Phylogenetic Analysis of Harmful Algal Bloom (HAB)-Causing Dinoflagellates Along the Korean Coasts, Based on SSU rRNA Gene

  • Kim, Se-Hee (Microbiology Lab., Korea Ocean Research &Development Institute, Department of Biological Science and The Basic Science Research Institute, Sungkyunkwan University) ;
  • Kim, Keun-Yong (Department of Aquaculture, Pukyong National University) ;
  • Kim, Chang-Hoon (Department of Aquaculture, Pukyong National University) ;
  • Lee, Woo-Sung (Department of Biological Science and The Basic Science Research Institute, Sungkyunkwan University) ;
  • Chang, Man (Microbiology Lab., Korea Ocean Research &Development Institute) ;
  • Lee, Jung-Hyun (Microbiology Lab., Korea Ocean Research &Development Institute)
  • Published : 2004.10.01

Abstract

Twenty-three cultures of harmful algal bloom (HAB)-(causing dinoflagellates were isolated from the coastal waters of Korea. For each of the 14 morphospecies, the nuclearencoded small subunit (SSU) rDNA was analyzed to determine the phylogenetic relatedness of the species. Despite temporal and spatial isolation, 3-4 clonal cultures of Alexandrium catenella, Cochlodinium polykrikoides, and Gymnodinium catenatum had 100% identical SSU rDNA sequences. In contrast, heterogeneities in the SSU rDNA sequences were observed in Akashiwo sanguinea and Lingulodinium polyedrum strains. Extreme sequence polymorphism was shown within the SSU rRNA genes of an Al. tamarense clonal culture. A homology search in GenBank revealed that 11 dinoflagellate species were located in clusters corresponding to their morphological classification. The SSU rDNA sequences of C. polykrikoides, Gyrodinium instriatum, and Pheopolykrikos hartmannii, which were determined for the first time in this study, showed the following phylogenetic relationships: C. polykrikoides formed an independent branch separated from other dinoflagellates; Gyr. instriatum was placed in a monophyletic group with Gyr. dorsum and Gyr. uncatenum; and Ph. hartmanii, which forms a distinct two-celled pseudocolony, belonged to Gymnodinium sensu Hansen and Moestrup.

