Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
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Two anthozoans, Entacmaea quadricolor (order Actiniaria) and Alveopora japonica (order Scleractinia), host consistent genotypes of Symbiodinium spp. across geographic ranges in the northwestern Pacific Ocean

  • Received : 2011.03.13
  • Accepted : 2011.05.29
  • Published : 2011.12.31
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Abstract

The actiniarian sea anemone, Entacmaea quadricolor, and the scleractinian coral, Alveopora japonica, host symbiotic dinoflagellates belonging to the genus Symbiodinium (Freudenthal). We studied the host-symbiont specificity of these two anthozoan hosts in the northwestern Pacific Ocean. Symbionts within the two hosts were identified using partial large subunit (LSU) ribosomal DNA (rDNA) and complete internal transcribed spacers (ITS) 1 rDNA regions. The host, E. quadricolor, was identified using the partial LSU rDNA molecular marker. Genetic analysis showed that E. quadricolor only harbors dinoflagellates belonging to subclade C1/3 of the genus Symbiodinium. Moreover, no genetic variation was detected among the symbionts of E. quadricolor within the study region (Korea and Japan), even though the two distant sites were separated by more than 1000 km, at collection depths of 1 m in shallow and 13-16 m in deep water. Whilst scleractinian corals host multiple Symbiodinium clades in tropical waters, A. japonica, sampled over a wide geographical range (800 km) within the study region, only hosts Symbiodinium sp. clade F3. The high specificity of endosymbionts in E. quadricolor and A. japonica within the northwestern Pacific Ocean could be accounted for because symbiotic dinoflagellates within the host anemones appear to be acquired maternally, and the Kuroshio Current might affect the marine biota of the northwestern Pacific. However, the consistency of the symbiotic relationships between these two anthozoan hosts and their endosymbionts could change after climate change, so this symbiotic specificity should be monitored.

