Genetic diversity of potentially free-living Symbiodinium in the Xisha Islands, South China Sea: Implications for the resilience of coral reefs

Authors

  • Guowei Zhou Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  • Hui Huang Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  • Ziniu Yu Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
  • Zhijun Dong Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China
  • Yuanchao Li Hainan Marine Development and Design Institute, Haikou 570125, China

Keywords:

chloroplast 23S hypervariable region, dinoflagellate, zooxanthellae

Abstract

Free-living Symbiodinium have been the focus of considerable attention among coral reef researchers because they represent a source of symbionts for both recently recruited corals and adult corals that are subject to environmental stress (e.g. climate change). We evaluated the genetic diversity of free-living Symbiodinium in seawater collected from the Xisha Islands in the South China Sea using sequence analysis of the hypervariable region of the chloroplast 23S. We sequenced a total of 267 cloned gene fragments representing Symbiodinium in clades A, B, C, D, F, and G, of which 34 were distinct types. The diversity of free-living Symbiodinium types was high at all sites. The majority of Symbiodinium sequences belonged to clade C. There was no significant difference in Symbiodinium sequence types among sites or depths. Our results highlight the high diversity of free-living Symbiodinium pools in the coral reef environment and provide a foundation for future studies of the spatiotemporal distribution of Symbiodinium. Such information is critical to understand and predict the influence of symbiotic dinoflagellates on the adaptation of their host to environmental changes.

References

Baker, A. C. 2003. Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. S., 34: 661–689.

Baker, A. C., Starger, C. J., McClanahan, T. R. and Glynn, P. W. 2004. Corals’ adaptive response to climate change. Nature, 430: 741–741.

Berkelmans, R. and van Oppen, M. J.H. 2006. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. P. R. Soc. B., 273: 2305–2312.

Buddemeier, R. W. and Fautin, D. G. 1993. Coral bleaching as an adaptive mechanism-a testable hypothesis. Bioscience, 43: 320–326.

Carlos, A. A., Baillie, B. K., Kawachi, M. and Maruyama, T. 1999. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J. Phycol., 35: 1054–1062.

Clarke, K. R. and Warwick, R. M. 2001. Change in marine communities: an approach to statistical analysis and interpretation, 2nd Edition, Plymouth: PRIMER-E.

Coffroth, M. A. and Santos, S. R. 2005. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156: 19–34.

Coffroth, M. A., Lewis, C. F., Santos, S. R. and Weaver, J. L. 2006. Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr. Biol., 16: R985–R987.

Coffroth, M. A., Poland, D. M., Petrou, E. L., Brazeau, D. A. and Holmberg, J. C. 2010. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoSONE, 5(10): e13258

Dong, Z. J., Huang, H., Huang, L. M. and Li, Y. C. 2009. Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the Xisha Islands in the South China Sea. J. Syst. Evol., 47: 321–326.

Fitt, W. K. and Trench, R. K. 1983. The relation of diel patterns of cell-division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New. Phytol., 94: 421–432.

Gou, W. L., Sun, J., Li, X. Q., Zhen, Y., Xin, Z. Y., Yu, Z. G. and Li, R. X. 2003. Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, PR China. J. Exp. Mar. Biol. Ecol., 296: 135–144.

Hirose, M., Reimer, J. D., Hidaka, M. and Suda, S. 2008. Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar. Biol., 155: 105–112.

Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res., 50: 839–866.

Howells, E. J., van Oppen, M. J.H. and Willis, B. L. 2009. High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs, 28: 215–225.

Huang, H., Dong, Z. J., Huang, L. M. and Zhang, J. B. 2006. Restriction fragment length polymorphism analysis of large subunit rDNA of symbiotic dinoflagellates from scleractinian corals in the Zhubi Coral Reef of the Nansha Islands. J., 48: 148–152. Integr. Plant Biol.

Jones, A. M., Berkelmans, R., van Oppen, M. J.H., Mieog, J. C. and Sinclair, W. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. P. R. Soc. B., 275: 1359–1365.

