Abstract
The chemical diversity of scleractinian corals is closely related to their physiological, ecological, and evolutionary status, and can be influenced by both genetic background and environmental variables. To investigate intraspecific variation in the metabolites of these corals, the metabolomes of four species (Pocillopora meandrina, Seriatopora hystrix, Acropora formosa, and Fungia fungites) from the South China Sea were analyzed using untargeted mass spectrometry-based metabolomics. The results showed that a variety of metabolites, including amino acids, peptides, lipids, and other small molecules, were differentially distributed among the four species, leading to their significant separation in principal component analysis and hierarchical clustering plots. The higher content of storage lipids in branching corals (P. meandrina, S. hystrix, and A. formosa) compared to the solitary coral (F. fungites) may be due to the high densities of zooxanthellae in their tissues. The high content of aromatic amino acids in P. meandrina may help the coral protect against ultraviolet damage and promote growth in shallow seawater, while nitrogen-rich compounds may enable S. hystrix to survive in various challenging environments. The metabolites enriched in F. fungites, including amino acids, dipeptides, phospholipids, and other small molecules, may be related to the composition of the coral’s mucus and its life-history, such as its ability to move freely and live solitarily. Studying the chemical diversity of scleractinian corals not only provides insight into their environmental adaptation, but also holds potential for the chemotaxonomy of corals and the discovery of novel bioactive natural products.
This is a preview of subscription content, log in via an institution to check access.
References
Brown B E, Bythell J C. 2005. Perspectives on mucus secretion in reef corals. Marine Ecology Progress Series, 296: 291–309, doi: https://doi.org/10.3354/meps296291
Chadwick N E. 1988. Competition and locomotion in a free-living fungiid coral. Journal of Experimental Marine Biology and Ecology, 123(3): 189–200, doi: https://doi.org/10.1016/0022-0981(88)90041-X
Darling E S, Alvarez-Filip L, Oliver TA, et al. 2012. Evaluating life-history strategies of reef corals from species traits. Ecology Letters, 15(12): 1378–1386, doi: https://doi.org/10.1111/j.1461-0248.2012.01861.x
d’Auriac I G, Quinn R A, Maughan H, et al. 2018. Before platelets: the production of platelet-activating factor during growth and stress in a basal marine organism. Proceedings of the Royal Society B: Biological Sciences, 285(1884): 20181307, doi: https://doi.org/10.1098/rspb.2018.1307
De Vos R C, Moco S, Lommen A, et al. 2007. Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry. Nature Protocols, 2(4): 778–791, doi: https://doi.org/10.1038/nprot.2007.95
Dettmer K, Aronov P A, Hammock B D. 2007. Mass spectrometry-based metabolomics. Mass Spectrometry Reviews, 26(1): 51–78, doi: https://doi.org/10.1002/mas.20108
Drollet J H, Glaziou P, Martin P M V. 1993. A study of mucus from the solitary coral Fungia fungites (Scleractinia: Fungiidae) in relation to photobiological UV adaptation. Marine Biology, 115(2): 263–266, doi: https://doi.org/10.1007/BF00346343
Dudareva N. 2015. Aromatic amino acid network: biosynthesis, regulation and transport. The FASEB Journal, 29(S1): 103.2
Farag M A, Porzel A, Al-Hammady M 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, doi: https://doi.org/10.1021/acs.jproteome.6b00002
Hadaidi G, Gegner H M, Ziegler M, et al. 2019. Carbohydrate composition of mucus from scleractinian corals from the central Red Sea. Coral Reefs, 38(1): 21–27, doi: https://doi.org/10.1007/s00338-018-01758-5
Han Minwei, Zhang Ruijie, Yu Kefu, et al. 2020. Polycyclic aromatic hydrocarbons (PAHs) in corals of the South China Sea: occurrence, distribution, bioaccumulation, and considerable role of coral mucus. Journal of Hazardous Materials, 384: 121299, doi: https://doi.org/10.1016/j.jhazmat2019.121299
Hartmann A C, Petras D, Quinn R A, et al. 2017. Meta-mass shift chemical profiling of metabolomes from coral reefs. Proceedings of the National Academy of Sciences of the United States of America, 114(44): 11685–11690
Hayes J M, Abdul-Rahman N H, Gerdes M J, et al. 2021. Coral genus differentiation based on direct analysis in real time-high resolution mass spectrometry-derived chemical fingerprints. Analytical Chemistry, 93(46): 15306–15314, doi: https://doi.org/10.1021/acs.anal-chem.1c02519
