Marine Biology

, Volume 75, Issue 1, pp 9–17 | Cite as

Examination of hydroxamate-siderophore production by neritic eukaryotic marine phytoplankton

  • C. G. Trick
  • R. J. Andersen
  • N. M. Price
  • A. Gillam
  • P. J. Harrison


Species of neritic eukaryotic marine phytoplankton were investigated during 1982 for hydroxamate-type siderophore production under iron-sufficient and iron-deficient culture conditions. Three of the 5 Prorocentrum species examined produced siderophores. Prorocentrin, the extracellular hydroxamate-type siderophore isolated from P. minimum, was also produced by P. mariae-lebouriae and P. gracile. P. maximum and P. micans grew poorly in iron-deficient medium and did not produce intracellular or extracellular hydroxamate-type siderophores. Thalassiosira pseudonana and Dunaliella tertiolecta produced extracellular siderophores under iron-deficient conditions, but siderophore production was not detected in the other two species, Skeletonema costatum and Olisthodiscus luteus. Each species which produced extracellular Csaky-positive hydroxamate showed a similar pattern of production. Under iron-sufficient conditions there was no measurable siderophore found either intracellularly or extracellularly. Under iron-deficient culture conditions hydroxamate-type siderophore was produced 1 to 2 d after the cessation of growth in the stationary phase. Production was over a short period of time (1 to 2 d) and the siderophore did not remain in the medium. The rate of siderophore disappearance from the medium was similar to the rate of production. Each species which produced siderophores showed an increase in in vivo fluorescence coincidental with the disappearance of the extracellular siderophore from the culture medium. There was no corresponding increase in in vivo fluorescence in iron-sufficient cultures. It is suggested that in vivo fluorescence may be used as a screening procedure for determining hydroxamate-type siderophore production in eukaryotic phytoplankton. An hypothesis on the iron uptake mechanism is proposed.


