Lipid metabolic response patterns to heat stress in two Symbiodiniaceae species with different environmental sensitivities (<i>Cladocopium goreaui</i> and <i>Durusdinium trenchii</i>)

Zhang Li; Li Zhicong; Yang Yating; Liang Zhuqing; Feng Yihe; Lu Mingyao; Hu Siyu; Yu Kefu; Liang Jiayuan

doi:10.12284/hyxb2025100

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Zhang Li，Li Zhicong，Yang Yating, et al. Lipid metabolic response patterns to heat stress in two Symbiodiniaceae species with different environmental sensitivities (Cladocopium goreaui and Durusdinium trenchii)[J]. Haiyang Xuebao，2025, 47(9)：1–14 doi: 10.12284/hyxb2025100

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Zhang Li，Li Zhicong，Yang Yating, et al. Lipid metabolic response patterns to heat stress in two Symbiodiniaceae species with different environmental sensitivities (Cladocopium goreaui and Durusdinium trenchii)[J]. Haiyang Xuebao，2025, 47(9)：1–14 doi: 10.12284/hyxb2025100

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Lipid metabolic response patterns to heat stress in two Symbiodiniaceae species with different environmental sensitivities (Cladocopium goreaui and Durusdinium trenchii)

doi: 10.12284/hyxb2025100

1.
School of Resources, Environment and Materials, Guangxi University, Nanning 530004, China
2.
School of Marine Sciences, Guangxi University, Nanning 530004, China
3.
Southern Marine Science and Engineering Guangxi Laboratory, Nanning 530004, China

Received Date: 2024-12-13
Rev Recd Date: 2025-04-25

Available Online: 2025-05-30

Abstract

Abstract

Symbiodiniaceae are indispensable partners in the coral symbiotic system, and different species exhibit varying sensitivities to environmental stress, thereby influencing the environmental adaptability of their coral hosts. This study investigates the stress response patterns of two widely distributed coral symbiotic Symbiodiniaceae species—environmentally sensitive Cladocopium goreaui and environmentally tolerant Durusdinium trenchii—under heat stress from the perspective of lipid metabolism. The results showed that heat stress significantly affected their cell density, photosynthetic pigment content, photochemical efficiency of photosystem II (Fv/Fm), and antioxidant activity, with statistically significant differences (P < 0.05). Lipidomics revealed that lipid-differentiated metabolites such as phosphatidylcholine, triglycerides, phosphatidylethanolamine and lysophosphatidylcholine were significantly enriched in glycerophospholipid metabolism, triglyceride metabolism, and polyunsaturated fatty acid-related metabolic pathways in response to heat stress in C. goreaui and D. trenchii. Notably, the two species exhibited significant differences in sphingolipid metabolism: D. trenchii downregulated ceramide levels to reduce oxidative stress damage, regulate autophagy, and adapt to changes in membrane fluidity, whereas C. goreaui primarily upregulated lipid molecules rich in polyunsaturated fatty acids to maintain membrane stability and regulate signal transduction. A deeper understanding of the lipid metabolic stress response mechanisms of Symbiodiniaceae with different environmental sensitivities under heat stress provides new insights into enhancing coral adaptability to environmental changes from a symbiotic partner perspective.
- heat stress,
- symbiodiniaceae,
- sphingolipid metabolism,
- lipidomics,
- oxidative stress

