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Morphological Characteristics and Molecular Phylogeny of Five Unarmored Dinoflagellates in Korean Coastal Waters

한국 연안에 출현하는 무각와편모조류 5종에 대한 형태 및 분자계통학적 특성

  • 조수연 (한양대학교 자연과학대학 생명과학과) ;
  • 기장서 (한양대학교 자연과학대학 생명과학과) ;
  • 한명수 (한양대학교 자연과학대학 생명과학과)
  • Published : 2008.03.01

Abstract

Many species in Gymnodiniales, which are unarmored dinoflagellates, are responsible for marine algal blooms and some of them have potent toxin in the cell. Their taxonomy has so far been well-defined, and several genera (e.g. Akashiwo, Gymnodinium, Karenia) have recently been re-described. In Korea, few works have been carried out on their taxonomical and molecular studies. This study focused on comparison of both morphological and molecular characteristics of five unarmored dinoflagellates on Korean coastal water: Akashiwo sanguinea, Cochlodinium polykrikoides, Gymnodinium catenatum, Gymnodinium impudicum and Karenia aureolum (=K. mikimotoi). Morphological characteristics observed here was in good accordance with the original descriptions of individual species. In addition, none of difference was found in morphological comparisons between the Korean and foreign strains. Furthermore, molecular analysis showed that the SSU rDNA sequences were generally identical according to each species. In some distinct features, A. sanguinea, which has generally the same morphological features, were divided into two groups: one was Korean isolates including European isolates, the other was American isolates. In the two groups, the nucleus was positioned differently: middle of the cells in the Korean isolates (GnSg02, GnSg03), near the epicone in American isolates (CCMP1593, CCMP1837). In addition, this was strongly supported by phylogenetic analysis, inferred from the SSU rDNA sequences. K. aureolum (GrAr01) was corresponded to European G. aureolum (=K. mikimotoi) in shape and position of nucleus, chloroplast, however, which is similar to K. digitata in view of having a finger-like sulcus. This was in good agreement with phylogenetic study of these species. G. catenatum have identical morphology except the ridge location, and their genotype of SSU rDNA was also identical to GenBank data of the same species. From this study, we found that the five Korean unarmored dinoflagellates are identical morphological characteristics and genotype to each species of foreign isolates.

Keywords

References

  1. 김창훈, 신재범. 1997. 한국 연안의 유해.유독 적조 조류의 발생과 독생산. Algae 12: 269-276
  2. 김학균. 2005. 해양적조. 다솜출판사. 467 pp.
  3. 김학균, 이삼근, 안경호. 1998. 한국연안의 적조-최근 적조의 발생 원인과 대책. 국립수산진흥원. 112 pp.
  4. 박종규, 박영식. 1999. Cochlodinium polykokoides와 Gyrodinium impudicum 형태특성과 24S rRNA 유전자 염기서열 비교. 한국해양학회지 바다, 4: 363-370
  5. 문성기, 이삼근, 홍채규. 1995. Prorocentrum 속에 관한 연구. 한국환경생물학회지 4: 105-116
  6. 유광일, 이준백. 1986. 마산만 일대 와편모조류의 분류학적 연구. I. Prorocentrum 속에 대하여. 한국해양학회지 21: 46-55
  7. 심재형, 신은영, 최중기. 1981. 여수 근해의 쌍편모조류에 관한 분류학적 연구. 한국해양학회지 16: 57-98
  8. 이삼근. 1991. 진해만에 출현하는 유독 와편모조류의 분류 및 분포에 관한 연구. 경상대학교 박사논문. 151 pp.
