Symbiodinium IN CORAL REEFS AND ITS ADAPTATION RESPONSES TOWARD CORAL BLEACHING EVENTS: A REVIEW

https://doi.org/10.55230/mabjournal.v51i3.2162

Authors

  • NURUL SHAFIQA-YUSOF INSTITUTE OF MARINE BIOTECHNOLOGY, UNIVERSITI MALAYSIA TERENGGANU, TERENGGANU, MALAYSIA
  • NUR SYAHIRAH MOHD RADZI Institute of Oceanography and Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

Keywords:

Adaptation Mechanisms, climate change, coral bleaching, Symbiodinium

Abstract

Symbiodinium is a category of symbiotic dinoflagellates commonly associated with various reef-building corals. Detrimental impacts of global climate change worsen the mutualistic association of coral-Symbiodinium, endangering the reefs to the bleaching and mass mortality phenomenon. Destruction of coral reef ecosystems has adverse effects not only on marine life but also on the human population. It has been proposed that to protect the coral reefs, an exclusive selection of thermal-tolerance traits in Symbiodinium will increase the survivability of coral reefs. However, there are still limited findings on the coral-endosymbiont resistance under adverse environments. Thus, this review aims to introduce shortly the coral reefs, Symbiodinium, and coral bleaching events, as well as to provide brief reviews of cellular and molecular responses in Symbiodinium to tackle thermal stress. Considering the potential applications of this knowledge to confront the threat of coral bleaching prevalence, more study especially in terms of cellular and molecular responses by omics approaches is needed to enhance the understanding of coral-Symbiodinium tolerance toward climate change, particularly heat stress.

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References

Abdullah, A.L., Anscelly, A.A., Mohamed, J. & Yasin, Z. 2016. Conservation of Pulau Payar Marine Park and Optical Remote Sensing Models. KEMANUSIAAN: The Asian Journal of Humanities, 23(1): 79–107. DOI: https://doi.org/10.21315/kajh2016.23.2.1

Baker, A. C. 2003. Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics, 34(1): 661–689. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132417

Biquand, E., Okubo, N., Aihara, Y., Rolland, V., Hayward, D.C., Hatta, M., Minagawa, J., Maruyama, T. & Takahashi, S. 2017. Acceptable symbiont cell size differs among cnidarian species and may limit symbiont diversity. The ISME Journal, 11(7): 1702-1712. DOI: https://doi.org/10.1038/ismej.2017.17

Bongaerts, P., Carmichael, M., Hay, K.B., Tonk, L., Frade, P.R. & Hoegh-Guldberg, O. 2015. Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. Royal Society Open Science, 2(2): 140297. DOI: https://doi.org/10.1098/rsos.140297

Buerger, P., Alvarez-Roa, C., Coppin, C.W., Pearce, S.L., Chakravarti, L.J., Oakeshott, J.G., Edwards, O.R. & van Oppen, M.J.H. 2020. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Science Advances, 6(20): eaba2498. DOI: https://doi.org/10.1126/sciadv.aba2498

Chan, W.Y., Oakeshott, J.G., Buerger, P., Edwards, O.R. & van Oppen, M.J. 2021. Adaptive responses of free‐living and symbiotic microalgae to simulated future ocean conditions. Global Change Biology, 27(9): 1737-1754. DOI: https://doi.org/10.1111/gcb.15546

Chakravarti, L.J. & van Oppen, M.J.H. 2018. Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Frontiers in Marine Science, 5: 227. DOI: https://doi.org/10.3389/fmars.2018.00227

Cziesielski, M.J., Liew, Y.J., Cui, G., Schmidt-Roach, S., Campana, S., Marondedze, C. & Aranda, M. 2018. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts, in: Proceedings of the Royal Society B: Biological Sciences. 285(1877): 20172654. DOI: https://doi.org/10.1098/rspb.2017.2654

