Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (dinophyceae) as the Sole representative of Symbiodinium clade e

Journal of Eukaryotic Microbiology

Volumn 61, Issue 1, 2014, Pages 75-94

  Jeong, Hae Jin ^a   Lee, Sung Yeon ^a   Kang, Nam Seon ^a   Yoo, Yeong Du ^a   Lim, An Suk ^a   Lee, Moo Joon ^a   Kim, Hyung Seop ^b   Yih, Wonho ^b   Yamashita, Hiroshi ^c   Lajeunesse, Todd C ^d  

^a Seoul National University   (South Korea)

^b Kunsan National University   (South Korea)

^c FISHERIES RESEARCH AGENCY   (Japan)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

phylogeny; plastid genes; species; systematics; taxonomy

Indexed keywords

CHLOROPLAST; CYTOCHROME; DINOFLAGELLATE; DNA; GENETIC ANALYSIS; MORPHOLOGY; PHYLOGENY; PLANKTON; PLASTID; SYMBIOSIS; TAXONOMY; TRANSMISSION ELECTRON MICROSCOPY;

CALIFORNIA; MEDITERRANEAN SEA; PACIFIC OCEAN; SPAIN; UNITED STATES;

BACTERIA (MICROORGANISMS); CNIDARIA; COCCOIDEA; DINOPHYCEAE; EUKARYOTA; MASTIGOPHORA (FLAGELLATES); SYMBIODINIUM; SYMBIODINIUM SP.;

CYTOCHROME B; PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOME DNA; RNA 23S; SEA WATER;

ALVEOLATA; ANIMAL; ARTICLE; CELL ORGANELLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; CYTOLOGY; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MEDITERRANEAN SEA; MICROSCOPY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PACIFIC OCEAN; PARASITOLOGY; PHYLOGENY; PLASTID GENES; RNA GENE; SPAIN; SPECIES; TAXONOMY; ULTRASTRUCTURE; UNITED STATES;

PHYLOGENY; PLASTID GENES; SPECIES; SYSTEMATICS; TAXONOMY;

ALVEOLATA; ANIMALS; CALIFORNIA; CLUSTER ANALYSIS; CYTOCHROMES B; DNA, PROTOZOAN; DNA, RIBOSOMAL; GENES, RRNA; MEDITERRANEAN SEA; MICROSCOPY; MOLECULAR SEQUENCE DATA; ORGANELLES; PACIFIC OCEAN; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL, 23S; SEAWATER; SEQUENCE ANALYSIS, DNA; SPAIN;

EID: 84893676690     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/jeu.12088     Document Type: Article

References (95)

