas, M. C., Nette, G. W., & Dove, S. G. (2012). A lipidomic approach to understanding free fatty acid lipogenesis derived from dissolved inorganic carbon within cnidarian-dinoflagellate symbiosis. PLoS One, 7, e46801.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  Google Scholar 

  • Fiehn, O. (2001). Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comparative and Functional Genomics, 2, 155–168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiehn, O., Wohlgemuth, G., & Scholz, M. (2005). Setup and annotation of metabolomic experiments spectrometric metadata. Data integration in the life sciences SE—18 (pp. 224–239). Berlin: Springer.

    Chapter  Google Scholar 

  • Fiehn, O., Wohlgemuth, G., Scholz, M., Kind, T., Lee, D. Y., Lu, Y., et al. (2008). Quality control for plant metabolomics: reporting MSI-compliant studies. The Plant Journal, 53, 691–704.

    Article  CAS  PubMed  Google 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.

    Article  Google Scholar 

  • Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A., & Watkinson, A. R. (2003). Long-term region-wide declines in Caribbean corals. Science, 301, 958.

    Article  CAS  PubMed  Google Scholar 

  • Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-harel, O., Eisen, M. B., Storz, G., et al. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell, 11, 4241–4257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gates, R. D., & Ainsworth, T. D. (2011). The nature and taxonomic composition of coral symbiomes as drivers of performance limits in Scleractinian corals. Journal of Experimental Marine Biology and Ecology, 408, 94–101.

    Article  Google Scholar 

  • Gattuso, J.-P., Allemand, D., & Frankignoulle, M. (1999). Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. American Zoologist, 39, 160–183.

    Article  CAS  Google Scholar 

  • Gigon, A., Matos, A.-R., Laffray, D., Zuily-Fodil, Y., & Pham-Thi, A.-T. (2004). Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Annals of Botany, 94, 345–351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glynn, P. W. (1984). Widespread coral mortality and the 1982-83 El Nino warming event. Environmental Conservation, 11, 133–146.

    Article  Google Scholar 

  • Gordon, B. R., & Leggat, W. (2010). Symbiodinium—invertebrate symbioses and the role of metabolomics. Marine Drugs, 8, 2546–2568.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Chapter  Google Scholar 

  • Goreau, T. F., Goreau, N. I., & Yonge, C. M. (1971). Reef corals: Autotrophs or heterotrophs? Biological Bulletin, 141, 247–260.

    Article  Google Scholar 

  • Goreau, T. J., & Macfarlane, A. H. (1990). Reduced growth rate of Montastrea annularis following the 1987–1988 coral bleaching event. Coral Reefs, 8, 211–215.

    Article  Google Scholar 

  • Grottoli, A. G., Rodrigues, L. J., & Juarez, C. (2004). Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Marine Biology, 145, 621–631.

    Article  CAS  Google Scholar 

  • Guy, C., Kaplan, F., Kopka, J., Selbig, J., & Hincha, D. K. (2008). Metabolomics of temperature stress. Physiologia Plantarum, 132, 220–235.

    CAS  PubMed  Google 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.

    CAS  Google Scholar 

  • Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., et al. (2007). Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., et al. (2007). Phase shifts, herbivory, and the resilience of coral reefs to climate change. Current Biology, 17, 360–365.

    Article  CAS  PubMed  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.

  • 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.

    Article  Google Scholar 

  • Kanehisa, M., & Goto, S. (2000). KEGG : Kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 28, 27–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaniewska, P., Campbell, P. R., Kline, D. I., Rodriguez-Lanetty, M., Miller, D. J., Dove, S., & Hoegh-Guldberg, O. (2012). Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS One, 7, e34659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaplan, F., Kopka, J., Haskell, D. W., Zhao, W., Schiller, K. C., Gatzke, N., et al. (2004). Exploring the temperature-stress metabolome. Plant Physiology, 136, 4159–4168.

    Article  CAS  PubMed  PubMed Central  Google 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.

    Article  CAS  PubMed  Google Scholar 

  • Kind, T., & Fiehn, O. (2006). Metabolite profiling in blood plasma. Metabolomics: Methods and protocols (pp. 3–18). Totowa: Humana Press.