Davies, S.W., Ries, J.B., Marchetti, A. & Castillo, K.D. 2018. Symbiodinium functional diversity in the coral Siderastrea siderea is influenced by thermal stress and reef environment, but not ocean acidification. Frontiers in Marine Science, 5: 150. DOI: https://doi.org/10.3389/fmars.2018.00150

Diaz, J.M. & Plummer, S. 2018. Production of extracellular reactive oxygen species by phytoplankton: past and future directions. Journal of Plankton Research, 40(6): 655-666. DOI: https://doi.org/10.1093/plankt/fby039

Douglas, A.E. 2009. Endosymbionts and intracellular parasites. In: Encyclopedia of Microbiology (Third Edition). M. Schaechter (Ed.). Elsevier, California. pp. 128-141. DOI: https://doi.org/10.1016/B978-012373944-5.00257-1

Dutra, L.X., Haywood, M.D., Singh, S., Ferreira, M., Johnson, J.E., Veitayaki, J., Kininmonth, S., Morris, C.W. & Piovano, S. 2021. Synergies between local and climate-driven impacts on coral reefs in the Tropical Pacific: A review of issues and adaptation opportunities. Marine Pollution Bulletin, 164: 111922. DOI: https://doi.org/10.1016/j.marpolbul.2020.111922

Farag, M.A., Meyer, A., Ali, S.E., Salem, M.A., Giavalisco, P., Westphal, H. & Wessjohann, L.A. 2018. Comparative metabolomics approach detects stress-specific responses during coral bleaching in soft corals. Journal of Proteome Research, 17(6): 2060-2071. DOI: https://doi.org/10.1021/acs.jproteome.7b00929

Fisher, P.L., Malme, M.K. & Dove, S. 2012. The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs, 31(2): 473-485. DOI: https://doi.org/10.1007/s00338-011-0853-0

Gan, S.H., Waheed, Z., Chung, F.C., Spiji, D.A., Sikim, L., Saleh, E. & Tan, C.H. 2021. In situ observations of coral spawning and spawn slick at Lankayan Island, Sabah, Malaysia. Marine Biodiversity, 51(1): 1-7. DOI: https://doi.org/10.1007/s12526-020-01158-5

Gardner, S.G., Raina, J.B., Ralph, P.J. & Petrou, K. 2017. Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress. Journal of Experimental Biology, 220(10): 1787-1791. DOI: https://doi.org/10.1242/jeb.153049

Gierz, S.L., Forêt, S. & Leggat, W. 2017. Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Frontiers in Plant Science, 8: 271. DOI: https://doi.org/10.3389/fpls.2017.00271

Goyen, S., Pernice, M., Szabó, M., Warner, M.E., Ralph, P.J. & Suggett, D.J. 2017. A molecular physiology basis for functional diversity of hydrogen peroxide production amongst Symbiodinium spp. (Dinophyceae). Marine Biology, 164(3): 46. DOI: https://doi.org/10.1007/s00227-017-3073-5

Grégoire, V., Schmacka, F., Coffroth, M.A. & Karsten, U. 2017. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). Journal of Applied Phycology, 29(4): 1893-1905. DOI: https://doi.org/10.1007/s10811-017-1127-1

Harrison, J.W., Silsbe, G.M. & Smith, R.E. 2015. Photophysiology and its response to visible and ultraviolet radiation in freshwater phytoplankton from contrasting light regimes. Journal of Plankton Research, 37(2): 472-488. DOI: https://doi.org/10.1093/plankt/fbv003

Hillyer, K.E., Dias, D.A., Lutz, A., Wilkinson, S.P., Roessner, U. & Davy, S.K. 2017. Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs, 36(1): 105-118. DOI: https://doi.org/10.1007/s00338-016-1508-y

Hoadley, K.D., Lewis, A.M., Wham, D.C., Pettay, D.T., Grasso, C., Smith, R., Kemp, D.W., LaJeunesse, T.C. & Warner, M.E. 2019. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Scientific Reports, 9(1): 1-15. DOI: https://doi.org/10.1038/s41598-019-46412-4

