Metabolomic richness and fingerprints of deep-sea coral species and populations
From shallow water to the deep sea, corals form the basis of diverse communities with significant ecological and economic value. These communities face many anthropogenic stressors including energy and mineral extraction activities, ocean acidification and rising sea temperatures. Corals and their symbionts produce a diverse assemblage of compounds that may help provide resilience to some of these stressors.
We aim to characterize the metabolomic diversity of deep-sea corals in an ecological context by investigating patterns across space and phylogeny.
We applied untargeted Liquid Chromatography-Mass Spectrometry to examine the metabolomic diversity of the deep-sea coral, Callogorgia delta, across three sites in the Northern Gulf of Mexico as well as three other deep-sea corals, Stichopathes sp., Leiopathes glaberrima, and Lophelia pertusa, and a shallow-water species, Acropora palmata.
Different coral species exhibited distinct metabolomic fingerprints and differences in metabolomic richness including core ions unique to each species. C. delta was generally least diverse while Lophelia pertusa was most diverse. C. delta from different sites had different metabolomic fingerprints and metabolomic richness at individual and population levels, although no sites exhibited unique core ions. Two core ions unique to C. delta were putatively identified as diterpenes and thus may possess a biologically important function.
Deep-sea coral species have distinct metabolomic fingerprints and exhibit high metabolomic diversity at multiple scales which may contribute to their capabilities to respond to both natural and anthropogenic stressors, including climate change.
KeywordsCallogorgia delta Diversity Rarefaction Chemotaxonomy
We thank Andrew Patterson, Phil Smith, Imhoi Koo, and Manuel Liebeke for advice and assistance with metabolomics analysis, Dana E Williams for A. palmata collections, and the ROV Hercules pilots and crew of the EV Nautilus for making this work possible. We would also like to thank Steve Auscavitch, Carlos Gomez, Styles Smith, Alaina Weinheimer, Calum Campbell, and Meghann Devlin-Durante for assistance with collections and laboratory analyses. This is contribution no. 519 from the Ecosystem Impacts of Oil and Gas Inputs to the Gulf (ECOGIG) consortium.
C.R.F and I.B.B conceived and designed the research. S.A.V. conducted the research and designed and conducted the analyses. S.A.V. wrote the paper with contributions from all authors.
This study was funded by a grant from the Gulf of Mexico Research Initiative awarded to the Ecosystem Impacts of Oil and Gas Inputs to the Gulf (ECOGIG) consortium. Collection of Acropora palmata was funded through NSF OCE-1516763.
Compliance with ethical standards
Conflict of interest
S.A.V. declares that he has no conflict of interest. C.R.F. declares that he has no conflict of interest. I.B.B. declares that she has no conflict of interest.
All applicable international, national, and institutional guidelines for the care and use of animals were followed. Acropora palmata was sampled under permit number FKNMS-2014-148-A2 issued by the National Oceanic and Atmospheric Administration in the Florida Keys National Marine Sanctuary. Permits are not required to sample deep-sea corals in the Gulf of Mexico. Letters of acknowledgment were obtained for our research cruise from NOAA following the Magnuson-Stevens Fishery Conservation and Management Act.
- Aceret, T. L., Coll, J. C., Uchio, Y., & Sammarco, P. W. (1998). Antimicrobial activity of the diterpenes flexibilide and sinulariolide derived from Sinularia flexibilis Quoy and Gaimard 1833 (Coelenterata: Alcyonacea, Octocorallia). Comparative Biochemistry and Physiology Part C, 120, 121–126.Google Scholar
- Aceret, T. L., Sammarco, P. W., & Coll, J. C. (1995). Effects of diterpenes derived from the soft coral Sinularia flexibilis on the eggs, sperm and embryos of the scleractinian corals Montipora digitata and Acropora Tenuis. Marine Biology, 122(2), 317–323.Google Scholar
- Bayer, F. M., & Weinheimer, A. J. (1974). Prostaglandins from Plexaura homomalla: Ecology, utilization and conservation of a major medical marine resource. Studies in Tropical Oceanography, 12(12), 165.Google Scholar
- Bonini, C., Kinnel, R. B., Li, M., Scheuer, P. J., & Djerassi, C. (1983). Minor and trace sterols in marine invertebrates 38: Isolation, structure elucidation and partial synthesis of papakusterol, a new biosynthetically unusual marine sterol with a cyclopropyl-containing side chain. Tetrahedron Letters, 24(3), 227–280.Google Scholar
