Marine Biology

, Volume 95, Issue 4, pp 625–630 | Cite as

Cell-cycle response to nutrient starvation in two phytoplankton species, Thalassiosira weissflogii and Hymenomonas carterae

  • D. Vaulot
  • R. J. Olson
  • S. Merkel
  • S. W. Chisholm


The influence of nutrient deprivation on cell-cycle progression was examined in two phytoplankton species, the diatom Thalassiosira weissflogii (actin) and the coccolithophorid Hymenomonas carterae (cocco II). The diatom was starved for nitrogen, silicon or both, whereas only nitrogen limitation was examined in H. carterae. In both species, nitrogen-starved cells were arrested in the early part of the cell cycle (G1 phase). In the diatom, silicon-starvation arrested cells in late G1 phase and also in the last part of the cell cycle (G2+M). In all cases, cell-cycle arrest could be reversed by addition of fresh medium, but cell-cycling times during the first generation were increased in comparison to those in nutrient replete, steady-state growth conditions. These results supply evidence for simultaneous dual-nutrient limitation of population growth and provide a mechanistic interpretation for the division patterns observed in cultures where nutrients are supplied periodically.


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Literature cited

  1. Alberghina, L. and E. Sturani: Control of growth and of the nuclear division cycle in Neurospora crassa. Microbiol. Rev. 45, 99–122 (1981)Google Scholar
  2. Baserga, R.: Growth in size and cell DNA replication. Expl Cell Res. 151, 1–5 (1984)Google Scholar
  3. Brzezinski, M. A.: The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. J. Phycol. 21, 347–357 (1985)Google Scholar
  4. Chisholm, S. W.: Temporal patterns of cell division in unicellular algae. Can. Bull. Fish. aquat. Sciences 210, 150–181 (1981)Google Scholar
  5. Chisholm, S. W., D. Vaulot and R. J. Olson: Cell cycle controls in phytoplankton: comparative physiology and ecology. In: Cell cycle clocks, pp 365–394. Ed. by L. N. Edmunds. New York: M. Dekker 1984Google Scholar
  6. Crissman, H. A. and J. A. Steinkamp: Rapid one step staining procedures for the analysis of cellular DNA and protein by single and dual laser flow cytometry. Cytometry (N.Y.) 3, 84–90 (1982)Google Scholar
  7. Darley, W. M. and B. E. Volcani: Role of silicon in diatom metabolism. A silicon requirement for deoxyribonucleic acid synthesis in the diatom Cylindrotheca fusiformis Reimann and Lewin. Expl Cell Res. 58, 334–342 (1969)Google Scholar
  8. Darley, W. M. and B. E. Volcani: Synchronized cultures: diatoms. In: Methods in enzymology, Vol. XXIII A. pp 85–96. Ed. by A. San Piero. New York: Academic Press 1971Google Scholar
  9. Darzynkiewicz, Z., H. Crissman, F. Traganos and J. Steinkamp: Cell heterogeneity during the cell cycle. J. cell. Physiol. 113, 465–474 (1982)Google Scholar
  10. Donnan, L., E. P. Carvill, T. J. Gilliland and P. C. L. John: The cell cycles of Chlamydomonas and Chlorella. New Phytol. 99, 1–40 (1985)Google Scholar
  11. Gould, A. R., N. P. Everett, T. L. Wang and H. E. Street: Studies on the control of the cell cycle in cultured plant cells. I. Effects of nutrient limitation and nutrient starvation. Protoplasma 106, 1–13 (1981)Google Scholar
  12. Guillard, R. R. L.: Culture of phytoplankton for feeding marine invertebrates. In: Culture of marine invertebrate animals, pp 29–60. Ed. by W. L. Smith and M. H. Chanley. New York: Plenum Publishing Corporation 1975Google Scholar
  13. Heath, M. R. and C. P. Spencer: A model of the cell cycle and cell division phasing in a marine diatom. J. gen. Microbiol. 131, 411–425 (1985)Google Scholar