Keywords

References

  1. Adachi, M., Y. Sako, and Y. Ishida. 1996. Identification of the toxic dinoflagellates Alexandrium catenella and A. tamarense (Dinophyceae) using DNA probes and whole-cell hybridization. J. Phycol. 32: 1049- 1052.
  2. Adachi, M., Y. Sako, and Y. Ishida. 1997. Analysis of Gymnodinium catenatum Dinophyceae using sequences of the 5.8S rDNA-ITS regions and random amplified polymorphic DNA. Fish. Sci. 63: 701-707.
  3. Akiba, T. and Y. Hattori. 1949. Food poisoning caused by eating asari (Venerupis semidecussata) and oyster (Ostrea gigas) and studies on the toxic substance, venerupin. Jpn. J. Exp. Med. 20: 271- 284.
  4. Anderson, D. M. 1997. Turning back the harmful red tide. Nature 388: 513- 514. https://doi.org/10.1038/41415
  5. Baek, S.-H., X.-X. Sun, Y.-J. Lee, S.-Y. Wang, K.-N. Han, J.-K. Choi, J.-H. Noh, and E.-K. Kim. 2003. Mitigation of harmful algal blooms by sophorolipid. J. Microbiol. Biotechnol. 13: 651-659.
  6. Balech, E. 1995. The Genus Alexandrium (Dinojlagellata), pp. 151. Sherkin Island Marine Station, Co. Cork.
  7. Bowers, H. A., T. Tengs, H. B. Glasgow Jr., J. M. Burkholder, P. A. Rublee, and D. W. Oldach. 2000. Development of realtime PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl. Environ. Microbiol. 66: 4641-4648.
  8. Cavalier-Smith, T. 1993. Kingdom Protozoa and its 18 phyla. Microbiol. Rev. 57: 953- 994.
  9. Cho, C. H. 1978. On the Gonyaulax red tide in Jinhae Bay. Bull. Korean Fish. Soc. 11: 111- 114.
  10. Daugbjerg, N., G. Hansen, J. Larsen, and $\phi$. Moestrup. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmored dinoflagellates. Phycologia 39: 302- 3I7.
  11. Draisci, R., E. Ferretti, L. Palleschi, C. Marchiafava, R. Poletti, A. Milandri, A. Ceredi, and M. Pompei. 1999. High levels of yessotoxin in mussels and presence of yessotoxin and homoyessotoxin in dinoflagellates of the Adriatic Sea. Toxicon 37: 1187- 1193.
  12. Edgcomb, V. P., D. T. Kysela, A. Teske, A. de Vera Gomez, and M. L. Sogin. 2002. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. USA 99: 7658- 7662.
  13. Faust, M. A. and R. A. Gulledge. 2002. Identifying harmful marine dinoflagellates. Smithsonian Contributions From United States National Herbarium 42: 1- 144.
  14. Fukuyo, Y. and H. Inoue 1990. Alexandrium affine (Inoue et Fukuyo) Balech, pp. 84- 85. In Y. Fukuyo, H. Takano, M. Chihara, and K. Matsuoka (eds.), Red Tide Organisms in Japan: An Illustrated Guide. Uchida Rokakuho, Tokyo, Japan.
  15. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79- 99. https://doi.org/10.2216/i0031-8884-32-2-79.1
  16. Han, M. S., J. K. Jeon, and Y-H. Yoon. 1993. Distribution and toxin profiles of Alexandrium tamarense (Lebour) Balech (Dinoflagellata) in the southeastern coastal waters, Korea. Korean J. Phycol. 8: 7- 13.
  17. Han, M. S., J. K. Jeon, and YO. Kim. 1992. Occurrence of dinoflagellate Alexandrium tamarense, a causative organism of paralytic shellfish poisoning in Chinhae Bay. Korea J. Plankton Res. 14: 1581- 1592.
  18. Herzog, M. and L. Maroteaux. 1986. Dinoflagellate 17S rRNA sequence inferred from the gene sequence: Evolutionary implications. Proc. Natl. Acad. Sci. USA 83: 8644- 8648.
  19. Huelsenbeck, J. P. and F. Ronquist. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754- 755.
  20. Huelsenbeck, J. P., F. Ronguist, R. Nielsen, and J. P. Bollback. 2001. Evolution-Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 23I0- 2314.
  21. Iwasaki, H. 1961. The life cycle of Porphyra tenera in vitro. BioI. Bull. 121: 173- 187.
  22. Jin E, J. E. W. Polle, H. K. Lee, S. M. Hyun, and M. Chang. 2003. Xanthophylls in microalgae: From biosynthesis to biotechnological mass production and application. J. Microbiol. Biotechnol. 13: 165- 174.
  23. Kim, C. H. and J. B. Shin. 1997. Harmful and toxic red tide algal development and toxins production in Korean coastal waters. Algae 12: 269- 276.
  24. Kim, H. G. 1997. Recent harmful algal blooms and mitigation strategies in Korea. Ocean Res. 19: 185- 192.
  25. Kim, H. G., K. Matsuoka, S. G. Lee, and K. H. An. 1996. The occurrence of a dinoflagellate Gymnodinium catenatum from Chinhae Bay, Korea. J. Korean Fish. Soc. 29: 837842.
  26. Kim, H. G., S. G. Lee, K. H. An, S. H. Youn, P. Y Lee, C. K. Lee, E. S. Cho, J. B. Kim, H. G. Choi, and P. J. Kim. 1997. Recent Red Tides in Korean Coastal Waters, pp. 280. National Fisheries Research and Development Institute, Busan, Korea.
  27. Kim, K. Y, M. Yoshida, Y Fukuyo, and C. H. Kim. 2002. Morphological observation of Alexandrium tamarense (Lebour) Balech, A. catenella (Whedon et Kofoid) Balech and one related mcrphotype (Dinophyceae) in Korea. Algae 17: 11- 19.
  28. Kofoid, C. A and O. Swezy. 1921. The free-living unarmored dinoflagellates. Mem. Univ. Calif. 5: 1- 562.
  29. Lee, S. G., J. S. Park, and H. G. Kim. 1993. Taxonomy of marine toxic flagellates occurring in the southern coastal waters of Korea. Bull. Natl. Fish. Res. Dev. Agen. 48: 1- 23.