1. Abramoff, M. D., Magalhaes, P. J., &, Ram, S. J., 2004. Image processing with image. J. Biophotonics Int., 11: 36-42.
2. Banaszak, A. T., Iglesias-Prieto, R., &, Trench, R. K., 1993. Scrippsiella velellae sp. nov. (Peridiniales) and Gloeodinium viscum sp. nov. (Phytodiniales), dinoflagellate symbionts of two hydrozoans (Cnidarians). J. Phycol., 29: 517-528.
3. Banaszak, A. T., &, Trench, R. K., 1995. Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. I. Response of the algal symbionts in culture and in hospite. J. Exp. Mar. Biol. Ecol., 194: 233-250.
4. Bayer, T., Aranda, M., Sunagawa, S., Yum, L. K., DeSalvo, M. K., Lundquist, E., Coffroth, M. A., Voolstra, C. R., &, Medina, M., 2012. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE, 7: e35269.
5. Blank, R. J., &, Huss, V. A. R., 1989. DNA divergency and speciation in Symbiodinium (Dinophyceae). Plant Syst. Evol., 163: 213-232.
6. Blank, R. J., &, Trench, R. K., 1985. Speciation in symbiotic dinoflagellates. Science, 229: 656-658.
7. Chang, F. H., 1983. Winter phytoplankton and microzooplankton populations off the coast of Westland, New Zealand, 1979. N. Z. J. Mar. Freshw. Res., 17: 279-304.
8. Chen, C. A., Yang, Y. W., Wei, N. V., Tsai, W. S., &, Fang, L. S., 2005. Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs, 24: 11-22.
9. Clode, P. L., Saunders, M., Maker, G., Ludwig, M., &, Atkins, C., 2009. Uric acid deposits in symbiotic marine algae. Plant Cell Environ., 32: 170-177.
10. Fan, L., Sui, Z., Mao, Y., &, Guo, H., 2007. Preliminary identification of three new isolates in the genus Alexandrium (Dinophyceae) from the China Sea area. J. Ocean Univ. China, 6: 33-39.
11. Finney, J. C., Pettay, T., Sampayo, E. M., Warner, M. E., Oxenford, H., &, LaJeunesse, T. C., 2010. The relative significance of host-habitat, depth, and geography on the ecology, endemism and speciation of coral endosymbionts. Microb. Ecol., 60: 250-263.
12. Fitt, W. K., &, 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.
13. Fitt, W. K., Chang, S. S., &, Trench, R. K., 1981. Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum (Freudenthal) in culture. Bull. Mar. Sci., 31: 436-443.
14. Freudenthal, H. D., 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool., 9: 45-52.
15. Gou, W. L., Sun, J., Li, X. Q., Zhen, Y., Xin, Z., Yu, Z. G., &, Li, R. X., 2003. Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P.R. China. J. Exp. Mar. Biol. Ecol., 296: 135-144.
16. Hansen, G., &, Daugbjerg, N., 2009. Symbiodinium natans sp. nov.: a free-living dinoflagellate from Tenerife (northeast-Atlantic Ocean). J. Phycol., 45: 251-263.
17. Haywood, A. J., Steidinger, K. A., Truby, E. W., Bergquist, P. R., Bergquist, P. L., Adamson, J., &, MacKenzie, L., 2004. Coparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol., 40: 165-179.
18. Hill, M., Allenby, A., Ramsby, B., Schonberg, C., &, Hill, A., 2011. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol. Phyl. Evol., 59: 81-88.
19. Hirose, M., Reimer, J. D., Hidaka, M., &, Suda, S., 2008. Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar. Biol., 155: 105-112.
20. Hollingsworth, L. L., Kinzie III, R. A., Lewis, T. D., Krupp, D. A., &, Leong, J. A., 2005. Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs, 24: 523.
21. Huelsenbeck, J. P., &, Ronquist, F., 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17: 754-755.
22. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S., &, Kim, T. H., 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J., 45: 65-91.
23. Jeong, H. J., Yoo, Y. D., Kang, N. S., Lim, A. S., Seong, K. A., Lee, S. Y., Lee, M. J., Lee, K. H., Kim, H. S., Shin, W. G., Nam, S. W., Yih, W. H., &, Lee, K., 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc. Natl Acad. Sci. USA, 109: 12604-12609.
24. Kang, N. S., Jeong, H. J., Moestrup, Ø., &, Park, T. G., 2011. Gyrodiniellum shiwhaense n. gen., n. sp., a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J. Eukaryot. Microbiol., 58: 284-309.
