Skip to main content
SpringerLink
Log in

DNA synthesis and the cell cycle in the noxious red-tide dinoflagellate Gymnodinium nagasakiense

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Gymnodinium nagasakiense is a noxious red tide dinoflagellate often associated with damage to fisheries in Japan. DNA synthesis and the cell cycle in this organism were investigated from 1989 to 1990 by determining relative DNA contents of individual cells using an epifluorescence microscopy-based microfluorometry system. The nuclei were stained with the DNA-specific fluorochrome 4′-6-diamidino-2-phenylindole (DAPI). Because photosynthetic pigment interferes with the fluorescence from the DAPI-DNA complex, the pigment was eliminated by methanol treatment as a first step in quantitative microfluorometry. Nuclear DNA contents, cell size distribution, cell density, and frequency of paired cells were determined every 2h for 24h using cells grown on a 12h light:dark cycle. DNA synthesis and cell division were tightly phased to a particular period of the light:dark cycle. DNA synthesis (S phase) occurred from 10:00 to 22:00 hrs and was followed by cytokinesis. The presence of such a distinct S phase strongly suggests that G. nagasakiense has a typical eukaryotic cell cycle. This type of cell cycle makes it possible to estimate speciesspecific in situ growth rate based on the diel pattern of DNA synthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abe, T., Hirayama, K. (1979). Lethal effect of Gymnodinium sp. on the rotifer, Brachionus plicatilis. Bull. Fac. Fish. Nagasaki Univ. 46: 1–6 (in Japanese with English summary)

    Google Scholar 

  • Bhaud, Y., Soyer-Gobillard, M. O. (1986). DNA synthesis and cell cycle of a primitive dinoflagellate, Prorocentrum micans Ehr. Protistologica 22: 23–30

    Google Scholar 

  • Carpenter, E. J., Chang, J. (1988). Species-specific phytoplankton growth rates via diel DNA synthesis cycles. I. Concept of the method. Mar. Ecol. Prog. Ser 43: 105–111

    Article  Google Scholar 

  • Cetta, C. M., Anderson, D. M. (1990). Cell cycle studies of the dinoflagellates Gonyaulax polyedra Stein and Gyrodinium uncatenum Hulburt during asexual and sexual reproduction. J. exp. mar. Biol. Ecol. 135: 69–84

    Article  Google Scholar 

  • Chang, J., Carpenter, E. J. (1985). Blooms of the dinoflagellate Gyrodinium aureolum in a Long Island estuary: box model analysis of bloom maintenance. Mar. Biol. 89: 83–93

    Article  Google Scholar 

  • Chang, J., Carpenter, E. J. (1988). Species-specific phytoplankton growth rates via diel DNA synthesis cycles. II. DNA quantification and model verification in the dinoflagellate Heterocapsa triquetra. Mar. Ecol. Prog. Ser. 44: 287–296

    Article  CAS  Google Scholar 

  • Chen, L. C. M., Edelstein, M., McLachlan, J. (1969). Bonnemaisonia hamifera Hariot in nature and in culture. J. Phycol. 5: 211–220

    Article  CAS  PubMed  Google Scholar 

  • Cho, C. H. (1981). On the Gymnodinium red tide in Jinhae Bay. Bull. Korean Fish. Soc. 14: 227–232

    Google Scholar 

  • Coleman, A. W., Maguire, M. J., Coleman, J. R. (1981). Mithramycin- and 4′-6-diamidino-2-phenylindole (DAPI)-DNA staining for fluorescence microspectrophotometric measurement of DNA in nuclei, plastids, and virus particles. J. Histochem. Cytochem. 29: 959–968

    Article  CAS  PubMed  Google Scholar 

  • Dodge, J. D. (1965). Chromosome structure in the dinoflagellates and the problem of the mesocaryotic cell. Excerpta Med. Int. Congr. Ser. 91: 264–265