  9. 이삼근, 박주석, 김학균. 1993. 한국 남해 연안 해역에서 출현하는 유독 편모조류의 분류. 국립수산진흥원 연구보고 48: 1-24
  10. 이진환. 1999. 한국연안에 있어서 적조발생과 식물플랑크톤 독성에 관한 개관. 환경생물학회지 17: 217-266
  11. 한명수. 1990. 유독플랑크톤(와편모조류를 중심으로)에 관한 고찰. 한국수산학회지 23: 51-60
  12. 한명수, 유광일. 1983a. 진해만의 쌍편모조류에 관한 분류학적 연구. 제 I 보: 유각류와 무각류. 해양연구소보 5: 37-47
  13. 한명수, 유광일. 1983b. 진해만의 쌍편모조류에 관한 분류학적 연 구. 제 II 보: 페리디니움목. 해양연구소보 5: 49-67
  14. Adachi M. and Irie H. 1981. Red-tide manual: II. Dinoflagellate. Red Tide Research Group, Tokyo, 172 pp.
  15. Bergholtz T., Daugbjerg N., Moestrup O and Fernandez-Tejedor M. 2005. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J. Phycol. 42: 170-193 https://doi.org/10.1111/j.1529-8817.2006.00172.x
  16. Bolch C.J.S., Blackburn S.I., Hallegraeff G.M. and Vaillancourt R.E. 1999a. Genetic variation among strains of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). J. Phycol. 35: 356-367 https://doi.org/10.1046/j.1529-8817.1999.3520356.x
  17. Bolch C.J.S., Nergi A.P. and Hallegraeff G.M. 1999b. Gymnodinium microreticulatum sp. nov. (Dinophyceae): A naked, microreticulate cyst-producing dinoflagellate, distinct from Gymnodinium catenatum and Gymnodonium nolleri. Phycologia 38: 301-313 https://doi.org/10.2216/i0031-8884-38-4-301.1
  18. Botes L., Sym S.D. and Pitcher G.C. 2003. Karenia cristata sp. nov. and Karenia bicuneiformis sp. nov. (Gymnodiniales, Dinophyceae): two new Karenia species from the South African coast. Phycologia 42: 563-571 https://doi.org/10.2216/i0031-8884-42-6-563.1
  19. Chang F.H. and Ryan K.G. 2004. Karenia concordia sp. nov. (Gymnodiniales, Dinophyceae), a new nonthecate dinoflagellate isolated from the New Zealand northeast coast during the 2002 harmful algal bloom events. Phycologia 43: 552- 562 https://doi.org/10.2216/i0031-8884-43-5-552.1
  20. Cho E.S., Kim G.Y. and Cho Y.C. 2001. Molecular analysis of morphologically similar dinoflagellates Cochlodinium polykrikoides, Gyrodinium impudicum and Gymnodinium catenatum based on internal transcribed spacer and 5.8S rDNA region. Algae 16: 53-57
  21. Costas E., Zardoya R., Bautista J., Garrido A., Rojo C. and Lopez- Rodas V. 1995. Morphospecies vs. genospecies in toxic marine dinoflagellates: An analysis of Gymnokinium catenatum / Gyrodinium impudicum and Alexandrium minutum / A. lusitanicum using antibodies, lectins, and gene sequences. J. Phycol. 31: 801-807 https://doi.org/10.1111/j.0022-3646.1995.00801.x
  22. Daugbjerg N., Hansen G., Larsen J. and Moestrup O. 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 dinoflagelltes. Phycologia 39: 302-317 https://doi.org/10.2216/i0031-8884-39-4-302.1
  23. de Salas M.E., Bolch C.J.S. and Hallegraeff G.M. 2004a. Karenia umbella sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia 43: 166-175 https://doi.org/10.2216/i0031-8884-43-2-166.1
  24. de Salas M.E., Bolch C.J.S. and Hallegraeff G.M. 2004b. Karenia asterichroma sp. nov. (Gymnodiniales, Dinophyceae), a new dinoflagellate species associated with finfish aquaculture mortalities in Tasmania, Australia. Phycologia 43: 624-631 https://doi.org/10.2216/i0031-8884-43-5-624.1
  25. de Salas M.E., Bolch C.J.S., Botes L., Nash G., Wright W. and Hallegraeff G.M. 2003. Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J. Phycol. 39: 1233-1246 https://doi.org/10.1111/j.0022-3646.2003.03-019.x