- Bose, U., Hewavitharana, A. K., Vidgen, M. E., Ng, Y. K., Shaw, P. N., Fuerst, J. A., & Hodson, M. P. (2014). Discovering the recondite secondary metabolome spectrum of Salinispora species: A study of inter-species diversity. PLoS ONE, 9(3), 1–10.Google Scholar
- Bruno, J. F., Selig, E. R., Casey, K. S., Page, C. A., Willis, B. L., Harvell, C. D., et al. (2007). Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology, 5(6), 1220–1227.Google Scholar
- Buhl-Mortensen, L., & Mortensen, P. B. (2005). Distribution and diversity of species associated with deep-sea gorgonian corals off Atlantic Canada. In A. Freiwald & J. M. Roberts (Eds.), Cold-water corals and ecosystems (pp. 849–879). Berlin: Springer.Google Scholar
- Cairns, S. D., & Bayer, F. M. (2002). Studies on the western Atlantic Octocorallia (Coelenterata: Anthozoa). Part 2. The genus Callogorgia Gray, 1858. Proceedings of the Biological Society of Washington, 115, 840–867.Google Scholar
- Calderón-Santiago, M., Fernández-Peralbo, M. A., Priego-Capote, F., & Luque de Castro, M. D. (2016). MSCombine: A tool for merging untargeted metabolomic data from high-resolution mass spectrometry in the positive and negative ionization modes. Metabolomics. https://doi.org/10.1007/s11306-016-0970-4.Google Scholar
- Cau, A., Follesa, M. C., Bo, M., Canese, S., Bellodi, A., Cannas, R., & Cau, A. (2013). Leiopathes glaberrima forest from South West Sardinia: A thousand years old nursery area for the small spotted catshark Scyliorinus canicula. Rapp. Comm. int. Mer Médit, 40(4), 717.Google Scholar
- Cesar, H., Burke, L., & Pet-Soede, L. (2003). The economics of worldwide coral reef degradation. Cesar Environmental Economics Consulting, 14, 23.Google Scholar
- Costa-Lotufo, L. V., Carnevale-Neto, F., Trindade-Silva, A. E., Silva, R. R., Silva, G. G. Z., Wilke, D. V., et al. (2018). Chemical profiling of two congeneric sea mat corals along the Brazilian coast: Adaptive and functional patterns. Chemical Communications, 54(16), https://doi.org/10.1039/C7CC08411K.
- Costello, M. J., McCrea, M., Freiwald, A., Lundälv, T., Jonsson, L., Bett, B. J., et al. (2005). Role of cold-water Lophelia pertusa coral reefs as fish habitat in the NE Atlantic. In A. Freiwald & J. M. Roberts (Eds.), Cold-water corals and ecosystems (pp. 771–805). Berlin: Springer.Google Scholar
- DeFelice, B. C., Singh Mehta, S., Samra, S., Čajka, T., Wancewicz, B., Fahrmann, J. F., & Oliver Fiehn (2017). Mass spectral feature list optimizer (MS-FLO): A tool to minimize false positive peak reports in untargeted liquid chromatography-mass spectrometry (LC-MS) data processing. Analytical Chemistry, 89(6), 3250–3255.PubMedGoogle Scholar
- Farag, M. A., Porzel, A., Al-Hammady, M. A., Hegazy, M. E. F., Meyer, A., Mohamed, T. A., et al. (2016). Soft corals biodiversity in the Egyptian Red Sea: A comparative MS and NMR metabolomics approach of wild and aquarium grown species. Journal of Proteome Research, 15(4), 1274–1287.PubMedGoogle Scholar
- Floros, D. J., Jensen, P. R., Dorrestein, P. C., & Koyama, N. (2016). A metabolomics guided exploration of marine natural product chemical space. Metabolomics, 12(9), 1–11.Google Scholar
- Freiwald, A., Henrich, R., & Pätzold, J. (1997). Anatomy of a deep-water coral reef mound from Stjernsund, West Finnmark, northern Norway. In N. P. James & J. A. D. Clark (Eds.), Cool-water carbonates (pp. 141–163). Tulsa, OK: Society for Sedimentary Geology. https://doi.org/10.2110/pec.97.56.0141.Google Scholar
- García-Matucheski, S., & Muniain, C. (2011). Predation by the nudibranch Tritonia odhneri (Opisthobranchia: Tritoniidae) on octocorals from the South Atlantic Ocean. Marine Biodiversity, 41(2), 287–297.Google Scholar
- Glazier, A. E., & Etter, R. J. (2014). Cryptic speciation along a bathymetric gradient. Biological Journal of the Linnean Society, 113(4), 897–913.Google Scholar
- Gong, L., Chen, W., Gao, Y., Liu, X., Zhang, H., Xu, C., et al. (2013). Genetic analysis of the metabolome exemplified using a rice population. Proceedings of the National Academy of Sciences of the United States, 110(50), 20320–20325.Google Scholar
- Guzmán, H. M., Jackson, J. B. C., & Weil, E. (1991). Short-term ecological consequences of a major oil spill on Panamian subtidal reef corals. Coral Reefs, 10, 1–12.Google Scholar
- Henry, L. A., & Roberts, J. M. (2007). Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep-Sea Research Part I: Oceanographic Research Papers, 54(4), 654–672.Google Scholar
- Hoegh-Guldberg, O., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., & Eakin, C. M. (2008). Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737–1742.Google Scholar