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References

[1]	Trench R K. Microalgalinvertebrate symbioses: a review[J]. Endocytobiosis and Cell Research, 1993, 9(2/3): 135−175.
[2]	Von Holt C, Von Holt M. Transfer of photosynthetic products from zooxanthellae to coelenterate hosts[J]. Comparative Biochemistry and Physiology, 1968, 24(1): 73−81. doi: 10.1016/0010-406X(68)90959-6
[3]	Cernichiari E, Muscatine L, Smith D C. Maltose excretion by the symbiotic algae of Hydra viridis[J]. Proceedings of the Royal Society of London Series B, Biological Sciences, 1969, 173(1033): 557−576.
[4]	Gordon B R, Leggat W. Symbiodinium-Invertebrate symbioses and the role of metabolomics[J]. Marine Drugs, 2010, 8(10): 2546−2568. doi: 10.3390/md8102546
[5]	Yellowlees D, Rees T A V, Leggat W. Metabolic interactions between algal symbionts and invertebrate hosts[J]. Plant Cell Environ, 2008, 31(5): 679−694. doi: 10.1111/j.1365-3040.2008.01802.x
[6]	Pochon X, Gates R D. A new Symbiodinium clade (dinophyceae) from soritid foraminifera in Hawai’i[J]. Molecular Phylogenetics and Evolution, 2010, 56(1): 492−497. doi: 10.1016/j.ympev.2010.03.040
[7]	Pochon X, Lajeunesse T C. Miliolidium n. gen, a new symbiodiniacean genus whose members associate with soritid foraminifera or are free-living[J]. Eukaryotic Microbiology, 2021, 68(4): e12856. doi: 10.1111/jeu.12856
[8]	Nitschke M R, Craveiro S C, Brandão C, et al. Description of Freudenthalidium gen. nov. and Halluxium gen. nov. to formally recognize clades Fr3 and H as genera in the family symbiodiniaceae (dinophyceae)[J]. Journal of Phycology, 2020, 56(4): 923−940. doi: 10.1111/jpy.12999
[9]	Lajeunesse T C, Parkinson J E, Gabrielson P W, et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts[J]. Current Biology, 2018, 28(16): 2570−2580. e6.
[10]	Abrego D, Ulstrup K E, Willis B L, et al. Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress[J]. Proceedings of the Royal Society B: Biological Sciences, 2008, 275(1648): 2273−2282. doi: 10.1098/rspb.2008.0180
[11]	Berkelmans R, Van Oppen M J H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change[J]. Proceedings of the Royal Society B: Biological Sciences, 2006, 273(1599): 2305−2312. doi: 10.1098/rspb.2006.3567
[12]	Silverstein R N, Cunning R, Baker A C. Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment[J]. Journal of Experimental Biology, 2017, 220(7): 1192−1196.
[13]	Baker A C, Starger C J, Mcclanahan T R, et al. Coral reefs: corals' adaptive response to climate change[J]. Nature, 2004, 430(7001): 741. doi: 10.1038/430741a
[14]	Rowan R. Thermal adaptation in reef coral symbionts[J]. Nature, 2004, 430(7001): 742. doi: 10.1038/430742a
[15]	Krueger T, Hawkins T D, Becker S, et al. Differential coral bleaching-contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress[J]. Comparative Biochemistry and Physiology Part: A Molecular & Integrative Physiology, 2015, 190: 15−25.
[16]	Baker D M, Freeman C J, Wong J C Y, et al. Climate change promotes parasitism in a coral symbiosis[J]. The ISME Journal, 2018, 12(3): 921−930. doi: 10.1038/s41396-018-0046-8
[17]	Little A F, Van Oppen M J H, Willis B L. Flexibility in algal endosymbioses shapes growth in reef corals[J]. Science, 2004, 304(5676): 1492−1494. doi: 10.1126/science.1095733
[18]	Baker A C. Reef corals bleach to survive change[J]. Nature, 2001, 411(6839): 765−766. doi: 10.1038/35081151
[19]	Glynn P W, MatéJ, Baker A C, et al. Coral bleaching and mortality in panamá and ecuador during the 1997-1998 El niño-southern oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event[J]. Bulletin of Marine Science, 2001, 69(1): 79−109.
[20]	Tchernov D, Gorbunov M Y, De Vargas C, et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals[J]. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(37): 13531−13535.
[21]	Huang Yayi, Carballo-Bolaños R, Kuo Chaoyang, et al. Leptoria phrygia in southern taiwan shuffles and switches symbionts to resist thermal-induced bleaching[J]. Scientific Reports, 2020, 10(1): 7808. doi: 10.1038/s41598-020-64749-z