    Google Scholar 

  • Kind, T., Liu, K., Lee, D. Y., Defelice, B., Meissen, J. K., & Fiehn, O. (2013). LipidBlast in silico tandem mass spectrometry database for lipid identification. Nature Methods, 10, 755–758.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klueter, A., Crandall, J., Archer, F., Teece, M., & Coffroth, M. (2015). Taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus Symbiodinium. Metabolites, 5, 74–99.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kopp, C., Domart-Coulon, I., Escrig, S., Humbel, B. M., Hignette, M., & Meibom, A. (2015). Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. mBio, 6, e02299–14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krediet, C., Ritchie, K., Paul, V., & Teplitski, M. (2013). Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proceedings of the Royal Society B, 280, 20122328.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroeker, K. J., Kordas, R. L., Crim, R. N., & Singh, G. G. (2010). Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters, 13, 1419–1434.

    Article  PubMed  Google Scholar 

  • Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annual Review of Physiology, 67, 225–257.

    Article  PubMed  CAS  Google Scholar 

  • Langdon, C., & Atkinson, M. J. (2005). Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal Geophysical Research, 110, 1–16.

    Article  CAS  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.

    CAS  Google Scholar 

  • Lesser, M. P., Mazel, C. H., Gorbunov, M. Y., & Falkowski, P. G. (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science, 305, 997–1000.

    Article  CAS  PubMed  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.

  • Loya, Y. (2001). Coral bleaching: The winners and the losers. Ecology Letters, 4, 122–131.

    Article  Google Scholar 

  • Marubini, F., Ferrier-Pages, C., Furla, P., & Allemand, D. (2008). Coral calcification responds to seawater acidification: A working hypothesis towards a physiological mechanism. Coral Reefs, 27, 491–499.

    Article  Google Scholar 

  • Matyash, V., Liebisch, G., Kurzchalia, T. V., Shevchenko, A., & Schwudke, D. (2008). Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. Journal of Lipid Research, 49, 1137–1146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McHardy, I. H., Goudarzi, M., Tong, M., Ruegger, P. M., Schwager, E., Weger, J. R., et al. (2013). Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome, 1, 17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendes, J. M., & Woodley, J. D. (2002). Timing of reproduction in Montastraea annularis: Relationship to environmental variables. Marine Ecology Progress Series, 277, 241–251.

    Article  Google Scholar 

  • Meyer, E., & Weis, V. M. (2012). Study of cnidarian-algal symbiosis in the “omics” age. Biological Bulletin, 223, 44–65.

    CAS  PubMed  Google Scholar 

  • Michal, G., & Schomburg, D. (Eds.). (1999). Biochemical Pathways: An atlas of biochemistry and molecular biology. New York: Wiley.

  • Moberg, F., & Folke, C. (1999). Ecological goods and services of coral reef ecosystems. Ecological Economics, 29, 215–233.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Muscatine, L. (1967). Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science, 156, 516–519.

    Article  CAS  PubMed  Google Scholar 

  • Muscatine, L., & Cernichiari, E. (1969). Assimilation of photosynthetic products of zooxanthellae by a reef coral. The Biological Bulletin, 137, 506–523.

    Article  CAS  Google Scholar 

  • Muscatine, L., & Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience, 27, 454–460.

    Article  Google Scholar 

  • Oku, H., Yahiro, H., & Onaga, K. (2003). Lipid biosynthesis from [14C]-glucose in the coral Montipora digitata. Fisheries Science, 69, 625–631.

    Article  CAS  Google Scholar 

  • Pandolfi, J. M., Connolly, S. R., Marshall, D. J., & Cohen, A. L. (2011). Projecting coral reef futures under global warming and ocean acidification. Science, 333, 418–422.

    Article  CAS  PubMed  Google Scholar 

  • Papina, M., Meziane, T., & van Woesik, R. (2003). Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 135, 533–537.

    Article  CAS  Google Scholar 

  • Parsons, H. M., Ekman, D. R., Collette, T. W., & Viant, M. R. (2009). Spectral relative standard deviation: A practical benchmark in metabolomics. Analyst, 134, 478–485.

