Abstract
In shallow tropical seas, hydrocoral colonies are locally abundant and important reef-framework builders. Hydrocorals are rich in lipids, which play an essential role in their physiology, but no data on seasonal variations in lipids of hydrocorals are available to date. In the present study, the profiles of total lipids, fatty acids (FA), storage and structural lipids classes, and molecular species of structural lipids in symbiotic dinoflagellates and the host of the hydrocorals Millepora dichotoma and M. platyphylla were analyzed each month throughout the year. In both hydrocoral species, the twofold increase in total lipids in the summer coincided with the water temperature rise and was caused primarily by the considerable accumulation of storage lipids with insignificant variations in structural lipids. The FA markers confirmed the year-round hydrocorals’ predation on zooplankton and indicated that M. dichotoma can consume more diatoms than M. platyphylla during October–January. The polar lipidomes of the two Millepora species were similar. The remodeling of alkyl and sphingosine groups in three structural lipid classes rather than unsaturation degree of their FA groups may be considered as a seasonal adaptive response of host biomembranes in Millepora. The symbiotic dinoflagellates of the hydrocorals kept the galactolipid ratio stable throughout the year but significantly increased the levels of sulfoquinovosyldiacylglycerol and betaine lipid in winter. The FA markers of the symbionts correlated negatively with galactolipids, thus, indicating a higher transfer of the symbiotic FA to the host in winter. Throughout the year, symbionts controlled their lipid class composition, but their lipid molecular species composition varied in a random manner. The considerable amounts of digalactosyldiacylglycerols with C20–22 polyunsaturated FA distinguished M. platyphylla from M. dichotoma and suggested that different hydrocorals contain different symbiont species. Data on seasonal variations of the lipidomes provide new background information for future studies of ecology, physiology, and biochemistry of hydrocorals.
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References
Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Func Ecol 23:539–550
Arai T, Kato M, Heyward A, Ikeda Y, Iizuka T, Maruyama T (1993) Lipid composition of positively buoyant eggs of reef building corals. Coral Reefs 12:71–75
Arts MT, Brett MT, Kainz MJ (2009) Lipids in aquatic ecosystems. Springer, Dordrecht
Awai K, Matsuoka R, Shioi Y (2012) Lipid and fatty acid compositions of Symbiodinium strains. Proc 12th Int Coral Reef Symp 6A
Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554
Baptista M, Lopes VM, Pimentel MS, Bandarra N, Narciso L, Marques A, Rosa R (2012) Temporal fatty acid dynamics of the octocoral Veretillum cynomorium. Comp Biochem Physiol Part B Biochem Mol Biol 161:178–187
Ben-David-Zaslow R, Benayahu Y (1999) Temporal variation in lipid, protein and carbohydrate content in the Red Sea soft coral Heteroxenia fuscescens. J Mar Biol Ass UK 79:1001–1006
Bishop DG, Kenrick JR (1980) Fatty acid composition of symbiotic zooxanthellae in relation to their hosts. Lipids 15:799–804
Dalsgaard J, John MS, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340
Dang LTP, Pham QM, Trinh HTT, Grigorchuk VP, Pham LQ, Luu HV, Imbs AB (2018) Investigation on the content of fatty acids, phospholipids, and phospholipid molecular species composition of the Vietnamese coral Bebryce sp. Viet J Mar Sci Tech 18:148–186
Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261
Dodds LA, Black KD, Orr H, Roberts JM (2009) Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar Ecol Prog Ser 397:113–124
Dowhan W, Bogdanov M, Mileykovskaya E (2008) Functional roles of lipids in membranes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, New York, pp 1–37
Drenkard EJ, Cohen AL, McCorkle DC, de Putron SJ, Starczak VR, Repeta DJ (2018) Juveniles of the Atlantic coral, Favia fragum (Esper 1797) do not invest energy to maintain calcification under ocean acidification. J Exp Mar Biol Ecol 507:61–69
Dubinsky Z, Stambler N (2011) Coral reefs: an ecosystem in transition. Springer, Dordrecht