He Qing, Sun Ruiqi, Liu Huijuan, et al. 2014. NMR-based metabolomic analysis of spatial variation in soft corals. Marine Drugs, 12(4): 1876–1890, doi: https://doi.org/10.3390/md12041876
Hou Dan, Lu Haiwen, Zhao Zhongyu, et al. 2022. Integrative transcriptomic and metabolomic data provide insights into gene networks associated with lignification in postharvest Lei bamboo shoots under low temperature. Food Chemistry, 368: 130822, doi: https://doi.org/10.1016/j≼odchem.2021.130822
Hughes T P, Kerry J T, Álvarez-Noriega M, et al. 2017. Global warming and recurrent mass bleaching of corals. Nature, 543(7645): 373–377, doi: https://doi.org/10.1038/nature21707
Imbs A B, Yakovleva I M. 2012. Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs, 31(1): 41–53, doi: https://doi.org/10.1007/s00338-011-0817-4
Jones R N, Brush E G, Dilley E R, et al. 2021. Autumn coral bleaching in Hawai’i. Marine Ecology Progress Series, 675: 199–205, doi: https://doi.org/10.3354/meps13837
Karabulut A, McClain M, Rubinstein B, et al. 2022. The architecture and operating mechanism of a cnidarian stinging organelle. Nature Communications, 13(1): 3494, doi: https://doi.org/10.1038/s41467-022-31090-0
Kopp C, Domart-Coulon I, Escrig S, et al. 2015. Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. mBio, 6(1): e02299–14
Kusano M, Yang Zhigang, Okazaki Y, et al. 2015. Using metabolomic approaches to explore chemical diversity in rice. Molecular Plant, 8(1): 58–67, doi: https://doi.org/10.1016/j.molp.2014.11.010
Lynch J H, Dudareva N. 2020. Aromatic amino acids: a complex network ripe for future exploration. Trends in Plant Science, 25(7): 670–681, doi: https://doi.org/10.1016/j.tplants.2020.02.005
Maeda H, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology, 63: 73–105, doi: https://doi.org/10.1146/annurev-arplant-042811-105439
Marcelino V R, Morrow K M, van Oppen M J H, et al. 2017. Diversity and stability of coral endolithic microbial communities at a naturally high pCO2 reef. Molecular Ecology, 26(19): 5344–5357, doi: https://doi.org/10.1111/mec.14268
Metz T O, Zhang Qibin, Page J S, et al. 2007. Future of liquid chromatography-mass spectrometry in metabolic profiling and metabolomic studies for biomarker discovery. Biomarkers in Medicine, 1(1): 159–185, doi: https://doi.org/10.2217/17520363.1.1.159
Meunier V, Bonnet S, Pernice M, et al. 2019. Bleaching forces coral’s heterotrophy on diazotrophs and Synechococcus. The ISME Journal, 13(11): 2882–2886, doi: https://doi.org/10.1038/s41396-019-0456-2
Murphy J W A, Richmond R H. 2016. Changes to coral health and metabolic activity under oxygen deprivation. Peerj, 4: e1956, doi: https://doi.org/10.7717/peerj.1956
Oku H, Yamashiro H, Onaga K, et al. 2002. Lipid distribution in branching coral Montipora digitata. Fisheries Science, 68(3): 517–522, doi: https://doi.org/10.1046/j.1444-2906.2002.00456.x
Pei Jiying, Chen Shiguo, Yu Kefu, et al. 2022a. Metabolomics characterization of scleractinia corals with different life-history strategies: a case study about Pocillopora meandrina and Seriatopora hystrix in the South China Sea. Metabolites, 12(11): 1079, doi: https://doi.org/10.3390/metabo12111079
Pei Jiying, Yu Wenfeng, Zhang Jingjing, et al. 2022b. Mass spectrometry-based metabolomic signatures of coral bleaching under thermal stress. Analytical and Bioanalytical Chemistry, 414(26): 7635–7646, doi: https://doi.org/10.1007/s00216-022-04294-y
Qin Zhenjun, Yu Kefu, Chen Biao, et al. 2019. Diversity of Symbiod-iniaceae in 15 coral species from the southern South China Sea: potential relationship with coral thermal adaptability. Frontiers in Microbiology, 10: 2343, doi: https://doi.org/10.3389/fmicb.2019.02343
Qin Zhenjun, Yu Kefu, Chen Shuchang, et al. 2021. Microbiome of juvenile corals in the outer reef slope and lagoon of the South China Sea: insight into coral acclimatization to extreme thermal environments. Environmental Microbiology, 23(8): 4389–4404, doi: https://doi.org/10.1111/1462-2920.15624
Qin Zhenjun, Yu Kefu, Liang Yanting, et al. 2020. Latitudinal variation in reef coral tissue thickness in the South China Sea: potential linkage with coral tolerance to environmental stress. Science of The Total Environment, 711: 134610, doi: https://doi.org/10.1016/j.scitotenv.2019.134610
Quévrain E, Domart-Coulon I, Bourguet-Kondracki M L. 2014. Marine natural products-chemical defense/chemical communication in sponges and corals. In: Osbourn A, Goss R J, Carter G T, eds. Natural Products: Discourse, Diversity, and Design. Hoboken: Wiley-Blackwell, 39–66