  26. Dodge J.D. 1982. Marine Dinoflagellates of the British Isles. Her Majesty's Stationery Office, London, 303 pp.
  27. Ellegaard M., Christensen B.F. and Moestrup O. 1993. Temperature and salinity effects on growth of a non-chain-forming strain of Gymnodinium catenatum (Dinophyceae) established from a cyst from recent sediments in the sound (Oresund), Denmark. J. Phycol. 29: 418-426 https://doi.org/10.1111/j.1529-8817.1993.tb00142.x
  28. Ellegaard M. and Oshima Y. 1998. Gymnodinium nolleri Eliegaard et Moestrup sp. ined. (Dinophyceae) from Danish waters, a new species producing Gymnodinium caternatum-like cysts: molecular and toxicological comparisons with Australian and Spanish strains Gymnodinium catenatum. Phycologia 37: 369-378 https://doi.org/10.2216/i0031-8884-37-5-369.1
  29. Fraga S., Bravo I., Delgado M., Franco J.M. and Zapata M. 1995. Gyrodinium impudicum sp. nov. (Dinophyceae), a non toxic, chain-forming, red tide dinoflagellate. Phycologia 34: 514-521 https://doi.org/10.2216/i0031-8884-34-6-514.1
  30. Graham H.W. 1943. Gymnodinium catenatum, a new dinoflagellate from the Gulf of California. Trans. Amer. Microsc. Soc. 62: 259- 261 https://doi.org/10.2307/3223028
  31. Guillard R.R.L. and Ryther J.H. 1962. Studies on marine planktonic diatoms. 1. Cyclotella nana Hustedt and Detontula confervaceae Cleve. Can. J. Microbiol. 8: 229-239
  32. Hallegraeff G.M., Anderson D.M. and Cembella A.D. 1995. Manual on harmful marine microalgae. IOC manuals and Guides No. 33. UNESCO. pp. 283-317
  33. Han M.-S., Jeon J.K. and Kim Y.O. 1992. Occurrence of dinoflagellate Alexandrium tamarense, a causative organism of paralytic shellfish poisoning in Chinhae Bay, Korea. J. Plankton. Res. 14: 1581-1592 https://doi.org/10.1093/plankt/14.11.1581
  34. Hansen G. 2001. Ultrastructure of Gymnodinium aureolum (Dinophyceae): Toward a further redefinition of Gymnodinium sensu stricto. J. Phycol. 37: 612-623 https://doi.org/10.1046/j.1529-8817.2001.037004612.x
  35. Hansen G. and Daugbjerg N. 2004. Ultrastructure of Gyrodinium spirale, the type species of Gyrodinium (Dinophyceae), including a phylogeny of G. dominans, G. rubrum and G. spirale deduced from partial LSU rDNA sequences. Protist 155: 271- 294 https://doi.org/10.1078/1434461041844231
  36. Hansen G., Daugbjerg N. and Henriksen P. 2000a. Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. J. Phycol. 36: 394- 410 https://doi.org/10.1046/j.1529-8817.2000.99172.x
  37. Hansen G., Moestrup O. and Roberts K.R. 2000b. Light and electron microscopical observations on the type species of Gymnodinium, G. fuscum (Dinophyceae). Phycologia 39: 365-376 https://doi.org/10.2216/i0031-8884-39-5-365.1
  38. Hansen G. and Moestrup O. 2005. Flagellar apparatus and nuclear chambers of the green dinoflagellate Gymnodinium chlorophorum. Phycol. Res. 53: 169-181 https://doi.org/10.1111/j.1440-1835.2005.tb00368.x
  39. Hansen G., Daugbjerg N. and Henriksen P. 2007. Baldinia anauniensis gen. et sp. nov.: a 'new' dinoflagellate from Lake Tovel, N. Italy. Phycologia 46: 86-108 https://doi.org/10.2216/0031-8884(2007)46[86:BAGESN]2.0.CO;2
  40. Haywood A.J., Steidinger K.A., Truby E.W., Bergquist P.R., Bergquist P.L., Adamson J. and MacKenzie L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 40: 165-179 https://doi.org/10.1111/j.0022-3646.2004.02-149.x
  41. Hulburt E.M. 1957. The taxonomy of unarmored dinophyceae of shallow embayment on Cape Cod, Massachusetts. Biol. Bull. Mar. Lab. Woods Hole 112: 196-219 https://doi.org/10.2307/1539198
  42. Jung M.K. 2001. A taxonomical study on the free-living unarmored dinoflagellates in the South Sea of Korea. Master's thesis, Inje University, Korea, 71 pp. (in Korean)
  43. Ki J.-S. 2005. Development of single-cell PCR and low density microarray for the detection of harmful microalgae in aquatic ecosystem. Ph. D thesis, Hanyang University, Korea, 179 pp.