25. Kang, N. S., Jeong, H. J., Moestrup, Ø., Shin, W. G., Nam, S. W., Park, J. Y., de Salas, M. F., Kim, K. W., &, Noh, J. H., 2010. Description of a new planktonic mixotrophic dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from the coastal waters off western Korea: morphology, pigments, and ribosomal DNA gene sequence. J. Eukaryot. Microbiol., 57: 121-144.
26. Kevin, J. M., Hall, T. W., McLaughlin, J. J. A., &, Zahl, P. A., 1969. Symbiodinium microadriaticum Freudenthal, a revised taxonomic description, ultrastructure. J. Phycol., 5: 341-350.
27. Krueger, T., &, Gates, R. D., 2012. Cultivating endosymbionts-host environment mimics support the survival of Symbiodinium C15 ex hospite. J. Exp. Mar. Biol. Ecol., 413: 169-176.
28. 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 Evol. Biol., 12: 217.
29. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., &, Higgins, D. G., 2007. Clustal w and clustal x version 2.0. Bioinformatics, 23: 2947-2948.
30. LaJeunesse, T. C., 2001. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the internal transcribed spacer region: in search of a "species" level marker. J. Phycol., 37: 866-880.
31. LaJeunesse, T. C., 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol., 141: 387-400.
32. LaJeunesse, T. C., &, Thornhill, D. J., 2011. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS ONE, 6: e29013.
33. LaJeunesse, T. C., &, Trench, R. K., 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol. Bull., 199: 126-134.
34. LaJeunesse, T. C., Fitt, W. K., &, Schmidt, G. W., 2010a. The reticulated chloroplasts of zooxanthellae (Symbiodinium) and differences in chlorophyll localization among life cycle stages. Coral Reefs, 29: 627.
35. 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. J. Phycol., 48: 1380-1391.
36. LaJeunesse, T. C., Bhagooli, R., Hidaka, M., DeVantier, L., Done, T., Schmidt, G. W., Fitt, W. K., &, Hoegh-Guldberg, O., 2004a. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser., 284: 147-161.
37. LaJeunesse, T. C., Thornhill, D. J., Cox, E. F., Stanton, F. G., Fitt, W. K., &, Schmidt, G. W., 2004b. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs, 23: 596-603.
38. LaJeunesse, T. C., Pettay, D. T., Sampayo, E. M., Phongsuwan, N., Brown, B., Obura, D., Hoegh-Guldberg, O., &, Fitt, W. K., 2010b. 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.
39. Lien, Y. T., Fukami, H., &, Yamashita, Y., 2012. Symbiodinium Clade C dominates zooxanthellate corals (Scleractinia) in the temperate region of Japan. Zool. Sci., 29: 173-180.
40. Lilly, E. L., Halanych, K. M., &, Anderson, D. M., 2005. Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae, 4: 1004-1020.
41. Lin, S., Zhang, H., Hou, Y., Zhuang, Y., &, Miranda, L., 2009. High-level diversity of dinoflagellates in the natural environment, revealed by assessment of mitochondrial cox1 and cob genes for dinoflagellate DNA barcoding. Appl. Environ. Microbiol., 75: 1279-1290.
42. Litaker, R. W., Vandersea, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Steidinger, K. A., Millie, D. F., Bendis, B. J., Pigg, R. J., &, Tester, P. A., 2003. Identification of Pfiesteria piscicida (Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. J. Phycol., 39: 754-761.
43. Loeblich, A. R. III, &, Sherley, J. L., 1979. Observations on the theca of the mobile phase of free-living and symbiotic isolates of Zooxanthella microadriaticum (Freudenthal) comb.nov. J. Mar. Biol. Assoc. U.K., 59: 195-205.
44. McBride, B. B., Muller-Parker, G., &, Jakobsen, H. H., 2009. Low thermal limit of growth rate of Symbiodinium californium (Dinophyta) in culture may restrict the symbiont to southern populations of its host anemones (Anthopleura spp.; Anthozoa, Cnidaria). J. Phycol., 45: 855-863.
45. Medlin, L., Elwood, H. J., Stickel, S., &, Sogin, M. L., 1988. The characterization of enzymatically amplified eukaryokic 16S-like rRNAcoding regions. Gene, 71: 491-499.
46. Moestrup, Ø., &, Daugbjerg, N,. 2007. On dinoflagellate phylogeny and classification. In, Brodie, J., &, Lewis, J., (ed.), Unravelling the Algae: The Past, Present, and Future of Algae Systematics. Systematics Association Special Volumes. Vol. 75. CRC Press, Boca Raton, FL. p. 215-230.