[22]	Fay S A, Weber M X. The occurrence of mixed infections of symbiodinium (dinoflagellata) within individual hosts[J]. Journal of Phycology, 2012, 48(6): 1306−1316. doi: 10.1111/j.1529-8817.2012.01220.x
[23]	Abrego D, Van Oppen M J H, Willis B L. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny[J]. Molecular Ecology, 2009, 18(16): 3532−3543. doi: 10.1111/j.1365-294X.2009.04276.x
[24]	Klepac C N, Barshis D J. Reduced thermal tolerance of massive coral species in a highly variable environment[J]. Proceedings of the Royal Society B: Biological Sciences, 2020, 287(1933): 20201379. doi: 10.1098/rspb.2020.1379
[25]	Stat M, Gates R D. Clade d symbiodinium in scleractinian corals: a “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above?[J]. Journal of Marine Sciences, 2011, 2011(2011): 1−9.
[26]	Warner M E, Fitt W K, Schmidt G W. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching[J]. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(14): 8007−8012.
[27]	Takahashi S, Nakamura T, Sakamizu M, et al. Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals[J]. Plant and Cell Physiology, 2004, 45(2): 251−255. doi: 10.1093/pcp/pch028
[28]	Jones R J, Hoegh-Guldberg O, Larkum A W D, et al. Temperature-induced bleaching of corals begins with impairment of the CO₂ fixation mechanism in zooxanthellae[J]. Plant, Cell & Environment, 1998, 21(12): 1219−1230
[29]	Takahashi S, Whitney S, Itoh S, et al. Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured symbiodinium[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(11): 4203−4208.
[30]	Weis V M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis[J]. Journal of Experimental Biology, 2008, 211(19): 3059−3066. doi: 10.1242/jeb.009597
[31]	Gates R D, Baghdasarian G, Muscatine L. Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching[J]. The Biological Bulletin, 1992, 182(3): 324−332. doi: 10.2307/1542252
[32]	Cunning R, Baker A C. Not just who, but how many: the importance of partner abundance in reef coral symbioses[J]. Frontiers in Microbiology, 2014, 5: 400.
[33]	Fitt W K, Brown B E, Warner M E, et al. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals[J]. Coral Reefs, 2001, 20: 51−65. doi: 10.1007/s003380100146
[34]	Wu Di, Tang Haiping, Qiu Xingyu, et al. Native MS-guided lipidomics to define endogenous lipid microenvironments of eukaryotic receptors and transporters[J]. Nature Protocols, 2025, 20(1): 1−25. doi: 10.1038/s41596-024-01037-4
[35]	Luo Y J, Wang L H, Chen W N U, et al. Ratiometric imaging of gastrodermal lipid bodies in coral–dinoflagellate endosymbiosis[J]. Coral Reefs, 2009, 28(1): 289−301. doi: 10.1007/s00338-008-0462-8
[36]	Yin Huiyong, Xu Libin, Porter N A. Free radical lipid peroxidation: mechanisms and analysis[J]. Chemical Reviews, 2011, 111(10): 5944−5972. doi: 10.1021/cr200084z
[37]	Han Xianlin. Lipidomics for studying metabolism[J]. Nature Reviews Endocrinology, 2016, 12(11): 668−679. doi: 10.1038/nrendo.2016.98
[38]	Endle H, Horta G, Stutz B, et al. AgRP neurons control feeding behaviour at cortical synapses via peripherally derived lysophospholipids[J]. Nature Metabolism, 2022, 4(6): 683−692. doi: 10.1038/s42255-022-00589-7
[39]	Sikorskaya T V, Ermolenko E V, Efimova K V. Lipids of Indo-Pacific gorgonian corals are modified under the influence of microbial associations[J]. Coral Reefs, 2022, 41: 277−291. doi: 10.1007/s00338-022-02222-1
[40]	Greenberg M E, Li Xinmin, Gugiu B G, et al. The lipid whisker model of the structure of oxidized cell membranes[J]. Journal of Biological Chemistry, 2008, 283(4): 2385−2396. doi: 10.1074/jbc.M707348200
[41]	Han Xianlin, Gross R W. The foundations and development of lipidomics[J]. Journal of Lipid Research, 2022, 63(2): 100164. doi: 10.1016/j.jlr.2021.100164
[42]	Domenick T M, Gill E L, Vedam-Mai V, et al. Mass spectrometry-based cellular metabolomics: current approaches, applications, and future directions[J]. Analytical Chemistry, 2021, 93(1): 546−566. doi: 10.1021/acs.analchem.0c04363