Hoegh-Guldberg, O., Poloczanska, E.S., Skirving, W. & Dove, S. 2017. Coral reef ecosystems under climate change and ocean acidification. Frontiers in Marine Science, 4: 158. DOI: https://doi.org/10.3389/fmars.2017.00158

Hull, R., Head, G. & Tzotzos, G.T. 2020. Current progress and future needs of genetically engineered crop plants. In: Genetically Modified Plants (Second Edition): Assessing Safety and Managing Risk. R. Hull, G. Head and G.T. Tzotzos (Eds.). Academic Press, London. pp. 83-97. DOI: https://doi.org/10.1016/B978-0-12-818564-3.00003-2

Ismail, M.S. & Goeden, G.B. 2020. Assessment of coral reefs community health in Pulau Berhala, Pahang, Malaysia. Journal of PeerScientist, 2(1): e1000017.

Khodzori, F.A., Saad, S. & Rani, H. 2021. Spatial and Temporal Variation of Scleractinian Coral Recruitment in Balok Coastal Waters and Bidong Island, Malaysia. Malaysian Journal of Applied Sciences, 6(1): 1-14. DOI: https://doi.org/10.37231/myjas.2021.6.1.246

Ladner, J.T., Barshis, D.J. & Palumbi, S.R. 2012. Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evolutionary Biology, 12(1): 1-13. DOI: https://doi.org/10.1186/1471-2148-12-217

LaJeunesse, T.C., Parkinson, J.E., Gabrielson, P.W., Jeong, H.J., Reimer, J.D., Voolstra, C.R. & Santos, S.R. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28(16): 2570-2580. DOI: https://doi.org/10.1016/j.cub.2018.07.008

LaJeunesse, T.C., Parkinson, J.E. & Reimer, J.D. 2012. A genetics‐based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov.(Dinophyceae), two dinoflagellates symbiotic with cnidaria. Journal of Phycology, 48(6): 1380-1391. DOI: https://doi.org/10.1111/j.1529-8817.2012.01217.x

Lin, S., Yu, L. & Zhang, H. 2018. Transcriptomic responses to thermal stress and varied phosphorus conditions in Symbiodinium kawagutii. BioRxiv, 499210. DOI: https://doi.org/10.3390/microorganisms7040096

Liu, H., Stephens, T.G., González-Pech, R.A., Beltran, V.H., Lapeyre, B., Bongaerts, P., Cooke, I, Aranda, M., Bourne, D.G., Forêt, S., Miller, D.J., van Oppen, M.J.H., Voolstra, C.R., Ragan, M.A. & Chan, C.X. 2018. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Communications Biology, 1(1): 1-11. DOI: https://doi.org/10.1038/s42003-018-0117-4

Loh, I.H., Chong, J.L. & Baird, M.H. 2018. The conservation of coral reefs through mangrove management. Biodiversity, 19(1-2): 95-100. DOI: https://doi.org/10.1080/14888386.2018.1473168

Lohr, K.E., Khattri, R.B., Guingab-Cagmat, J., Camp, E.F., Merritt, M.E., Garrett, T.J. & Patterson, J.T. 2019. Metabolomic profiles differ among unique genotypes of a threatened Caribbean coral. Scientific Reports, 9(1): 1-11. DOI: https://doi.org/10.1038/s41598-019-42434-0

Louis, Y.D., Kaullysing, D., Gopeechund, A., Mattan-Moorgawa, S., Bahorun, T., Dyall, S. D. & Bhagooli, R. 2016. In hospite Symbiodinium photophysiology and antioxidant responses in Acropora muricata on a coast-reef scale: implications for variable bleaching patterns. Symbiosis, 68(1-3): 61-72. DOI: https://doi.org/10.1007/s13199-016-0380-4