47. Muller-Parker, G., Lee, K. W., &, Cook, C. B., 1996. Changes in the ultrastructure of symbiotic zooxanthellae (Symbiodinium sp., Dinophyceae) in fed and starved sea anemones maintained under high and low light. J. Phycol., 32: 987-994.
48. Muscatine, L., McCloskey, L. R., &, Marian, R. E., 1981. Estimating the daily contribution of carbon to coral animal respiration. Limnol. Oceanogr., 26: 601-611.
49. Park, T. G., Park, G. H., Park, Y. T., Kang, Y. S., Bae, H. M., Kim, C. H., Jeong, H. J., &, Lee, Y., 2009. Identification of the dinoflagellate community during Cochlodinium polykrikoides (Dinophyceae) blooms using amplified rDNA melting curve analysis and real-time PCR probes. Harmful Algae, 8: 430-440.
50. Polne-Fuller, M., 1991. A novel technique for preparation of axenic cultures of Symbiodinium (Pyrrophyta) through selective digestion by amoebae. J. Phycol., 27: 552-554.
51. Porter, K. G., &, Feig, Y. S., 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr., 25: 943-948.
52. Porto, I., Granados, C., Restrepo, J. C., &, Sanchez, J. A., 2008. Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE, 3: e2160.
53. 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.
54. Pochon, X., Montoya-Burgos, J. I., Stadelmann, B., &, Palowski, J., 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol. Phyl. Evol., 38: 20-30.
55. Pochon, X., Garcia-Cuestos, L., Baker, A. C., Castella, E., &, Pawlowski, J., 2007. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in sorited foraminifera. Coral Reefs, 26: 867-882.
56. Pochon, X., &, Gates, R. D., 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol. Phylogenet. Evol., 56: 492-497.
57. Rodriguez-Lanetty, M., Chang, S. J., &, Song, J. I., 2003. Specificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean. Mar. Biol., 143: 1193-1199.
58. Ronquist, F., &, Huelsenbeck, J. P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572-1574.
59. Rowan, R., &, Powers, D. A., 1991. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbiosis. Science, 251: 1348-1351.
60. Rowan, R., &, Powers, D. A., 1992. Ribosomal-RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc. Natl Acad. Sci. USA, 89: 3639-3643.
61. Sampayo, E., Dove, S., &, LaJeunesse, T. C., 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol. Ecol., 18: 500-519.
62. Sanders, J. G., &, Palumbi, S. R., 2011. Populations of Symbiodinium muscatinei show strong biogeographic structuring in the intertidal anemone Anthopleura elegantissima. Biol. Bull., 220: 199-208.
63. Santos, S. R., 2004. Comment: phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P.R. China. J. Phycol., 40: 395-397.
64. Santos, S. R., Gutierrez-Rodriguez, C., &, Coffroth, M. A., 2003. Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S) ribosomal DNA sequences. Mar. Biotech., 5: 130-140.
65. Santos, S. R., Taylor, D. J., Kinzie III, R. A., Hidaka, M., Sakai, K., &, Coffroth, M. A., 2002. Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S) rDNA sequences. Mol. Phylogenet. Evol., 23: 97-111.
66. Schoenberg, D. A., &, Trench, R. K., 1980a. 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 S. microadriaticum. Proc. R. Soc. Lond. B, 207: 405-427.
67. Schoenberg, D. A., &, Trench, R. K., 1980b. Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. II. Morphological variation in S. microadriaticum. Proc. R. Soc. Lond. B, 207: 429-444.
68. Schoenberg, D. A., &, Trench, R. K., 1980c. Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc. R. Soc. Lond. B, 207: 445-460.
69. Scholin, C. A., Herzog, M., Sogin, M., &, Anderson, D. M., 1994. Identification of group and strain-specific genetic makers for globally distributed Alexandrium (Dinophyceae) II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol., 30: 999-1011.
70. Shao, P., Chen, Y. Q., Zhou, H., Yuan, J., Qu, L. H., Zhao, D., &, Lin, Y. S., 2004. Genetic variability in the Gymnodiniaceae ITS regions: implications for species identification and phylogenetic analysis. Mar. Biol., 144: 215-224.