Phytoplankton Stationary Phase Iron Uptake Dunaliella Uptake Mechanism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Andersen, R. J., M. J. LeBlanc and F. W. Sum: 1(2,6,6-trimethyl-4-hydroxycyclohexenyl)-1,3-butanedione, extracellular metabolite from the dinoflagellate Prorocentrum minimum. J. org. Chem. 45, 1169–1170 (1980)Google Scholar
  2. Anderson, M. A. and F. M. Morel: Uptake of Fe (II) by a diatom in oxic culture medium. Mar. Biol. Lett. 1, 263–268 (1980)Google Scholar
  3. Anderson, M. A. and F. M. Morel: The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol. Oceanogr. 27, 789–813 (1982)Google Scholar
  4. Armstrong, J. E. and C. Van Baalen: Iron transport in microalgae: the isolation and biological activity of a hydroxamate siderophore from the blue-green alga Agmenellum quadruplicatum. J. gen. Microbiol. 111, 253–262 (1979)Google Scholar
  5. Bezkorovainy, A.: Biochemistry of nonheme iron, 435 pp. New York: Plenum Press 1980Google Scholar
  6. Davies, A. G.: Iron, chelation and the growth of marine phytoplankton. I. Growth kinetics and chlorophyll production in cultures of the euryhaline dinoflagellate Dunaliella tertiolecta under iron-limiting conditions. J. mar. biol. Ass. U.K. 50, 65–86 (1970)Google Scholar
  7. Estep, M., J. E. Armstrong and C. Van Baalen: Evidence for the occurrence of specific iron (III)-binding compounds in nearshore marine ecosystems. Appl. Microbiol. 30, 186–188 (1975)Google Scholar
  8. Garibaldi, J. A. and J. B. Neilands: Formation of iron-binding compounds by microorganisms. Nature, Lond. 177, 526–527 (1956)Google Scholar
  9. Gillam, A. H., A. G. Lewis and R. J. Andersen: Quantitative determination of hydroxamate acids. Analyt. Chem. 53, 841–844 (1981)Google Scholar
  10. Glover, H. E.: Iron in Maine coastal waters; seasonal variation and its apparent correlation with the dinoflagellate bloom. Limnol. Oceanogr. 23, 534–537 (1978)Google Scholar
  11. Gonye, E. R. and E. J. Carpenter: Production of iron-binding compounds by marine organisms. Limnol. Oceanogr. 19, 840–841 (1974)Google Scholar
  12. Hayward, J.: Studies on the growth of Phaeodactylum tricornutum. III. The effect of iron on growth. J. mar. biol. Ass. U.K. 48, 295–302 (1968)Google Scholar
  13. Hellebust, J. A.: Extracellular products. In: Algal physiology and biochemistry, pp 838–863. Ed. by W. D. P. Stewart. Berkeley: University of California Press 1974Google Scholar
  14. Hobbie, J. E., R. J. Daley and S. Jasper: Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. envirl Microbiol. 33, 1225–1228 (1977)Google Scholar
  15. Horowitz, N. H., G. Charlang, G. Horn and N. P. Williams: Isolation and identification of the conidial germination factor in Neorospora crassa. J. Bact. 127, 135–140 (1976)Google Scholar
  16. 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
  17. Lewin, J. and C. H. Chen: Available iron: a limiting factor for marine phytoplankton. Limnol. Oceanogr. 16, 670–675 (1971)Google Scholar
  18. Lewin, J. and C. H. Chen: Changes in the concentration of soluble and particulate iron in seawater enclosed in containers. Limnol. Oceanogr. 18, 590–596 (1973)Google Scholar
  19. Light, P. A. and R. A. Clegg: Metabolism in iron limited growth. In: Microbial iron metabolism: a comprehensive treatise, pp 35–63. Ed. by J. B. Neilands. New York: Academic Press 1974Google Scholar
  20. Lyons, W. B., H. E. Gaudette and P. B. Armstrong: Evidence for organically associated iron in nearshore pore fluids. Nature, Lond. 282, 202–203 (1979)Google Scholar
  21. Mantoura, R. F. C. and J. P. Riley: The analytical concentration of humic substances from natural waters. Analytica. chim. Acta 76, 97–106 (1975)Google Scholar
  22. McKnight, D. M. and F. M. Morel: Release of weak and strong copper-complexing agents by algae. Limnol. Oceanogr. 24, 823–837 (1979)Google Scholar
  23. Menzel, D. W. and J. H. Ryther: Nutrients limiting the production of phytoplankton in the Sargasso Sea, with special reference to iron. Deep-Sea Res. 7, 276–281 (1961)Google Scholar
  24. Morel, F. M., J. G. Rueter, D. M. Anderson and R. R. L. Guillard: Aquil: a chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 15, 135–151 (1979)Google Scholar
  25. Murphy, T. P., D. R. S. Lean and C. Nalewajko: Blue-green algae: their excretion of iron-selective chelators enables them to dominate other algae. Science, N.Y. 192, 900–902 (1976)Google Scholar
  26. Myers, J.: Culture conditions and the development of the photosynthetic mechanism. V. Influence of the composition of the nutrient medium. Pl. Physiol., Lancaster, Pa. 22, 590–597 (1947)Google Scholar
  27. Neilands, J. B.: Iron and its role in microbial physiology. In: Microbial iron metabolism: a comprehensive treatise, pp 3–34. Ed. by J. B. Neilands. New York: Academic Press 1974Google Scholar
  28. Raymond, K. N. and C. J. Carrano: Coordination chemistry and microbial iron transport. Accts chem. Res. 12, 183–190 (1979)Google Scholar
  29. Ryther, J. H. and D. D. Kremer: Relative iron requirement of some coastal and off-shore plankton algae. Ecology 42, 444–446 (1961)Google Scholar
  30. Simpson, F. B. and J. B. Neilands: Siderochromes in cyanophyceae: isolation and characterization of schizokinen from Anabaena sp. J. Phycol. 12, 44–48 (1976)Google Scholar
  31. Spencer, L. T., R. T. Barber and R. A. Palmer: The detection of ferric specific organic chelators in marine phytoplankton cultures. In: Food-drugs from the sea, pp 203–216. Ed. by P. C. Singer. Washington: Marine Technology Society 1973Google Scholar
  32. Stuermer, D. H. and G. R. Harvey: Humic substances from seawater. Nature, Lond. 250, 480–481 (1974)Google Scholar
  33. Sugimura, Y., Y. Suzuki and Y. Miyake: The dissolved organic iron in seawater. Deep-Sea Res. 25, 309–314 (1978)Google Scholar
  34. Swallow, K. C., J. C. Westall, D. M. McKnight, N. M. L. Morel and F. M. Morel: Potentiometric determination of copper complexation by phytoplankton exudates. Limnol. Oceanogr. 23, 538–542 (1978)Google Scholar
  35. Trick, C. G., R. J. Andersen, A. Gillam and P. J. Harrison: Prorocentrum: an extracellular siderophore produced by the marine dinoflagellate Prorocentrum minimum. Science, N.Y. 219, 306–308 (1983)Google Scholar
  36. Trick, C. G., P. J. Harrison and R. J. Andersen: Extracellular secondary metabolite production by the marine dinoflagellate Prorocentrum minimum in culture. Can J. Fish. aquat. Sciences 38, 864–867 (1981)Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • C. G. Trick
    • 1
  • R. J. Andersen
    • 2
    • 3
  • N. M. Price
    • 4
    • 5
  • A. Gillam
    • 1
  • P. J. Harrison
    • 4
    • 5
  1. 1.Department of OceanographyUniversity of British ColumbiaVancouverCanada
  2. 2.Department of ChemistryUniversity of British ColumbiaVancouverCanada
  3. 3.Department of OceanographyUniversity of British ColumbiaVancouverCanada
  4. 4.Department of BotanyUniversity of British ColumbiaVancouverCanada
  5. 5.Department of OceanographyUniversity of British ColumbiaVancouverCanada

Personalised recommendations