    Article  CAS  PubMed  Google Scholar 

  • Patton, J. S., Abraham, S., & Benson, A. A. (1977). Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: Evidence for a light-driven carbon cycle between symbiont and host. Marine Biology, 44, 235–247.

    Article  CAS  Google Scholar 

  • Peng, S. E., Chen, C. S., & Song, Y. F. (2012). Assessment of metabolic modulation in free-living versus endosymbiotic Symbiodinium using synchrotron radiation-based infrared microspectroscopy. Biology Letters, 8, 434–437.

    Article  PubMed  PubMed Central  Google Scholar 

  • Putnam, H., & Gates, R. D. (2015). Preconditioning the reef-buildling coral Pocillopora damicornis and the potenital for trans-generation acclimatization in coral larvae under future climate change conditions. Journal of Experimental Marine Biology and Ecology, 218, 2365–2372.

    Article  Google Scholar 

  • Putron, S., McCorkle, D., Cohen, A., & Dillon, A. (2011). The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs, 30, 321–328.

    Article  Google Scholar 

  • Rahav, O., Dubinsky, Z., Achituv, Y., & Falkowski, P. G. (1989). Ammonium metabolism in the zooxanthellate coral, Stylophora pistillata. Proceedings of the Royal Society of London B: Biological Sciences, 236, 325–337.

    Article  CAS  Google Scholar 

  • Raina, J., Tapiolas, D., Willis, B. L., & Bourne, D. G. (2009). Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Applied and Environmental Microbiology, 75, 3492–3501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos-Silva, P., Kaandorp, J., Herbst, F., Plasseraud, L., Alcaraz, G., Stern, C., et al. (2014). The skeleton of the staghorn coral Acropora millepora: Molecular and structural characterization. PLoS One, 9, e97454.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ries, J. B., Cohen, A. L., & McCorkle, D. C. (2009). Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology, 37, 1131–1134.

    Article  CAS  Google Scholar 

  • Rodolfo-Metalpa, R., Martin, S., Ferrier-Pages, C., & Gattuso, J.-P. (2010). Response of the temperate coral Cladocora caespitosa to mid- and long-term explosure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences, 7, 289–300.

    Article  CAS  Google Scholar 

  • Rosenberg, E., Koren, O., Reshef, L., Efrony, R., & Zilber-Rosenberg, I. (2007). The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology, 5, 355–362.

    Article  CAS  PubMed  Google Scholar 

  • Rowher, F., Serguritan, V., Azam, F., & Knowlton, N. (2002). Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series, 243, 1–10.

    Article  Google Scholar 

  • Schock, T. B., Stancyk, D. A., Thibodeaux, L., Burnett, K. G., Burnett, L. E., Boroujerdi, A. F., & Bearden, D. W. (2010). Metabolomic analysis of Atlantic blue crab, Callinectes sapidus, hemolymph following oxidative stress. Metabolomics, 6, 250–262.

    Article  CAS  Google Scholar 

  • Seneca, F. O., & Palumbi, S. R. (2015). The role of transcriptome resilience in resistance of corals to bleaching. Molecular Ecology, 7, 1467–1484.

    Article  Google Scholar 

  • Shankar, V., Homer, D., Rigsbee, L., Khamis, H. J., Michail, S., Raymer, M., et al. (2015). The networks of human gut microbe-metabolite associations are different between health and irritable bowel syndrome. The ISME Journal, 9, 1899–1903.

    Article  PubMed  CAS  Google Scholar 

  • Shinzato, C., Shoguchi, E., Kawashima, T., Hamada, M., Hisata, K., Tanaka, M., et al. (2011). Using the Acropora digitifera genome to understand coral responses to environmental change. Nature, 476, 320–323.

    Article  CAS  PubMed  Google Scholar 

  • Sogin, E. M., Anderson, P., Williams, P., Chen, C.-S., & Gates, R. D. (2014). Application of 1H-NMR metabolomic profiling for reef-building corals. PLoS One, 9, e111274.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stitt, M., Lunn, J., & Usadel, B. (2010). Arabidopsis and primary photosynthetic metabolism—more than the icing on the cake. The Plant Journal, 61, 1067–1091.