  44. Ki J.-S. and Han M.-S. 2005. Molecular analysis of complete SSU to LSU rDNA sequence in the harmful dinoflagellate Alexandrium tamarense (Korean isolate, HY970328M). Ocean Science Journal 40: 155-166 https://doi.org/10.1142/9789812701619_0024
  45. Ki J.-S., Jang K.-Y. and Han M.-S. 2004. Integrated method for single-cell DNA extraction, PCR amplification, and sequencing on ribosomal DNA from harmful dinoflagellates Cochlodinium polykrikoies and Alexandrium catenella. Mar. Biotechnol. 6: 587- 593 https://doi.org/10.1007/s10126-004-1700-x
  46. Kim G.Y., Ha M.G., Cho E.S., Lee T.H., Lee S.J. and Lee J.D. 1999. Molecular identification of Gyrodinium impudicum and Gymnodinium sanguineum by comparing the sequences of the internal transcribed spacers 1, 2 and 5.8S ribosomal DNA. J. Fish. Sci. Tech. 2: 66-77
  47. Kim K.Y. 2005. Phylogenetic relationships of dinoflagelltes in Korea based on nuclear ribosomal SSU and LUS region comparisons. Ph. D thesis, Pukyong National University, Korea, 123 pp.
  48. Kimball J.F. and Wood E.J.F. 1965. A dinoflagellate with characteristics of Gymnodinium and Gyrodinium. J. Protozool. 12: 577-580 https://doi.org/10.1111/j.1550-7408.1965.tb03257.x
  49. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120 https://doi.org/10.1007/BF01731581
  50. Kofoid C.A. and Swezy O. 1921. The free-living unarmored dinoflagellata. Mem Univ. Calif., 564 pp.
  51. Lebour M.V. 1925. The dinoflagellates of the Northern Sea. Marine Biological Association of the United Kingdom, Plymouth, UK, 250 pp.
  52. Margalef R. 1961. Hidrografía y fitoplancton de un area marina de la costa meridinal de Puerto Rico. Inv. Pesq. 18: 33-96
  53. Morey-Gaines G. 1982. Gymnodinium catenatum Graham (Dinophyceae): morphology and affinities with armoured forms. Phycologia 21: 154-163 https://doi.org/10.2216/i0031-8884-21-2-154.1
  54. Pfiester L.A. and Anderson D.M. 1987. Dinoflagellate reproduction. In: Taylor F.J.R. (ed.). The biologi of donoflagellates. Blackwell, Oxford. pp. 611-648
  55. Posada D. and Crandall K.A. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818 https://doi.org/10.1093/bioinformatics/14.9.817
  56. Richardson T.L. and Pinckney J.L. 2004. Monitoring of toxic dinoflagellate Karenia brevis using gyroxanthin-based detection methods. J. Appl. Phycol. 16: 315-328 https://doi.org/10.1023/B:JAPH.0000047788.31312.4f
  57. Schiller J. 1937. Dinoflagellatae(Peridiniae) in monographischer Behandlung. II. Teil, Lieferung 4. In: Rabenhorst L. (ed.), Kryptogamen-Flora von Deutschland, Osterreich and der Schweiz. Akademische Verlagsgesellschaft, Leipzig. Germany. 417 pp.
  58. Silva E.S. 1967. Cochlodinium heterolobatum sp. nov.: Structure and some cytophysiological aspects. J. Protozool. 14: 745-754 https://doi.org/10.1111/j.1550-7408.1967.tb02072.x
  59. Shao P., Chen Y.-Q., Zhou H., Yuan J., Qu L.-H., Zhao D. and Lin Y.-S. 2004. Genetic variability in Gymnodiniaceae ITS regions: implications for species identification and phylogenetic analysis. Mar. Biol. 144: 215-224 https://doi.org/10.1007/s00227-003-1157-x
  60. Shim J.H. 1994. Illustrated encyclopedia of fauna and flora of Korea, Vol. 34 Marine Phytoplankton. Ministry of Education, Korea, 487 pp. (in Korean)
  61. Shin E.Y. 1999. A taxonomical study on the thecate dinoflagellates of Korean coastal waters. Ph. D thesis, Seoul National University, Korea, 240 pp.