Malerba, M.E., Palacios, M.M., Palacios Delgado, Y.M., Beardall, J. & Marshall, D.J. 2018. Cell size, photosynthesis and the package effect: an artificial selection approach. New Phytologist, 219(1): 449-461. DOI: https://doi.org/10.1111/nph.15163

Matthews, J.L., Raina, J.B., Kahlke, T., Seymour, J.R., van Oppen, M.J. & Suggett, D.J. 2020. Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks. Environmental Microbiology, 22(5): 1675-1687. DOI: https://doi.org/10.1111/1462-2920.14918

Mayfield, A.B., Chen, Y.J., Lu, C.Y. & Chen, C.S. 2018. The proteomic response of the reef coral Pocillopora acuta to experimentally elevated temperatures. PloS One, 13(1): e0192001. DOI: https://doi.org/10.1371/journal.pone.0192001

Morikawa, M.K. & Palumbi, S.R. 2019. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proceedings of the National Academy of Sciences, 116(21): 10586-10591. DOI: https://doi.org/10.1073/pnas.1721415116

Nakajima, R., Yamazaki, H., Lewis, L.S., Khen, A., Smith, J.E., Nakatomi, N. & Kurihara, H. 2017. Planktonic trophic structure in a coral reef ecosystem–Grazing versus microbial food webs and the production of mesozooplankton. Progress in Oceanography, 156: 104-120. DOI: https://doi.org/10.1016/j.pocean.2017.06.007

Nand, A., Zhan, Y., Salazar, O.R., Aranda, M., Voolstra, C.R. & Dekker, J. 2021. Genetic and spatial organization of the unusual chromosomes of the dinoflagellate Symbiodinium microadriaticum. Nature Genetics, 53(5): 618-629. DOI: https://doi.org/10.1038/s41588-021-00841-y

Nielsen, D.A., Petrou, K. & Gates, R.D. 2018. Coral bleaching from a single cell perspective. The ISME Journal, 12(6): 1558-1567. DOI: https://doi.org/10.1038/s41396-018-0080-6

Oakley, C.A., Ameismeier, M.F., Peng, L., Weis, V.M., Grossman, A.R. & Davy, S.K. 2016. Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia. Cellular Microbiology, 18(7): 1009-1023. DOI: https://doi.org/10.1111/cmi.12564

Oakley, C.A. & Davy, S.K. 2018. Cell biology of coral bleaching. In: Coral bleaching. van M.J.H. Oppen and J.M. Lough (Eds.). Springer, Cham. pp. 189-211. DOI: https://doi.org/10.1007/978-3-319-75393-5_8

Petrou, K., Nielsen, D.A. & Heraud, P. 2018. Single-cell biomolecular analysis of coral algal symbionts reveals opposing metabolic responses to heat stress and expulsion. Frontiers in Marine Science, 5: 110. DOI: https://doi.org/10.3389/fmars.2018.00110

Pochon, X. & Gates, R.D. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Molecular Phylogenetics and Evolution, 56(1): 492-497. DOI: https://doi.org/10.1016/j.ympev.2010.03.040

Pochon, X., LaJeunesse, T.C. & Pawlowski, J. 2004. Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Marine Biology, 146(1): 17-27. DOI: https://doi.org/10.1007/s00227-004-1427-2

Qin, Z., Yu, K., Chen, B., Wang, Y., Liang, J., Luo, W., Xu, L. & Huang, X. 2019. Diversity of Symbiodiniaceae 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

Reich, H.G., Kitchen, S. A., Stankiewicz, K.H., Devlin-Durante, M., Fogarty, N.D. & Baums, I.B. 2021. Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium ‘fitti’) among closely related coral hosts. Molecular Ecology, 30(14): 3500-3514. DOI: https://doi.org/10.1111/mec.15952

Rohrscheib, C.E. & Brownlie, J.C. 2013. Microorganisms that manipulate complex animal behaviours by affecting the host’s nervous system. Springer Science Reviews, 1(1): 133-140. DOI: https://doi.org/10.1007/s40362-013-0013-8