[43]	Imbs A B, Latyshev N A, Dautova T, et al. Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae[J]. Marine Ecology Progress Series, 2010, 409: 65−75. doi: 10.3354/meps08622
[44]	Baumann J, Grottoli A G, Hughes A D, et al. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage[J]. Journal of Experimental Marine Biology and Ecology, 2014, 461: 469−478. doi: 10.1016/j.jembe.2014.09.017
[45]	Chen Hungkai, Wang L H, Chen W N U, et al. Coral lipid bodies as the relay center interconnecting diel-dependent lipidomic changes in different cellular compartments[J]. Scientific Reports, 2017, 7: 3244. doi: 10.1038/s41598-017-02722-z
[46]	Revel J, Massi L, Mehiri M, et al. Differential distribution of lipids in epidermis, gastrodermis and hosted Symbiodinium in the sea anemone Anemonia viridis[J]. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2016, 191: 140−151
[47]	Pasaribu B, Lin I P, Tzen J T C, et al. SLDP: a novel protein related to caleosin is associated with the endosymbiotic symbiodinium lipid droplets from euphyllia glabrescens[J]. Marine Biotechnology, 2014, 16(5): 560−571. doi: 10.1007/s10126-014-9574-z
[48]	Fitt W K. Chemosensory responses of the symbiotic dinoflagellate Symbiodinium microadriaticum (dinophyceae)[J]. Journal of Phycology, 1985, 21(1): 62−67. doi: 10.1111/j.0022-3646.1985.00062.x
[49]	Ishikura M, Hagiwara K, Takishita K, et al. Isolation of new symbiodinium strains from tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolidia ianthina) using culture medium containing giant clam tissue homogenate[J]. Marine Biotechnology, 2004, 6(4): 378−385. doi: 10.1007/s10126-004-1800-7
[50]	Krueger T, Gates R D. Cultivating endosymbionts — host environmental mimics support the survival of symbiodinium C15 ex hospite[J]. Journal of Experimental Marine Biology and Ecology, 2012, 413: 169−176. doi: 10.1016/j.jembe.2011.12.002
[51]	Buerger P, Alvarez-ROA C, Coppin C W, et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance[J]. Science Advances, 2020, 6(20): eaba2498. doi: 10.1126/sciadv.aba2498
[52]	覃良云, 许勇前, 陈金妮, 等. 造礁石珊瑚共生虫黄藻离体培养方法的优化[J]. 微生物学报, 2023, 63(4): 1658−1671. Qin Liangyun, Xu Yongqian, Chen Jinni, et al. Optimization of in vitro culture method for zooxanthellae associated with reef-building corals[J]. Acta Microbiologica Sinica, 2023, 63(4): 1658−1671.
[53]	Andersen R A. Algal Culturing Techniques[M]. New York: Academic Press, 2005.
[54]	Goldman J C, Mccarthy J J. Steady state growth and ammonium uptake of a fast-growing marine diatom[J]. Limnology and Oceanography, 1978, 23(4): 695−703. doi: 10.4319/lo.1978.23.4.0695
[55]	Waheed Z, Hoeksema B. Diversity patterns of scleractinian corals at Kota Kinabalu, Malaysia, in relation to exposure and depth[J]. The Raffles Bulletin of Zoology, 2014, 62: 66−82.
[56]	Strychar K, Sammarco P. Effects of heat stress on phytopigments of zooxanthellae (Symbiodinium spp. ) symbiotic with the corals acropora hyacinthus, Porites solida, and Favites complanata[J]. International Journal of Biology, 2012, 4(1).
[57]	Ritchie R J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents[J]. Photosynthesis Research, 2006, 89(1): 27−41. doi: 10.1007/s11120-006-9065-9
[58]	Rijstenbil J W. Assessment of oxidative stress in the planktonic diatom Thalassiosira pseudonana in response to UVA and UVB radiation[J]. Journal of Plankton Research, 2002, 24(12): 1277−1288. doi: 10.1093/plankt/24.12.1277
[59]	Lesser M P, Farrell J H. Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress[J]. Coral Reefs, 2004, 23: 367−377. doi: 10.1007/s00338-004-0392-z
[60]	Buck B H, Rosenthal H, Saint-Paul U. Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas[J]. Aquatic Living Resources, 2002, 15(2): 107−117. doi: 10.1016/S0990-7440(02)01159-2
[61]	Goulet T L, Cook C B, Goulet D. Effect of short‐term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis[J]. Limnology and Oceanography, 2005, 50(5): 1490−1498. doi: 10.4319/lo.2005.50.5.1490