    Google Scholar 

  • Filfilan, S. A., Sigee, D. C. (1977). Continuous DNA replication in the nucleus of the dinoflagellate Prorocentrum micans (Ehrenberg). J. Cell Sci. 27: 81–90

    Article  CAS  PubMed  Google Scholar 

  • Franker, C. K., Sakhrani, L. M., Prichard, C. D., Lamden, C. A. (1974). DNA synthesis in Cryptothecodinium cohnii. J. Phycol. 10: 91–94

    CAS  Google Scholar 

  • Calleron, C., Durrand, A. M. (1979). Cell cycle and DNA synthesis in a marine dinoflagellate Amphidinium carterae. Protoplasma 100: 155–165

    Article  Google Scholar 

  • Hamada, S., Fujita, S. (1983). DAPI staining improved for quantitative cytofluorometry. Histochemistry 79: 219–226

    Article  CAS  PubMed  Google Scholar 

  • Hamkalo, B. A., Rattner, J. B. (1977). The structure of a mesokaryotie chromosome. Chromosoma 60: 39–47

    Article  CAS  PubMed  Google Scholar 

  • Heller, M. D. (1977). The phased division of the freshwater dino-flagellate Ceratium hirundinella and its use as a method of assessing growth in natural populations. Freshwat. Biol. 7: 527–533

    Article  Google Scholar 

  • Hirayama, K., Numaguchi, K. (1972). Growth of Gymnodinium Type-'65, causative organism of red tide in Omura Bay, in medium supplied with bottom mud extract. Bull. Plankton Soc. Japan 19: 13–21

    Google Scholar 

  • Holt, J. R., Pfiester, L. A. (1982). A technique for counting chromosomes of armored dinoflagellates, and chromosome numbers of six freshwater dinoflagellate species. Am. J. Bot. 69: 1165–1168

    Article  Google Scholar 

  • Honjo, T., Yamamoto, S., Nakamura, O., Yamaguchi, M. (1990). Annual cycle of motile cells of Gymnodinium nagasakiense and ecological features during the period of red tide development. In: Granéli, E., Sundström, B., Edler, L., Anderson, D. M. (eds.) Toxic marine phytoplankton. Elsevier, New York, p. 165–170

    Google Scholar 

  • Hull, H. M., Hoshaw, R. W., Wang, J.-C. (1982). Cytofluorometric determination of nuclear DNA in living and preserved algae. Stain Technol. 57: 273–282

    Article  CAS  PubMed  Google Scholar 

  • Iizuka, S., Irie, H. (1966). The hydrographic conditions and the fisheries damages by the red water occurred in Omura Bay in summer 1965-II. The biological aspects of a dominant species in the red water. Bull. Fac. Fish. Nagasaki Univ. 21: 67–101 (in Japanese with English summary)

    Google Scholar 

  • Iizuka, S., Nakashima, T. (1975). Response of red tide organisms to sulphide. Bull. Plankton Soc. Japan 22: 27–32 (in Japanese with English summary)

    Google Scholar 

  • Ishimaru, T., Takeuchi, T., Fukuyo, Y., Kodama, M. (1989). The selenium requirement of Gymnodinium nagasokiense. In: Okaichi, T., Anderson, D. M., Nemoto, T. (eds.) Red tides. Biology, environmental science, and toxicology. Elsevier, New York, p. 357–360

    Google Scholar 

  • Itakura, S., Imai, I., Itoh, K. (1990). Seasonal occurrence of the noxious red tide dinoflagellate Gymnodinium nagasakiense in Hiroshima Bay, Seto Inland Sea. Bull. Nansei natn. Fish. Res. Inst. 23: 27–33 (in Japanese with English summary)

    Google Scholar 

  • Itoh, K., Imai, I. (1987). Rafido so (Raphidophyceae). In: Japan Fisheries Resource Conservation Association (ed.) A guide for studies of red tide organisms. Shuwa, Tokyo, p. 122–130 (in Japanese)