    Article  CAS  PubMed  Google Scholar 

  • Tapiolas, D. M., Motti, C., Holloway, P., & Boyle, S. G. (2010). High levels of acrylate in the Great Barrier Reef coral Acropora millepora. Coral Reefs, 29, 621–625.

    Article  Google Scholar 

  • Tarrant, A. M., Atkinson, S., & Atkinson, M. J. (1999). Estrone and estradiol-17β concentration in tissue of the scleractinian coral, Montipora verrucosa. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 122, 85–92.

    Article  CAS  Google Scholar 

  • Tarrant, A. M., Blomquist, C. H., Lima, P. H., Atkinson, M. J., & Atkinson, S. (2003). Metabolism of estrogens and androgens by scleractinian corals. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 136, 473–485.

    Article  CAS  Google 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.

    Article  Google Scholar 

  • Trygg, J., & Wold, S. (2002). Orthogonal projections to latent structures (O-PLS). Journal of Chemometrics, 16, 119–128.

    Article  CAS  Google Scholar 

  • van Den Berg, R. A., Hoefsloot, H. C. J., Westerhuis, J. A., Smilde, A. K., & Van Der Werf, M. (2006). Centering, scaling, and transformations: Improving the biological information content of metabolomics data. BMC Genomics, 7, 142.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Meer, G., Voelker, D. R., & Feigenson, G. W. (2008). Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9, 112–124.

    Article  PubMed  PubMed Central  CAS  Google 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.

    Article  CAS  Google Scholar 

  • von Holt, C. (1968). Uptake of glycine and release of nucleoside-polyphosphates by zooxanthellae. Comparative Biochemistry and Physiology, 3, 1071–1079.

    Article  Google Scholar 

  • Wagner, N. D., Hillebrand, H., Wacker, A., & Frost, P. C. (2013). Nutritional indicators and their uses in ecology. Ecology Letters, 16, 535–544. doi:10.1111/ele.12067.

    Article  PubMed  Google Scholar 

  • Whitehead, L. F., & Douglas, A. E. (2003). Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. Journal of Experimental Biology, 206, 3149–3157.

    Article  CAS  PubMed  Google Scholar 

  • Wikoff, W. R., Anfora, A. T., Liu, J., Schultz, P. G., Lesley, S. A., Peters, E. C., & Siuzdak, G. (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences USA, 106, 3698–3703.

    Article  CAS  Google Scholar 

  • Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. Journal of Experimental Biology, 208, 2819–2830.

    Article  CAS  PubMed  Google Scholar 

  • Yancey, P., Heppenstall, M., & Ly, S. (2010). Betaines and dimethylsulfoniopropionate as major osmolytes in cnidaria with endosymbiotic dinoflagellates. Physiological and Biochemical Zoology, 83, 167–173.

    Article  CAS  PubMed  Google Scholar 

  • Yellowlees, D., Rees, T. A. V., & Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell and Environment, 31, 679–694.

    Article  CAS  PubMed  Google Scholar 

  • Yost, D. M., Wang, L.-H., Fan, T.-Y., Chen, C.-S., Lee, R. W., Sogin, E., & Gates, R. D. (2013). Diversity in skeletal architecture influences biological heterogeneity and Symbiodinium habitat in corals. Zoology (Jena), 116, 262–269.

    Article  Google Scholar 

  • Zhang, P. (1993). Model selection via multifold cross validation. The Annals of Statistics, 21, 299–313.

    Article  Google Scholar 

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Acknowledgments

We thank the National Science Foundation Hawaii Experimental Program to Simulate Competitive Research (EPS-0903833) and the National Park Service George Melendez Wright Global Climate Change Fellowship Program for supporting this research. We would also like to thank UC Davis West coast metabolomics facility their metabolomic and lipidomic core services. We thank D. Horgen and P. Williams for the advice and input.

Funding

This study was funded by the National Science Foundation EPSCoR Program (#EPS-0903833) and the National Park Service George Melendez Wright Global Climate Change Fellowship Program

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Sogin, E.M., Putnam, H.M., Anderson, P.E. et al. Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis . Metabolomics 12, 71 (2016). https://doi.org/10.1007/s11306-016-0987-8

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