[62]	Muller-Parker G, Pierce-Cravens J, Bingham B L. Broad thermal tolerance of the symbiotic dinoflagellate symbiodinium muscatinei (dinophyta) in the sea anemone Anthopleura elegantissima (cnidaria) from northern latitudes¹[J]. Journal of Phycology, 2007, 43(1): 25−31. doi: 10.1111/j.1529-8817.2006.00302.x
[63]	刘旭. 造礁石珊瑚对温度胁迫的响应机制研究[D]. 南宁: 广西大学, 2020. Liu X. Responsive mechanism of reef-building coral rocks to temperature stress[D]. Nanning: Guangxi University, 2020.
[64]	Murata N, Takahashi S, Nishiyama Y, et al. Photoinhibition of photosystem II under environmental stress[J]. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2007, 1767(6): 414−421. doi: 10.1016/j.bbabio.2006.11.019
[65]	Nishiyama Y, Allakhverdiev S I, Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II[J]. Biochimica Et Biophysica Acta(BBA)-Bioenergetics, 2006, 1757(7): 742−749. doi: 10.1016/j.bbabio.2006.05.013
[66]	Venn A A, Loram J E, Douglas A E. Photosynthetic symbioses in animals[J]. Journal of Experimental Botany, 2008, 59(5): 1069−1080. doi: 10.1093/jxb/erm328
[67]	Del Rio D, Stewart A J, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress[J]. Nutrition, Metabolism and Cardiovascular Diseases, 2005, 15(4): 316−328. doi: 10.1016/j.numecd.2005.05.003
[68]	Fridovich I. Superoxide anion radical (O·̄₂), superoxide dismutases, and related matters[J]. Journal of Biological Chemistry, 1997, 272(30): 18515−18517. doi: 10.1074/jbc.272.30.18515
[69]	Barshis D J, Ladner J T, Oliver T A, et al. Lineage-Specific transcriptional profiles of symbiodinium spp. unaltered by heat stress in a coral host[J]. Molecular Biology and Evolution, 2014, 31(6): 1343−1352. doi: 10.1093/molbev/msu107
[70]	Rosic N N, Pernice M, Dove S, et al. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching[J]. Cell Stress and Chaperones, 2011, 16(1): 69−80. doi: 10.1007/s12192-010-0222-x
[71]	Li-Beisson Y, Thelen J J, Fedosejevs E, et al. The lipid biochemistry of eukaryotic algae[J]. Progress in Lipid Research, 2019, 74: 31−68. doi: 10.1016/j.plipres.2019.01.003
[72]	Maxfield F R, Tabas I. Role of cholesterol and lipid organization in disease[J]. Nature, 2005, 438(7068): 612−621. doi: 10.1038/nature04399
[73]	Veldhuis M, Gijsbert K, Timmermans K. Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth[J]. European Journal of Phycology, 2001, 36(2): 167−177. doi: 10.1080/09670260110001735318
[74]	Shevchenko A, Simons K. Lipidomics: coming to grips with lipid diversity[J]. Nature Reviews Molecular Cell Biology, 2010, 11(8): 593−598. doi: 10.1038/nrm2934
[75]	Li F Q, Vierstra R D. Autophagy: a multifaceted intracellular system for bulk and selective recycling[J]. Trends in plant science, 2012, 17(9): 526−537. doi: 10.1016/j.tplants.2012.05.006
[76]	Singh R, Kaushik S, Wang Y Q, et al. Autophagy regulates lipid metabolism[J]. Nature, 2009, 458(7242): 1131−1135. doi: 10.1038/nature07976
[77]	Hou Q C, Ufer G, Bartels D. Lipid signalling in plant responses to abiotic stress[J]. Plant, Cell & Environment, 2016, 39(5): 1029−1048
[78]	Berkowitz L, Cabrera-Reyes F, Salazar C, et al. Sphingolipid profiling: a promising tool for stratifying the metabolic syndrome-associated risk[J]. Frontiers in Cardiovascular Medicine, 2022, 8: 785124. doi: 10.3389/fcvm.2021.785124
[79]	Huang W C, Chen C L, Lin Y S, et al. Apoptotic sphingolipid ceramide in cancer therapy[J]. Journal of Lipids, 2011, 2011: 565316.
[80]	Sun X F, Li Y, Du J, et al. Targeting ceramide transfer protein sensitizes AML to FLT3 inhibitors via a GRP78-ATF6-CHOP axis[J]. Nature Communications, 2025, 16(1): 1358. doi: 10.1038/s41467-025-56520-7
[81]	Li Y Z, Wang L C, Wang H M, et al. Polysaccharides from Eucommia ulmoides Oliv. leaves alleviates alcohol-induced mouse brain injury and BV-2 microglial dysfunction[J]. International Journal of Biological Macromolecules, 2024, 273: 132887. doi: 10.1016/j.ijbiomac.2024.132887
[82]	Zhang M, Su R N, Corazzin M, et al. Lipid transformation during postmortem chilled aging in Mongolian sheep using lipidomics[J]. Food Chemistry, 2023, 405: 134882. doi: 10.1016/j.foodchem.2022.134882