Ernst R, Ejsing CS, Antonny B (2016) Homeoviscous adaptation and the regulation of membrane lipids. J Mol Biol 428:4776–4791
Figueiredo J, Baird AH, Cohen MF, Flot J-F, Kamiki T, Meziane T, Tsuchiya M, Yamasaki H (2012) Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31:613–619
Fleury BG, Coll JC, Sammarco PW, Tentori E, Duquesne S (2004) Complementary (secondary) metabolites in an octocoral competing with a scleractinian coral: effects of varying nutrient regimes. J Exp Mar Biol Ecol 303:115–131
Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509
Garrett TA, Schmeitzel JL, Klein JA, Hwang JJ, Schwarz JA (2013) Comparative lipid profiling of the cnidarian Aiptasia pallida and its dinoflagellate symbiont. PLoS ONE 8:e57975. https://doi.org/10.1371/journal.pone.0057975
Gray CG, Lasiter AD, Li C, Leblond JD (2009) Mono- and digalactosyldiacylglycerol composition of dinoflagellates I peridinin-containing taxa. Eur J Phycol 44:191–197
Grinyó J, Viladrich N, Diaz D, Munoz A, Mallol S, Salazar J, Castillo R, Gili JM, Gori A (2018) Reproduction, energy storage and metabolic requirements in a mesophotic population of the gorgonian Paramuricea macrospina. PLoS ONE 13:e0203308. https://doi.org/10.1371/journal.pone.0203308
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Ann Rev Physiol 57:19–42
Hinrichs S, Patten NL, Allcock RJN, Saunders SM, Strickland D, Waite AM (2013) Seasonal variations in energy levels and metabolic processes of two dominant Acropora species (A. spicifera and A. digitifera) at Ningaloo Reef. Coral Reefs 32:623–635
Imbs AB (2013) Fatty acids and other lipids of corals: Composition, distribution, and biosynthesis. Rus J Mar Biol 39:153–168
Imbs AB, Dang LTP (2017) The molecular species of phospholipids of the cold-water soft coral Gersemia rubiformis (Ehrenberg, 1834) (Alcyonacea, Nephtheidae). Rus J Mar Biol 43:239–244
Imbs AB, Grigorchuk VP (2019) Lipidomic study of the influence of dietary fatty acids on structural lipids of cold-water nudibranch molluscs. Sci Rep 9:20013. https://doi.org/10.1038/s41598-019-56746-8
Imbs AB, Latyshev NA (2012) Fatty acid composition as an indicator of possible sources of nutrition for soft corals of the genus Sinularia (Alcyoniidae). J Mar Biol Ass UK 92:1341–1347
Imbs AB, Demina OA, Demidkova DA (2006) Lipid class and fatty acid composition of the boreal soft coral Gersemia rubiformis. Lipids 41:721–725
Imbs AB, Yakovleva IM, Pham LQ (2010a) Distribution of lipids and fatty acids in the zooxanthellae and host of the soft coral Sinularia sp. Fish Sci 76:375–380
Imbs AB, Latyshev NA, Dautova TN, Latypov YY (2010b) Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser 409:65–75
Imbs AB, Yakovleva IM, Latyshev NA, Pham LQ (2010c) Biosynthesis of polyunsaturated fatty acids in zooxanthellae and polyps of corals. Rus J Mar Biol 36:452–457
Imbs AB, Dang LPT, Rybin VG, Svetashev VI (2015a) Fatty acid, lipid class, and phospholipid molecular species composition of the soft coral Xenia sp. (Nha Trang Bay, the South China Sea, Vietnam). Lipids 50:575–589
Imbs AB, Dang LPT, Rybin VG, Nguyen NT, Pham LQ (2015b) Distribution of very-long-chain fatty acids between molecular species of different phospholipid classes of two soft corals. Biochem Anal Biochem 4:205. https://doi.org/10.4172/2161-1009.1000205
Imbs AB, Rybin VG, Kharlamenko VI, Dang LPT, Nguyen NT, Pham KM, Pham LQ (2015c) Polyunsaturated molecular species of galactolipids: markers of zooxanthellae in a symbiotic association of the soft coral Capnella sp. (Anthozoa: Alcyonacea). Russ J Mar Biol 41:461–467
Imbs AB, Dang LPT, Nguyen KB (2019) Comparative lipidomic analysis of phospholipids of hydrocorals and corals from tropical and cold-water regions. PLoS ONE 14:e0215759. https://doi.org/10.1371/journal.pone.0215759
Imbs AB, Dang LPT, Nguyen KB, Luu HV, Pham LQ (2020) Annual dynamics of the composition of polar lipids, storage lipids, and fatty acid markers in the hydrocoral Millepora dichotoma Forskål, 1775 from coastal waters of Vietnam. Rus J Mar Biol 46:221–225
Iverson SJ (2008) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer, New York, pp 281–307