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References

  1. Allen GR. 1975. The anemonefishes. Their classification and biology. 2nd ed. Neptune City, NJ: TFH Publishing. 351 pp.
  2. Baker AC. 1999. The symbiosis ecology of reef-building corals [PhD thesis]. Miami: Rosenstiel School of Marine and Atmospheric Science, University of Miami.120p.
  3. Baker AC. 2001. Reef corals bleach to survive change. Nature. 411:765-766. https://doi.org/10.1038/35081151
  4. Baker AC. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst. 34:661-689. https://doi.org/10.1146/annurev.ecolsys.34.011802.132417
  5. Baker AC, Starger CJ, McClanahan TR, Glynn PW. 2004. Corals' adaptive response to climate change. Nature. 430:741. https://doi.org/10.1038/430741a
  6. Barneah O, Weis VN, Perez S, Benayahu Y. 2004. Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser. 275:89-95. https://doi.org/10.3354/meps275089
  7. Bui B, Hoegh-Guldberg O, Low W, Carter D. 2000. Analyzing the diversity of symbiotic dinoflagellates (zooxanthellae) using molecular approachAust Soc Microbiol Conf Poster No. P1.22
  8. Carlos AA, Baillie BK, Kawachi M, Maruyama T. 1999. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from Tridacnids (Bivalvia), Cardids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a freeliving strain. J Phycol. 35:1054-1062. https://doi.org/10.1046/j.1529-8817.1999.3551054.x
  9. Chen CA, Odorico DM, ten Lohuis M, Veron JEN, Miller DJ. 1995. Systematic relationships within the Anthozoa (Cnidaria: Anthozoa) using the 5'-end of the 28S rDNA. Mol Phylogenet Evol 4:175-183. https://doi.org/10.1006/mpev.1995.1017
  10. Davy SK, Turner JR. 2003. Early development and acquisition of zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks). Biol Bull. 205: 66-72. https://doi.org/10.2307/1543446
  11. Davy SK, Lucas IAN, Turner JR. 1997. Uptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennant). Biol Bull. 192:208-216. https://doi.org/10.2307/1542715
  12. Dunn DF. 1981. The clownfish sea anemone: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Phil Soc. 71:1-115.
  13. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 39:783-791 https://doi.org/10.2307/2408678
  14. Harii S, Omori M, Yamakawa H, Koike Y. 2001. Sexual reproduction and larval settlement of the zooxanthellate Alveopora japonica Eguchi at high latitudes. Coral Reefs. 20:19-23. https://doi.org/10.1007/s003380000134
  15. Hoegh-Guldberg O, Salvat B. 1995. Periodic mass-bleaching and elevated sea temperatures: Bleaching of outer reef slope communities in Moorea, French Polynesia. Mar Ecol Prog Ser. 121:181-190. https://doi.org/10.3354/meps121181
  16. Iglesias-Prieto R, Trench RK. 1994. Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser. 113:163-175. https://doi.org/10.3354/meps113163
  17. Jokiel PL, Coles SL. 1990. Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs. 8:155-162. https://doi.org/10.1007/BF00265006
  18. LaJeunesse TC. 2001. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a species level marker. J Phycol. 37:866-880. https://doi.org/10.1046/j.1529-8817.2001.01031.x
  19. LaJeunesse TC. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol. 141:387-400. https://doi.org/10.1007/s00227-002-0829-2
  20. LaJeunesse TC. 2005. ''Species'' radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol. 22:570-581. https://doi.org/10.1093/molbev/msi042
  21. LaJeunesse TC, Trench RK. 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull. 199:126-134. https://doi.org/10.2307/1542872
  22. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura O, Hoegh-Guldberg O, Fitt WK. 2010. Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr. 37:785-800. https://doi.org/10.1111/j.1365-2699.2010.02273.x
  23. Loh WKW, Toha L, Carter D, Hoegh-Guldberg O. 2001. Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser. 222:97-107. https://doi.org/10.3354/meps222097
  24. Loi T. 1998. Molecular diversity of the predominant clade C zooxanthellae from scleractinian corals of the Great Barrier Reef. Honours thesis. Department of Microbiology. The University of Sydney, Sydney.
  25. Muller-Parker G, Davy SK. 2001. Temperate and tropical algalsea anemone symbioses. Invert Biol. 120:104-123. https://doi.org/10.1111/j.1744-7410.2001.tb00115.x
  26. Muscatine L, Grossman D, Doino J. 1991. Release of symbiotic algae by tropical anemones and corals after cold shock. Mar Ecol Prog Ser. 77:233-243. https://doi.org/10.3354/meps077233
  27. Ono S, Reimer JD, Nozawa Y, Tsukahara J. 2010. Long-term changes of infra-littoral zone zooxanthellae cnidarians in the Taisho lava field, Sakurajima, Kagoshima, Japan. Galaxia. 12:15-22. https://doi.org/10.3755/galaxea.12.15
  28. Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ. 2001. Molecular identification of algal endosymbionts in large miliolid foraminifera. 2. Dinoflagellates. J Eukar Microbiol. 48:368-373. https://doi.org/10.1111/j.1550-7408.2001.tb00326.x
  29. Pochon X, Pawlowski J, Zaninetti L, Rowan R. 2001. High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol. 139:1069-1078. https://doi.org/10.1007/s002270100674