Rowan, R. 2004. Thermal adaptation in reef coral symbionts. Nature, 430(7001): 742. DOI: https://doi.org/10.1038/430742a

Solayan, A. 2016. Biomonitoring of coral bleaching-A glimpse on biomarkers for the early detection of oxidative damages in corals. In: Invertebrates: Experimental Models in Toxicity Screening. M.L. Larramendy and S. Soloneski (Eds.). Intech, Croatia. pp. 101-117. DOI: https://doi.org/10.5772/61831

Sogin, E.M., Putnam, H.M., Nelson, C.E., Anderson, P. & Gates, R.D. 2017. Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environmental Microbiology Reports, 9(3): 310-315. DOI: https://doi.org/10.1111/1758-2229.12541

Suggett, D.J., Goyen, S., Evenhuis, C., Szabó, M., Pettay, D.T., Warner, M.E., & Ralph, P.J. 2015. Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytologist, 208(2): 370-381. DOI: https://doi.org/10.1111/nph.13483

Szabó, M., Larkum, A.W.D. & Vass, I. 2020. A Review: The Role of Reactive Oxygen Species in Mass Coral Bleaching. In: Photosynthesis in Algae: Biochemical and Physiological Mechanisms. A. Larkum, A. Grossman and J. Raven (Eds.). Springer, Cham. pp. 459-488. DOI: https://doi.org/10.1007/978-3-030-33397-3_17

Tan, Y.T.R., Wainwright, B.J., Afiq-Rosli, L., Ip, Y.C.A., Lee, J.N., Nguyen, N.T.H., Pointing, S.B. & Huang, D. 2020. Endosymbiont diversity and community structure in Porites lutea from Southeast Asia are driven by a suite of environmental variables. Symbiosis, 80(3): 269-277. DOI: https://doi.org/10.1007/s13199-020-00671-2

Tolleter, D., Seneca, F.O., DeNofrio, J.C., Krediet, C.J., Palumbi, S.R., Pringle, J.R. & Grossman, A.R. 2013. Coral bleaching independent of photosynthetic activity. Current Biology, 23(18): 1782-1786. DOI: https://doi.org/10.1016/j.cub.2013.07.041

Tonk, L., Sampayo, E.M., Weeks, S., Magno-Canto, M. & Hoegh-Guldberg, O. 2013. Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLoS One, 8(7): e68533. DOI: https://doi.org/10.1371/journal.pone.0068533

Waheed, Z. & Hoeksema, B.W. 2014. Diversity patterns of Scleractinian corals at Kota Kinabalu, Malaysia, in relation to exposure and depth. Raffles Bulletin of Zoology, 62: 66-82.

Wham, D.C., Ning, G. & LaJeunesse, T.C. 2017. Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia, 56(4): 396-409. DOI: https://doi.org/10.2216/16-86.1

Wong, H.S. & Yong, C.C. 2020. Fisheries regulation: a review of the literature on input controls, the ecosystem, and enforcement in the straits of Malacca of Malaysia. Fisheries Research, 230: 105682. DOI: https://doi.org/10.1016/j.fishres.2020.105682

Wietheger, A., Starzak, D.E., Gould, K.S. & Davy, S.K. 2018. Differential ROS generation in response to stress in Symbiodinium spp. The Biological Bulletin, 234(1): 11-21. DOI: https://doi.org/10.1086/696977

Published

30-09-2022

How to Cite

SHAFIQA-YUSOF, N., & MOHD RADZI, N. S. (2022). Symbiodinium IN CORAL REEFS AND ITS ADAPTATION RESPONSES TOWARD CORAL BLEACHING EVENTS: A REVIEW. Malaysian Applied Biology, 51(3), 1–15. https://doi.org/10.55230/mabjournal.v51i3.2162

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Review Articles