- Holopainen, J. K., & Blande, J. D. (2012). Molecular plant volatile communication. In C. López-Larrea (Ed.), Sensing in nature. Advances in experimental medicine and biology (pp. 17–31). New York: Springer.Google Scholar
- Hu, P., Luo, G.-A., Zhao, Z.-Z., & Jiang, Z.-H. (2005). Quantitative determination of four diterpenoids in Radix Salviae Miltiorrhizae using LC-MS-MS. Chemical & Pharmaceutical Bulletin, 53(6), 705–709.Google Scholar
- Idjadi, J. A., & Edmunds, P. J. (2006). Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Marine Ecology Progress Series, 319, 117–127.Google Scholar
- Januar, H., Marraskuranto, E., Patantis, G., & Chasanah, E. (2012). LC-MS metabolomic analysis of environmental stressor impacts on the metabolite diversity in Nephthea spp. Chronicles of Young Scientists, 3(1), 57.Google Scholar
- Jensen, A., & Frederiksen, R. (2011). The fauna associated with the bank-forming deepwater coral Lophelia pertusa (Scleractinia) on the Faroe shelf. Sarsia, 77(1), 53–69.Google Scholar
- Kornprobst, J.-M. (2014). Encyclopedia of marine natural products. Weinheim: Wiley-VCH.Google Scholar
- La Rivière, M., Garrabou, J., & Bally, M. (2015). Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals. Coral Reefs, 34(4), 1087–1098.Google Scholar
- Lirman, D. (1999). Reef fish communities associated with Acropora palmata: Relationship to benthic attributes. Bulletin of Marine Science, 65, 235–252.Google Scholar
- Öhman, M. C., & Rajasuriya, A. (1998). Relationships between habitat structure and fish communities on coral. Environmental Biology of Fishes, 53, 19–31.Google Scholar
- Post, A. L., Obrien, P. E., Beaman, R. J., Riddle, M. J., & De Santis, L. (2010). Physical controls on deep water coral communities on the George V Land slope, East Antarctica. Antarctic Science, 22(4), 371–378.Google Scholar
- Quinn, R. A., Vermeij, M. J. A., Hartmann, A. C., Galtier, I., Benler, S., Haas, A., et al. (2016). Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2016.0469.PubMedGoogle Scholar
- Rasher, D. B., Stout, E. P., Engel, S., Kubanek, J., & Hay, M. E. (2011). Macroalgal terpenes function as allelopathic agents against reef corals. Proceedings of the National Academy of Sciences of the United States, 108(43), 17726–17731.Google Scholar
- Roark, E. B., Guilderson, T. P., Dunbar, R. B., & Ingram, B. L. (2006). Radiocarbon-based ages and growth rates of Hawaiian deep-sea corals. Marine Ecology Progress Series, 327, 1–14.Google Scholar
- Ruiz-Ramos, D. V., Saunders, M., Fisher, C. R., & Baums, I. B. (2015). Home bodies and wanderers: Sympatric lineages of the Deep-Sea black coral Leiopathes glaberrima. PLoS ONE, 10(10), 1–19.Google Scholar
- Slattery, M., Avila, C., Starmer, J., & Paul, V. J. (1998). A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis Avila, Ballesteros, Slattery, Starmer and Paul. Journal of Experimental Marine Biology and Ecology, 226(1), 33–49.Google Scholar
- Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K., & Schmidt, G. W. (2006). Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology, 148(4), 711–722.Google Scholar
- van de Water, J. A. J. M., Melkonian, R., Junca, H., Voolstra, C. R., Reynaud, S., Allemand, D., & Ferrier-Pagès, C. (2016). Spirochaetes dominate the microbial community associated with the red coral Corallium rubrum on a broad geographic scale. Scientific Reports, 6, 1–7.Google Scholar
- van de Water, J. A. J. M., Melkonian, R., Voolstra, C. R., Junca, H., Beraud, E., Allemand, D., & Ferrier-Pagès, C. (2017). Comparative assessment of Mediterranean Gorgonian-associated microbial communities reveals conserved core and locally variant bacteria. Microbial Ecology, 73(2), 466–478.PubMedGoogle Scholar
- van de Water, J. A. J. M., Voolstra, C. R., Rottier, C., Cocito, S., Peirano, A., Allemand, D., & Ferrier-Pagès, C. (2018b). Seasonal stability in the microbiomes of temperate gorgonians and the red coral Corallium rubrum across the Mediterranean Sea. Microbial Ecology, 75(1), 274–288.PubMedGoogle Scholar
- White, H. K., Hsing, P., Cho, W., Shank, T. M., Cordes, E. E., Quattrini, A. M., et al. (2012). Impact of the Deepwater Horizon oil spill on a deep-water coral community in the Gulf of Mexico. Proceedings of the National Academy of Sciences of the United States, 109(50), 20303–20308.Google Scholar
- Yesson, C., Taylor, M. L., Tittensor, D. P., Davies, A. J., Guinotte, J., Baco, A., et al. (2012). Global habitat suitability of cold-water octocorals. Journal of Biogeography, 39(7), 1278–1292.Google Scholar