  30. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J. 2006. Molecular phylogeny, evolutionary rates and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol. 38:20-30. https://doi.org/10.1016/j.ympev.2005.04.028
  31. Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics. 14(9):817-818. https://doi.org/10.1093/bioinformatics/14.9.817
  32. Rodriguez-Lanetty M. 2003. Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol. 28:152-168. https://doi.org/10.1016/S1055-7903(03)00033-2
  33. Rodriguez-Lanetty M, Cha HR, Song JI. 2000. Genetic diversity of symbiotic dinoflagellates associated to anthozoans from Korean waters. Proc 9th Coral Reef Symp. 1:163-166.
  34. Rodriguez-Lanetty M, Chang SJ, Song JI. 2003. Specificity of two temperate dinoflagellate-anthozoan associations from the northwestern Pacific Ocean. Mar Biol. 143: 1193-1199. https://doi.org/10.1007/s00227-003-1165-x
  35. Roopin M, Henry RP, Chadwick NE. 2008. Nutrient transfer in a marine mutualism: Patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol. 154:547-556. https://doi.org/10.1007/s00227-008-0948-5
  36. Rowan R. 1998. Diversity and ecology of zooxanthellae in coral reefs. J Phycol. 34:407-417. https://doi.org/10.1046/j.1529-8817.1998.340407.x
  37. Rowan R, Knowlton N. 1995. Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA. 92:1850-1853.
  38. Rowan R, Knowlton N, Baker A, Jara J. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature. 388(17):265-269. https://doi.org/10.1038/40843
  39. Rowan R, Powers DA. 1991a. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science. 251:1348-1351. https://doi.org/10.1126/science.251.4999.1348
  40. Rowan R, Powers DA. 1991b. Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser. 71:65-73. https://doi.org/10.3354/meps071065
  41. Sampayo EM, Dove S, LaJeunesse TC. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol. 18:500-519. https://doi.org/10.1111/j.1365-294X.2008.04037.x
  42. Santos SR, Taylor DJ, Coffroth MA. 2001. Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. J Phycol. 37:900-912. https://doi.org/10.1046/j.1529-8817.2001.00194.x
  43. Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA. 2002. Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol. 23(2):97-111. https://doi.org/10.1016/S1055-7903(02)00010-6
  44. Saunders BK, Muller-Parker G. 1996. The effects of temperature and light on algal populations in the temperature sea anemone Anthopleura elegantissima (Brandt, 1835). J Exp Mar Biol Ecol. 211:213-224.
  45. Schoenberg DA, Trench RK. 1980. Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc Lond B. 207:405-427. https://doi.org/10.1098/rspb.1980.0031
  46. Scott A, Harrison PL. 2007. Embryonic and larval development of the host sea anemones Entacmaea quadricolor and Heteractis crispa. Biol Bull. 213:110-121 https://doi.org/10.2307/25066627
  47. Song JI. 1991. A systematic study on the Korean Anthozoa 12. Order Scleractinia. Korean J Syst Zool. 7(1):127-150. pp.
  48. Sprung J, Delbeek JC. 1997. The reef aquarium Vol. 2. Coconut Grove, FL: Ricordea Publishing.
  49. Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA. 2008. Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs. 27:763-772. https://doi.org/10.1007/s00338-008-0412-5
  50. Steen RG, Muscatine L. 1987. Low temperature evokes rapid exocytosis of symbiotic algae by a sea anemone. Biol Bull. 172:246-263. https://doi.org/10.2307/1541797
  51. Swofford DL. 2002. PAUP* 4.0: phylogenetic analysis using parsimony (* and other methods). Sunderland: MA: Sinauer Associates.
  52. Taylor DL. 1974. Symbiotic marine algae: taxonomy and biological fitness. In: Vernberg WB, editor. Symbiosis in the sea. Columbia: SC: University of South Carolina Press. p. 245-262.
  53. Taylor DL. 1983. The coral-algal symbiosis. In: Goff LJ, editor. Algal symbiosis. Cambridgej: Cambridge University Press. p. 19-35.
  54. Thompson DJ, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876-4882.
  55. Thornhill D, LaJeunesse TC, Santos SR. 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol. 16: 5326-5340. https://doi.org/10.1111/j.1365-294X.2007.03576.x
  56. Toller WW, Rowan R, Knowlton N. 2001. Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull. 201:360-373. https://doi.org/10.2307/1543614
  57. Trench RK, Blank RJ. 1987. Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov. Gymnodinioid dinoflagellate symbionts of marine invertebrates. J Phycol. 23:469-481. https://doi.org/10.1111/j.1529-8817.1987.tb02534.x
  58. van Oppen MJH, Palstra EP, Piquet AMT, Miller D. 2001. Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond B. 268:1767-1779.
  59. Veron JEN. 1992. Conservation of biodiversity: A critical time for hermatypic corals of Japan. Coral Reefs. 11: 13-21. https://doi.org/10.1007/BF00291930
  60. Wilcox TP. 1998. Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: Morphology does not recapitulate phylogeny. Mol Phylogenet Evol. 10:436-448. https://doi.org/10.1006/mpev.1998.0546
  61. Xu J, Su J. 1997. Hydrographic analysis on the intrusion of the Kuroshio into the South China Sea. 2. Trop Oceanol/ Redai Haiyang. 16:1-23.

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