    Google Scholar 

  • Iwasaki H. (1967). The isolation and culture of unicellular algae. Japan Fisheries Resource Conservation Association, Tokyo, p. 1–55 (in Japanese)

    Google Scholar 

  • Iwasaki, H., Kim, C.-H., Tsuchiya, M. (1990). Growth characteristics of a dinoflagellate Gymnodinium nagasakiense Takayama et Adachi. Japan. J. Phycol. 38: 155–161

    Google Scholar 

  • Karentz, D. (1983). Patterns of DNA synthesis and cell division in marine dinoflagellates. J. Protozool. 30: 581–588

    Article  CAS  Google Scholar 

  • Kasten, F. H. (1989). The origins of modern fluorescence microscopy and fluorescent probes. In: Kohen, E., Hirschberg, J. G. (eds.) Cell structure and function by microspectrofluorometry. Academic Press, San Diego, p. 3–50

    Chapter  Google Scholar 

  • Loeblich, A. R. III. (1976). Dinoflagellate evolution: speculation and evidence. J. Protozool. 23: 13–28

    Article  PubMed  Google Scholar 

  • Loeblich, A. R. III. (1977). Studies on synchronously dividing populations of Cachonina niei, a marine dinoflagellate. Bull. Jap. Soc. Phycol. 25 (Suppl.): 119–128

    Google Scholar 

  • Loper, C. L., Steidinger, K. A., Walker, L. M. (1980). A simple chromosome spread technique for unarmored dinoflagellates and implications of polyploidy in algal cultures. Trans. Am. microsc. Soc. 99: 343–346

    Article  Google Scholar 

  • Matsuoka, K., Iizuka, S., Takayama, H., Honjo, T., Fukuyo, Y., Ishimaru, T. (1989). Geographic distribution of Gymnodinium nagasakiense Takayama et Adachi around west Japan. In: Okaichi, T., Anderson, D. M., Nemoto, T. (eds.) Red tides. Biology, environmental science, and toxicology. Elsevier, New York, p. 101–104

    Google Scholar 

  • McDuff, R. E., Chisholm, S. W. (1982). The calculation of in situ growth rates of phytoplankton populations from fractions of cells undergoing mitosis: a clarification. Limnol. Oceanogr 27: 783–788

    Article  Google Scholar 

  • Nagasaki, K., Uchida, A., Ishida, Y. (1991). A monoclonal antibody which recognizes the cell surface of red tide alga Gymnodinium nagasakiense. Nippon SuiSan Gakk. 57: 1211–1214

    Article  CAS  Google Scholar 

  • Nakata, K., Iizuka, S. (1987). A note on overwintering of a red tide dinoflagellate Gymnodinium nagasakiense (Dinophyceae) in Omura Bay, Kyushu. Bull. Plankton Soc. Japan 34: 199–201 (in Japanese with English summary)

    Google Scholar 

  • Nishimura, A. (1982). Effects of organic matters produced in fish farms on the growth of red tide algae Gymnodinium type-'65 and Chattonella antiqua. Bull. Plankton Soc. Japan 29: 1–7 (in Japanese with English summary)

    Google Scholar 

  • Numaguchi, K., Hirayama, K. (1972). On the suitable pH and chlorinity to the growth of Gymnodinium type-'65, causative organism of the red tide in Omura Bay. Bull. Fac. Fish. Nagasaki Univ. 33: 7–10 (in Japanese with English summary)

    Google Scholar 

  • Olson, R. J., Chisholm, S. W. (1986). Effects of light and nitrogen limitation on the cell cycle of the dinoflagellate Amphidinium carteri. J. Plankton Res. 8: 785–793

    Article  Google Scholar 

  • Olson, R. J., Frankel, S. L., Chisholm, S. W., Shapiro, H. M. (1983). An inexpensive flow cytometer for the analysis of fluorescence signals in phytoplankton: chlorophyll and DNA distributions. J. exp. mar. Biol. Ecol. 68: 129–144