  62. Stæhr P.A. and Cullen J.J. 2003. Detection of Karenia mikimotoi by spectral absorption signatures. J. Plankton Res. 25: 1237-1249 https://doi.org/10.1093/plankt/fbg083
  63. Steidinger K.A. and Tangen K. 1997. Dinoflagellates. In: Tomas C.R. (ed.), Identifying marine and dinoflagellate. Academic Press, Inc., San Diago. pp. 387-588
  64. Swofford D.L. 2002. PAUP*:Phylogenetic analysis using parsimony (*and other methods). V. 4.0b10. Sinauer Associates, Sunderland, Massachusetts, USA, 133 pp.
  65. Takano Y. and Horiguchi T. 2004. Surface ultrastructure and molecular phylogenetics of four unarmored heterotrophic dinoflagellates, including the type species of the genus Gyrodinium (Dinophyceae). Phycol. Res. 52: 107-116 https://doi.org/10.1111/j.1440-1835.2004.tb00319.x
  66. Takayama H. 2000. Morphological taxonomy of unarmored dinoflagellates Gymnodinium and Gyrodinium. Bull. Plankton Soc. Japan 47: 44-46
  67. Takayama H. and Matsuoka K. 1991. A reassessment of the specific characters of Gymnodinium mikimotoi Miyake et Kominami ex Oda and Gymnodinium nagasakiense Takayama et Adachi. Bull. Plankton Soc. Japan 38: 53-68
  68. Takayama H., Matsuoka K. and Fukuyo Y. 1998. A taxonomic study on Gyrodinium aureolum Hulnurt (Dinophyceae) from the morphological viewpoint based on materials collected in Japanese coastal waters. Bull. Plankton Soc. Japan 45: 9-19
  69. Takishita K., Nakano K. and Uchida A. 2000. Preliminary phylogenetic analysis of plastid-encoded genes from an anomalously pigmented dinoflagellate Gymnodinium mikimotoi (Gymnodiniales, Dinophyta). Phycol. Res. 47: 257-262 https://doi.org/10.1111/j.1440-1835.1999.tb00306.x
  70. Takishita K. and Uchida A. 1999. Molecular cloning and nucleotide sequence analysis psbA from the dinoflagellate: Origin of the dinoflagellate plastid. Phycol. Res. 47: 207-216 https://doi.org/10.1111/j.1440-1835.1999.tb00300.x
  71. Tangen K. and Bjornland T. 1981. Observations on pigments and morphology of Gyrodinium aureolum Hulburt, a marine dinoflagellate containing 19'-hexanoyloxyfucoxanthin as the main carotenoid. J. Plankton Res. 3: 389-401 https://doi.org/10.1093/plankt/3.3.389
  72. Thompson J.D., Higgins D.G., and Gibson T.J.1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680 https://doi.org/10.1093/nar/22.22.4673
  73. Von Drebes G. 1974. Marine phytoplankton. Georg Thieme Verlag, Stuttgart, 117 pp.
  74. Yang Z.B., Hodgkiss I.J. and Hansen G. 2001. Karenia longicanalis sp. nov. (Dinophyceae): a new bloom-forming species isolated from Hong Kong, May 1998. Bot. Mar. 44: 67-74 https://doi.org/10.1515/BOT.2001.009
  75. Yang Z.B., Takayama H. Matsuoka K. and Hodgkiss I.J. 2000. Karenia digitata sp. nov. (Gymnodiniales, Dinophyceae), a new harmful algal bloom species from the coastal waters of West Japan and Hong Kong. Phycologia 39: 463-470 https://doi.org/10.2216/i0031-8884-39-6-463.1
  76. Yuki K. and Yoshimatsu S. 1987. Morphology of the athecate dinoflagellate Gymnodinium catenatum in culture. Bull. Plankton Soc. Japan 4: 109-117
  77. Zhang H., Bhattacharya D. and Lin S. 2005. Phylogeny of Dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J. Phycol. 41: 411-420 https://doi.org/10.1111/j.1529-8817.2005.04168.x

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