Roach T N F, Dilworth J, Christian M H, et al. 2021. Metabolomic signatures of coral bleaching history. Nature Ecology & Evolution, 5(4): 495–503
Rocha L A, Pinheiro H T, Shepherd B, et al. 2018. Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science, 361(6399): 281–284, doi: https://doi.org/10.1126/science.aaq1614
Rosic N N, Dove S. 2011. Mycosporine-like amino acids from coral dinoflagellates. Applied and Environmental Microbiology, 77(24): 8478–8486, doi: https://doi.org/10.1128/AEM.05870-11
Schmidt C A, Daly N L, Wilson D T. 2019. Coral venom toxins. Frontiers in Ecology and Evolution, 7: 320, doi: https://doi.org/10.3389/fevo.2019.00320
Shinzato C, Shoguchi E, Kawashima T, et al. 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature, 476(7360): 320–323, doi: https://doi.org/10.1038/nature10249
Sinniger F, Morita M, Harii S. 2013. “Locally extinct” coral species Seriatopora hystrix found at upper mesophotic depths in Okinawa. Coral Reefs, 32(1): 153, doi: https://doi.org/10.1007/s00338-012-0973-1
Sogin E M, Anderson P, Williams P, et al. 2014. Application of 1H-NMR metabolomic profiling for reef-building corals. PLoS One, 9(10): e111274, doi: https://doi.org/10.1371/journal.pone.0111274
Stabili L, Schirosi R, Licciano M, et al. 2014. Role of Myxicola infundibulum (Polychaeta, Annelida) mucus: from bacterial control to nutritional home site. Journal of Experimental Marine Biology and Ecology, 461: 344–349, doi: https://doi.org/10.1016/j.jembe.2014.09.005
Subbaraj A K, Huege J, Fraser K, et al. 2019. A large-scale metabolomics study to harness chemical diversity and explore biochemical mechanisms in ryegrass. Communications Biology, 2: 87, doi: https://doi.org/10.1038/s42003-019-0289-6
Tang Fenfen, Hatzakis E. 2020. NMR-based analysis of pomegranate juice using untargeted metabolomics coupled with nested and quantitative approaches. Analytical Chemistry, 92(16): 11177–11185, doi: https://doi.org/10.1021/acs.analchem.0c01553
Tang Jia, Cai Wenqi, Yan Zhicong, et al. 2022. Interactive effects of acidification and copper exposure on the reproduction and metabolism of coral endosymbiont Cladocopium goreaui. Marine Pollution Bulletin, 177: 113508, doi: https://doi.org/10.1016/j.marpolbul.2022.113508
Vohsen S A, Fisher C R, Baums I B. 2019. Metabolomic richness and fingerprints of deep-sea coral species and populations. Metaolomics, 15(3): 34, doi: https://doi.org/10.1007/s11306-019-1500-y
Wang Mingxun, Carver J J, Phelan V V, et al. 2016. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nature Biotechnology, 34(8): 828–837, doi: https://doi.org/10.1038/nbt.3597
Williams A, Chiles E N, Conetta D, et al. 2021. Metabolomic shifts associated with heat stress in coral holobionts. Science Advances, 7(1): eabd4210, doi: https://doi.org/10.1126/sciadv.abd4210
Yamashiro H, Oku H, Onaga K. 2005. Effect of bleaching on lipid content and composition of Okinawan corals. Fisheries Science, 71(2): 448–453, doi: https://doi.org/10.1111/j.1444-2906.2005.00983.x
Yu Wanjun, Wang Wenhuan, Yu Kefu, et al. 2019. Rapid decline of a relatively high latitude coral assemblage at Weizhou Island, northern South China Sea. Biodiversity and Conservation, 28(14): 3925–3949, doi: https://doi.org/10.1007/s10531-019-01858-w
Zhao Xiaoyan, E Hengchao, Dong Hui, et al. 2022. Combination of untargeted metabolomics approach and molecular networking analysis to identify unique natural components in wild Morchella sp. by UPLC-Q-TOF-MS. Food Chemistry, 366: 130642, doi: https://doi.org/10.1016/j.foodchem.2021.130642
Author information
Authors and Affiliations
Corresponding author
Additional information
Foundation item: The National Natural Science Foundation of China under contract Nos 22264003, 42090041 and 42030502; the Guangxi Natural Science Fund Project under contract Nos AD17129063, AA17204074 and 2018GXNSFAA281354; the Innovation and Entrepreneurship Training Program of College Students from Guangxi University under contract Nos 202210593888 and 202210593890.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Pei, J., Zhou, Y., Chen, S. et al. Chemical diversity of scleractinian corals revealed by untargeted metabolomics and molecular networking. Acta Oceanol. Sin. 42, 127–135 (2023). https://doi.org/10.1007/s13131-023-2173-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13131-023-2173-y