Joseph JD (1979) Lipid composition of marine and estuarine invertebrates: Porifera and Cnidaria. Prog Lipid Res 18:1–30
Kern J, Zouni A, Guskov A, Krauss N (2009) Lipids in the structure of photosystem I, photosystem II and the cytochrome b6f complex. In: Wada H, Murata N (eds) Lipids in photosynthesis: Essential and regulatory functions. Springer, New York, pp 203–241
Kharlamenko VI, Zhukova NV, Khotimchenko SV, Svetashev VI, Kamenev GM (1995) Fatty acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar Ecol Prog Ser 120:231–241
Kneeland J, Hughen K, Cervino J, Hauff B, Eglinton T (2013) Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress. Coral Reefs 32:923–934
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580
Latyshev NA, Nguen HK, Do NT, Svetashev VI (1986) Compositional and seasonal variations of phospholipid contents of alcyonarians. Rus J Mar Biol 3:52–56
Latyshev NA, Naumenko NV, Svetashev VI, Latypov YY (1991) Fatty acids of reef-building corals. Mar Ecol Prog Ser 76:295–301
Leblond JD, Chapman PJ (2000) Lipid class distribution of highly unsaturated ling chain fatty acids in marine dinoflagellates. J Phycol 36:1103–1108
Leblond JD, Dahmen JL, Evens TJ (2010) Mono- and digalactosyldiacylglycerol composition of dinoflagellates. IV. Temperature-induced modulation of fatty acid regiochemistry as observed by electrospray ionization/mass spectrometry. Eur J Phycol 45:13–18
Leblond JD, Khadka M, Duong L, Dahmen JL (2015) Squishy lipids: Temperature effects on the betaine and galactolipid profiles of a C18/C18 peridinin-containing dinoflagellate, Symbiodinium microadriaticum (Dinophyceae), isolated from the mangrove jellyfish, Cassiopea xamachana. Phycol Res 63:219–230
Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531
Lewis JB (1992) Heterotrophy in corals: zooplankton predation by the hydrocoral Millepora complanata. Mar Ecol Prog Ser 90:251–256
Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. In: Southward AJ, Young CM, Fuiman LA (eds) Advances in marine biology, vol 50. Elsevier, New York, pp 1–55
Li-Beisson Y, Thelen JJ, Fedosejevs E, Harwood JL (2019) The lipid biochemistry of eukaryotic algae. Prog Lipid Res 74:31–68
Lim CS, Bachok Z, Hii YS (2017) Effects of supplementary polyunsaturated fatty acids on the health of the scleractinian coral Galaxea fascicularis (Linnaeus, 1767). J Exp Mar Biol Ecol 491:1–8
McCauley M, Banaszak AT, Goulet TL (2018) Species traits dictate seasonal-dependent responses of octocoral-algal symbioses to elevated temperature and ultraviolet radiation. Coral Reefs 37:901–917
Mies M, Guth AZ, Tenorio AA, Banha TNS, Waters L, Polito P, Taniguchi S, Bicego MC, Sumida PYG (2018) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37:677–689
Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta 1817:194–208
Monroig O, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11:3998–4018
Naumann MS, Tolosa I, Taviani M, Grover R, Ferrier-Pagès C (2015) Trophic ecology of two cold-water coral species from the Mediterranean Sea revealed by lipid biomarkers and compound-specific isotope analyses. Coral Reefs 34:1165–1175
Oakley CA, Davy SK (2018) Cell biology of coral bleaching. In: van Oppen MJH, Lough JM (eds) Coral bleaching: Patterns, processes, causes and consequences. Springer, Cham, pp 189–212
Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H (2003) Seasonal changes in the content and composition of lipids in the coral Goniastrea aspera. Coral Reefs 22:83–85
Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Physiol Part B Biochem Mol Biol 135:533–537
Rezanka T, Kolouchova I, Gharwalova L, Palyzova A, Sigler K (2018) Lipidomic analysis: from Archaea to mammals. Lipids 53:5–25
Rocker MM, Francis DS, Fabricius KE, Willis BL, Bay LK (2019) Temporal and spatial variation in fatty acid composition in Acropora tenuis corals along water quality gradients on the Great Barrier Reef, Australia. Coral Reefs 38:215–228
Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanog 52:1874–1882
Rodrigues LJ, Grottoli AG, Pease TK (2008) Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J Exp Mar Bio Ecol 358:136–143