    Article  CAS  Google Scholar 

  • Olson, R. J., Vaulot, D., Chisholm, S. W. (1986). Effects of environmental stresses on the cell cycle of two marine phytoplankton species. Pl. Physiol., Lancaster 80: 918–925

    Article  CAS  Google Scholar 

  • Rizzo, P. J. (1987). Biochemistry of the dinoflagellate nucleus. In: Taylor, F. J. R. (ed.) The biology of dinoflagellates. Blackwell Scientific Publications, Oxford, p. 143–173

    Google Scholar 

  • Sako, Y., Uchida, A., Ishida, Y. (1989). Electrophoretic analysis of isozymes in red tide dinoflagellates (Gymnodinium nagasakiense, Protogonyaulax catenella, & Peridinium bipes). In: Okaichi, T., Anderson, D. M., Nemoto, T. (eds.) Red tides. Biology, environmental science, and toxicology. Elsevier, New York, p. 325–328

    Google Scholar 

  • Spector, D. L., Vasconcelos, A. C., Triemer, R. E. (1981). DNA duplication and chromosome structure in the dinoflagellates. Protoplasma 105: 185–194

    Article  CAS  PubMed  Google Scholar 

  • Takayama, H., Adachi, R. (1984). Gymnodinium nagasakiense sp. nov., a red-tide forming dinophyte in the adjacent waters of Japan. Bull. Plankton Soc. Japan 31: 7–14

    Google Scholar 

  • Terada, K., Ikeuchi, H., Takayama, H. (1987). Winter distribution of Gymnodinium nagasakiense (Dinophyceae) in coastal waters of Suo-Nada, Inland Sea of Japan. Bull. Plankton Soc. Japan 34: 201–204 (in Japanese with English summary)

    Google Scholar 

  • Weiler, C. S., Chisholm, S. W. (1976). Phased cell division in natural populations of marine dinoflagellates from shipboard cultures. J. exp. mar. Biol. Ecol. 25: 239–247

    Article  Google Scholar 

  • Weiler, C. S., Eppley R. W. (1979). Temporal pattern of division in the dinoflagellate genus Ceratium and its application to the determination of growth rate. J. exp. mar. Biol. Ecol. 39: 1–24

    Article  Google Scholar 

  • Wong, P. S. (1989). The occurrence and distribution of red tides in Hong Kong-applications in red tide management. In: Okaichi, T., Anderson, D. M., Nemoto, T. (eds.) Red tides. Biology, environmental science, and toxicology. Elsevier, New York, p. 125–128

    Google Scholar 

  • Yamaguchi, M., Honjo, T. (1989). Effects of temperature, salinity and irradiance on the growth of the noxious red tide flagellate Gymnodinium nagasakiense. Nippon Suisan Gakk. 55: 2029–2036 (in Japanese with English summary)

    Article  Google Scholar 

  • Yamaguchi, M., Honjo, T. (1990). Phased cell division in the noxious red tide flagellate Gymnodinium nagasakiense (Dinophyceae) and application of the frequency of dividing cells technique for the determination of growth rate. Bull. Plankton Soc. Japan 37: 3–18 (in Japanese with English summary)

    Google Scholar 

  • Yentsch, C. M., Mague, F. C., Horan, P. K., Muirhead, K. (1983). Flow cytometric DNA determinations on individual cells of the dinoflagellate Gonyaulax tamarensis var. excavata. J. exp. mar. Biol. Ecol. 67: 175–183

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Nansci National Fisheries Research Institute, Ohno-cho, Saeki-gun, 739-04, Hiroshima, Japan

    M. Yamaguchi

Authors
  1. M. Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by M. Anraku, Suva

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamaguchi, M. DNA synthesis and the cell cycle in the noxious red-tide dinoflagellate Gymnodinium nagasakiense . Mar. Biol. 112, 191–198 (1992). https://doi.org/10.1007/BF00702461

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00702461

Keywords

Search

Navigation