  30. Matsuoka, K. and Y. Fukuyo. 1986. Cyst and motile morphology of a colonial dinoflagellate Pheopolykrikos hartmannii (Zimmermann) comb. nov. J. Plankton Res. 8: 811- 818.
  31. Montresor, M., A Zingone, and D. Marino. 1993. The calcareous resting cyst of Pentapharsodinium tyrrhenicum com. nov. (Dinophyceae). J. Phycol. 29: 223- 230.
  32. Moon-van der Staay, S. Y, R. De Wachter, and D. Vaulot. 2001. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607- 610.
  33. Oldach, D. W., C. F. Delwiche, K. S. Jakobsen, T Tengs, E. G. Brown, J. W. Kempton, E. E Schaefer, H. A Bowers, H. B. Glasgow Jr., J. M. Burkholder, K. A. Steidinger, and P. A Rublee. 2000. Heteroduplex mobility assay-guided sequence discovery: Elucidation of the small subunit (18S) rDNA sequences of Pfiesteria pisciclda and related dinoflagellates from complex alga: culture and environmental sample DNA pools. Proc. Natl. Acad. Sci. USA 97: 4303- 4308.
  34. Reinecke,P. 1967.Gonyaulax grindleyisp. nov.:A dinoflagellate causing a red tide at Elands Bay, Cape Province, in December 1966. J. South Afr. Bot. 33: 157- 160.
  35. Saldarriaga, J. E, E J. R. Taylor, P. J. Keeling, and T Cavalier-Smith. 2001. Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J. Mol. Evol. 53: 204- 213.
  36. Satake, M., T Ichirnura, K. Sekiguchi, S. Yoshirnatsu, and Y Oshima. 1999. Confirmation of yessotoxin and 45,46,47trinoryessotoxin productions by Protoceratium reticulatum collected in Japan. Nat. Toxins 7: 147- 150.
  37. Saunders, G. W., D. R. A Hill, J. P. Sexton, and R. A Andersen. 1997. Small-subunit ribosomal RNA sequences from selected dinoflagellates: Testing classical evolutionary hypothesis with molecular systematic methods, pp. 237-259. In D. Bhattacharya (ed.), Origins of Algae and their Plastids. Springer, New York, U.S.A
  38. Schnepf, E. and M. Elbrachter, 1999. Dinophyta plastids and phylogeny: A review. Grana 38: 81- 97.
  39. Scholin, C. A, D. M. Anderson, and M. Sogin. 1993. Two distinct small-subur.it ribosomal RNA genes North American toxic dinoflagellate Alexandrium fundyense (Dinophyceae). J. Phycol. 29: 209- 216.
  40. Scholin, C. A, M. Herzog, M. Sogin, and D. M. Anderson. 1994. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30: 999- 1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  41. Soltis, D. E. and P. S. Soltis. 1998. Choosing an approach and an appropriate gene for phylogenetic analysis, pp. 1- 42. In D. E. Soltis, P. S. Soltis, and J. J. Doyle (eds.), Molecular Systematics of Plants II. DNA Sequencing. Kluwer Academic Publishers, Boston, U.S.A
  42. Steidinger, K. A. and K. Tangen. 1996. Dinoflagellates, pp. 387- 598. In C. R. Tomas (ed.), Identifying Marine Phytoplankton. Academic Press, San Diego.
  43. Swofford, D. L. 1998. $PAUP^*$. Phylogenetic Analysis Using Parsimony ($^*$ and many other methods). Version 4.0b8. Sinauer, Sunderland, MA, U.S.A
  44. Taylor, E J. R. and Y Fukuyo. 1998. The neurotoxigenic dinoflagellate genus Alexandrium Halim: General introduction, pp. 3 11. In D. M. Anderson, A D. Cembella, and G. M. Hallegraeff, (eds.), Physiological Ecology of Harmful Algal Blooms. NATO ASI Series, Vol. 41, Springer-Verlag, Berlin.
  45. Tengs, T, H. A. Bowers, A. P.Ziman, D. K. Stoecker, and D. W. Oldach. 2001. Genetic polymorphism in Gymnodinium galatheanum chloroplast DNA sequences and development of a molecular detection assay. Mol. Ecol. 10: 515- 523.
  46. Thompson, J. D., D. G. Higgins, and T J. Gibson. 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.
  47. Toriumi, S. 1990. Gyrodinium instriatum Freudenthal et Lee, pp. 62- 63. In Y. Fukuyo, H. Takano, M. Chihara, and K. Matsuoka (eds.), Red Tide Organisms in Japan: An Illustrated Guide. Uchida Rokakuho, Tokyo, Japan.
  48. Turabo, A, L. Sidari, R. D. Loggia, and T Yasumoto. 1998. Occurrence of yessotoxin-like toxins in phytoplankton and mussels from northern Adriatic Sea, pp. 470- 472. In B. Reguera, J. Blanco, M. L. Fernandez, and T Wyatt, (eds.), Harmful Algae. Xunta de Galicia and Intergovernmental Commission of UNESCO.
  49. Whyte,J. N. C., N. Haigh, N. G. Ginther,and L. J. Keddy. 2001. First record of blooms of Cochlodinium sp. (Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycologia 40: 298- 304.
  50. Wuyts, J., Y. Van de Peer, T. Winkelmans, and R. De Wachter. 2002. The European small subunit ribosomal RNA database. Nucleic Acids Res. 30: 183-185.
  51. Yoo,l S.,Y. Fukuyo, B. Cheun, S. G. Lee, and H. G. Kim. 2000. Toxic algal bloom caused by dinoflagellate Alexandrium tamarense. J. Fish. Sci. Tech. 3: 26- 32.
  52. Yuki, K. and S. Yoshimatsu. 1989. Two fish-killing species of Cochlodinium from Harima-Nada, Seto Inland Sea, Japan, pp. 451- 454. In T Okaichi, D. M. Anderson, and T Nemoto (eds.), Red Tides: Biology, Environmental Science, and Toxicology. Elsevier, New York, U.S.A.
  53. Zhang, H. and S. Lin. 2002. Detection and quantification of Pfiesteria piscicida by using the mitochondrial cytochrome b gene. Appl. Environ. Microbiol. 68: 989- 994.