  14. Johnston, G. C., R. A. Singer, S. O. Sharrow and M. L. Slater: Cell division in the yeast Saccharomyces cerevisiae growing at different rates. J. gen. Microbiol. 118, 479–484 (1980)Google Scholar
  15. Johnston, R.: Seawater, the natural medium of phytoplankton. II. Trace metals and chelation, and general discussion. J. mar. biol. Ass. U.K. 44, 87–109 (1964)Google Scholar
  16. McAteer, M., L. Donnan and P. C. L. John: The timing of division in Chlamydomonas. New Phytol. 99, 41–56 (1985)Google Scholar
  17. Mitchison, J. M.: The biology of the cell cycle, 313 pp. Cambridge: University Press 1971Google Scholar
  18. Olashaw, N., M. Harrington and W. J. Pledger: The regulation of the cell cycle by multiple growth factors. Cell Biol. int. Rep. (Lond.) 7, 489–491 (1983)Google Scholar
  19. Olson, R. J. and S. W. Chisholm: Effects of photocycles and periodic ammonium supply on three marine phytoplankton species. I. Cell division patterns. J. Phycol. 19, 522–528 (1983)Google Scholar
  20. Olson, R. J. and S. W. Chisholm: Effects of light and nitrogen limitation on the cell cycle of the dinoflagellate Amphidinium carteri. J. Plankton Res. 8, 785–793 (1986)Google Scholar
  21. Olson, R. J., S. L. Frankel, S. W. Chisholm and H. M. Shapiro: An inexpensive flow cytometer for the analysis of fluorescence signals in phytoplankton: chlorophyll and DNA distributions. J. exp. mar. Biol. Ecol. 68, 129–144 (1983)Google Scholar
  22. Olson, R. J., D. Vaulot and S. W. Chisholm: Effect of environmental stresses on the cell cycle of two marine phytoplankton species. Pl. Physiol. 80, 918–925 (1986)Google Scholar
  23. Pardee, A. B., D. L. Coppock and H. C. Yang: Regulation of cell proliferation at the onset of DNA synthesis. J. Cell Sci. (Suppl.) 4, 171–180 (1986)Google Scholar
  24. Pardee, A. B., R. Dubron, J. L. Hamlin and R. F. Klevtzien: Animal cell cycle. A. Rev. Biochem. 47, 715–750 (1978)Google Scholar
  25. Singer, R. A. and G. C. Johnston: Growth and the DNA-division sequence in the yeast Saccharomyces cerevisiae. Expl Cell Res. 157, 387–396 (1985)Google Scholar
  26. Slater, M. L., S. O. Sharrow and J. J. Gart: Cell cycle of Saccharomyces cerevisiae in populations growing at different rates. Proc. natn. Acad. Sci. U.S.A. 74, 3850–3954 (1977)Google Scholar
  27. Spencer, C. P.: Studies on the culture of a marine diatom. J. mar. biol. Ass. U.K. 33, 265–290 (1954)Google Scholar
  28. Spudich, J. and R. Sager: Regulation of Chlamydomonas cell cycle by light and dark. J. Cell Biol. 85, 136–145 (1980)Google Scholar
  29. Sullivan, C. W. and B. E. Volcani: Role of silicon in diatom metabolism. III. The effects of silicic acid on DNA polymerase, TMP kinase and DNA synthesis in Cylindrotheca fusiformis. Biochim. biophys. Acta 308, 205–211 (1973)Google Scholar
  30. Sullivan, C. W. and B. E. Volcani: Silicon in the cellular metabolism of diatoms. In: Silicon and siliceous structures in biological systems, pp 15–42. Ed. by T. L. Simpson and B. E. Volcani. New York: Springer Verlag 1981Google Scholar
  31. Vaulot, D.: Cell cycle controls in marine phytoplankton, 268 pp. Ph.D. thesis, Massachusetts Institute of Technology/Woods Hole Oceanographic Institution 1985. (Ref. WHOI-85-10)Google Scholar
  32. Vaulot, D. and S. W. Chisholm: A simple model of the growth of phytoplankton populations in light/dark cycles. 9, 345–366 J. Plankton Res. (1987)Google Scholar
  33. Vaulot, D., R. J. Olson and S. W. Chisholm: Light and dark control of the cell cycle in two phytoplankton species. 80, 918–925 Expl Cell Res. (1986)Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • D. Vaulot
    • 1
  • R. J. Olson
    • 1
  • S. Merkel
    • 1
  • S. W. Chisholm
    • 1
  1. 1.Ralph M. Parsons Laboratory 48-425Massachusetts Institute of TechnologyCambridgeUSA

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