Rodríguez L, Lopez C, Casado-Amezua P, Ruiz-Ramos DV, Martínez B, Banaszak A, Tuya F, García-Fernández A, Hernández M (2019) Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic. Coral Reefs 38:255–268
Rosset S, Koster G, Brandsma J, Hunt AN, Postle AD, D’Angelo C (2019) Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts. Coral Reefs 38:1241–1253
Rossi S, Tsounis G (2007) Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Mar Biol 152:429–439
Rossi S, Gili JM, Coma R, Linares C, Gori A, Vert N (2006) Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavata (Anthozoa, Octocorallia): evidence for summer-autumn feeding constraints. Mar Biol 149:643–651
Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, Amsterdam, pp 182–257
Saunders SM, Radford B, Bourke SA, Thiele Z, Bech T, Mardon J (2005) A rapid method for determining lipid fraction ratios of hard corals under varying sediment and light regimes. Env Chem 2:331–336
Seemann J, Sawall Y, Auel H, Richter C (2013) The use of lipids and fatty acids to measure the trophic plasticity of the coral Stylophora subseriata. Lipids 48:275–286
Servetto N, Rossi S, Fuentes V, Alurralde G, Lagger C, Sahade R (2017) Seasonal trophic ecology of the dominant Antarctic coral Malacobelemnon daytoni (Octocorallia, Pennatulacea, Kophobelemnidae). Mar Env Res 130:264–274
Sikorskaya TV (2020) Investigation of the total lipidoma from a zoantharia Palythoa sp. Chem Nat Comp 56:44–49
Sikorskaya TV, Imbs AB (2018) Study of total lipidome of the Sinularia siaesensis soft coral. Rus J Bioorg Chem 44:712–723
Sikorskaya TV, Ermolenko EV, Imbs AB (2020) Effect of experimental thermal stress on lipidomes of the soft coral Sinularia sp. and its symbiotic dinoflagellates. J Exp Mar Biol Ecol 524:151295
Weather Spark (2020) Average weather in Nha Trang Vietnam year round. https://www.seatemperature.org/asia/vietnam/nha-trang.htm
Spener F, Lagarde M, Geloen A, Record M (2003) What is lipidomics? Eur J Lipid Sci Tech 105:481–482
Tang CH, Shi SH, Lin CY, Li HH, Wang WH (2019) Using lipidomic methodology to characterize coral response to herbicide contamination and develop an early biomonitoring model. Sci Total Env 648:1275–1283
Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Nat Acad Sci USA 101:13531–13535
Teece MA, Estes B, Gelsleichter E, Lirman D (2011) Heterotrophic and autotrophic assimilation of fatty acids by two scleractinian corals, Montastraea faveolata and Porites astreoides. Limnol Oceanog 56:1285–1296
Treignier C, Grover R, Ferrier-Pages C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanog 53:2702–2710
Viladrich N, Bramanti L, Tsounis G, Chocarro B, Martinez-Quitana A, Ambroso S, Madurell T, Rossi S (2016) Variation in lipid and free fatty acid content during spawning in two temperate octocorals with different reproductive strategies: surface versus internal brooder. Coral Reefs 35:1033–1045
Wall CB, Ritson-Williams R, Popp BN, Gates RD (2019) Spatial variation in the biochemical and isotopic composition of corals during bleaching and recovery. Limnol Oceanog 64:2011–2028
Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87–90
Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physiol Part B Biochem Mol Biol 122:397–407
Yamashiro H, Oku H, Onaga K, Iwasaki H, Takara K (2001) Coral tumors store reduced level of lipids. J Exp Mar Biol Ecol 265:171–179
Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453
Acknowledgements
This study was supported by the Russian Foundation for Basic Research (Grant 19-54-54002) and the Vietnam Academy of Science and Technology (Grant QTRU01.05/18-19). This manuscript benefited from valuable input by Prof. Morgan Pratchett and three anonymous reviewers. The first author thanks Dr. Irina M. Yakovleva for fruitful discussions on statistical analyses. Thanks are due to Evgenii P. Shvetsov for his help in improving the English.
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Imbs, A.B., Ermolenko, E.V., Grigorchuk, V.P. et al. Seasonal variation in the lipidome of two species of Millepora hydrocorals from Vietnam coastal waters (the South China Sea). Coral Reefs 40, 719–734 (2021). https://doi.org/10.1007/s00338-021-02073-2
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DOI: https://doi.org/10.1007/s00338-021-02073-2