71. Siano, R., Montresor, M., Probert, I., Not, F., &, de Vargas, C., 2010. Pelagodinium gen. nov. and P. beii comb. nov. a dinoflagellate symbiont of planktonic foraminifera. Protist, 161: 385-399.
72. Silverstein, R. N., Correa, A. M. S., LaJeunesse, T. C., &, Baker, A. C., 2011. Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar. Ecol. Prog. Ser., 422: 63-75.
73. Spector, D. L., 1984. Dinoflagellate nuclei. In:, Spector, D. L., (ed.), Dinoflagellates. Academic Press Inc., Orlando, FL, USA.
74. Spurr, A. R., 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res., 26: 31-42.
75. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688-2690.
76. Stat, M., Pochon, X., Cowie, R. O. M., &, Gates, R. D., 2009. Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar. Ecol. Prog. Ser., 386: 83-96.
77. Stern, R. F., Horak, A., Andrew, R. L., Coffroth, M. A., Andersen, R. A., Kupper, F. C., Jameson, I., Hoppenrath, M., Veron, B., Kasai, F., Brand, J., James, E. R., &, Keeling, P. J., 2010. Environmental barcoding reveals massive dinoflagellate diversity in marine environments. PLoS ONE, 5: e13991.
78. Stern, R. F., Andersen, R. A., Jameson, I., Kupper, F. C., Coffroth, M.-A., Vaulot, D., LeGall, F., Veron, Benoit, Brand, J. J., Skelton, H., Kasai, F., Lilly, E. L., &, Keeling, P. J., 2012. Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS ONE, 7: e42780.
79. Stoecker, D. K., 1999. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol., 46: 397-401.
80. Swofford, D,. 2000. PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sinauer Associates, Sunderland, MA.
81. Tamura, K., Dudley, J., Nei, M., &, Kumar, S., 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software v. 4.0. Mol. Biol. Evol., 24: 1596-1599.
82. Tchernov, D., Gorbunov, M. Y., de Vargas, C., Yadav, S. N., Vardi, A., Häggblom, M., &, Falkowski, P., 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl Acad. Sci. USA, 101: 13531-13535.
83. Thornhill, D. J., LaJeunesse, T. C., &, Santos, S. R., 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol. Ecol., 16: 5326-5340.
84. Thornhill, D. J., Lewis, A., Wham, D. C., &, LaJeunesse, T. C,. 2013. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution. DOI: 10.1111/evo.12270 (in press)
85. Trench, R. K., 1993. Microalgal-invertebrate symbioses: a review. Endocyt. Cell Res., 9: 135-175.
86. Trench, R. K., &, Blank, R. J., 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.
87. Trench, R. K., &, Thinh, L. V., 1995. Gymnodinium linucheae sp. nov.: the dinoflagellate symbiont of the jellyfish Linuche unguiculata. Eur. J. Phycol., 30: 149-154.
88. Udy, J. W., Hinde, R., &, Vesk, M., 1993. Chromosomes and DNA in Symbiodinium from Australian hosts. J. Phycol., 29: 314-320.
89. Wang, L. H., Liu, Y. H., Ju, Y. M., Hsiao, Y. Y., Fang, L. S., &, Chen, C. S., 2008. Cell cycle propagation is driven by light-dark stimulation in a cultured symbiotic dinoflagellate isolated from corals. Coral Reefs, 27: 823-835.
90. Xiang, T., Hambleton, E. A., DeNofrio, J. C., Pringle, J. R., &, Grossman, A. R., 2013. Isolation of clonal, axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J. Phycol., 49: 447-458.
91. Yacobovitch, T., Benayahu, Y., &, Weis, V. M., 2004. Motility of zooxanthellae isolated from the Red Sea soft coral Hetroxenia fuscescens (Cnidaria). J. Exp. Mar. Biol. Ecol., 298: 35-48.
92. Yamashita, H., &, Koike, K,. 2013. The genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol. Res., 61: 68-80.
93. Yamashita, H., Kobiyama, A., &, Koike, K., 2009. Do uric acid deposits in zooxanthellae function as eye-spots? PLoS ONE, 4: e63003.
94. Zardoya, R., Costas, E., Lopez-Rodas, V., Garrido-Pertierra, A., &, Bautista, J. M., 1995. Revised dinoflagellate phylogeny inferred from molecular analysis of large subunit ribosomal RNA gene sequences. J. Mol. Evol., 41: 637-645.
95. Zhang, H., Bhattacharya, D., &, Lin, S., 2005. Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J. Phycol., 41: 411-420.