Jones, R. J. and Yellowlees, D. 1997. Regulation and control of intracellular algae (equals zooxanthellae) in hard corals. Philos. T. Roy. Soc. B., 352: 457–468.

LaJeunesse, T. C., Thornhill, D. J., Cox, E. F., Stanton, F. G., Fitt, W. K. and Schmidt, G. W. 2004. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs, 23: 596–603.

LaJeunesse, T. C., Smith, R. T., Finney, J. and Oxenford, H. 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. P. R. Soc. B., 276: 4139–4148.

LaJeunesse, T. C., Smith, R., Walther, M., Pinzo, J., Pettay, D. T., McGinley, M., Aschaffenburg, M., Medina-Rosas, P., Cupul-Magan, A. L., Peez, A. L., Reyes-Bonilla, H. and Warner, M. E. 2010. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. P. R. Soc. B., 277: 2925–2934.

Lewis, C. L. and Coffroth, M. A. 2004. The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science, 304: 1490–1492.

Little, A. F., van Oppen, M. J.H. and Willis, B. L. 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304: 1492–1494.

Littman, R. A., van Oppen, M. J.H. and Willis, B. L. 2008. Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J. Exp. Mar. Biol. Ecol., 364: 48–53.

Manning, M. M. and Gates, R. D. 2008. Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol. Oceanogr., 53: 1853–1861.

Mieog, J. C., van Oppen, M. J.H., Cantin, N. E., Stam, W. T. and Olsen, J. L. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs, 26: 449–457.

Pochon, X. and Pawlowski, J. 2006. Evolution of the soritids-Symbiodinium symbiosis. Symbiosis, 42: 77–88.

Pochon, X. and Gates, R. D. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol. Phylogenet. Evol., 56: 492–497.

Pochon, X., Montoya-Burgos, J. I., Stadelmann, B. and Pawlowski, J. 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phylogenet. Evol., 38: 20–30.

Pochon, X., Stat, M., Takabayashi, M., Chasqui, L., Chauka, L. J., Logan, D. D.K. and Gates, R. D. 2010. Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J. Phycol., 46: 53–65.

Porto, I., Granados, C., Restrepo, J. C. and Sanchez, J. A. 2008. Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE, 3: 2161–2165.

Rowan, R. 2004. Coral bleaching-Thermal adaptation in reef coral symbionts. Nature, 430: 742–742.

Rowan, R. and Powers, D. A. 1991. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science, 251: 1348–1351.

Santos, S.R., Taylor, D.J., Kinzie, R.A., Sakai, K. and Coffroth, M.A. 2002. Evolution of length variation and heteroplasmy in the chloroplast rDNA of symbiotic dinoflagellates (Symbiodinium, Dinophyta) and a novel insertion in the universal core region of the large subunit rDNA. Phycologia, 41: 311–318.

Stat, M., Carter, D. and Hoegh-Guldberg, O. 2006. The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol. Evol. Syst., 8: 23–46.

Tamura, K., Dudley, J., Nei, M. and Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol., 24(8): 1596–1599.

Thompson, J. D., Higgins, D. G. and Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22: 4673–4680.

Thornhill, D. J., Daniel, M. W., LaJeunesse, T. C., Schmidt, G. W. and Fitt, W. K. 2006. Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. J. Exp. Mar. Biol. Ecol., 338: 50–56.

Thornhill, D. J., Xiang, Y., Fitt, W. K. and Santos, S. R. 2009. Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLos ONE, 4: e6262

van Oppen, M. J.H., Palstra, F. P., Piquet, A. M.T. and Miller, D. J. 2001. Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. P. R. Soc. B., 268: 2617–2617.

Venera-Ponton, D. E., Diaz-Pulido, G., Rodriguez-Lanetty, M. and Hoegh-Guldberg, O. 2010. Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs, 29: 1049–1060.

Yacobovitch, T., Benayahu, Y. and Weis, V. M. 2004. Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). J. Exp. Mar. Biol. Ecol., 298: 35–48.

Published

2012-04-01