Skip to main content
Log in

Examination of hydroxamate-siderophore production by neritic eukaryotic marine phytoplankton

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • 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 

  • 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 

  • 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 

  • 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 

  • Bezkorovainy, A.: Biochemistry of nonheme iron, 435 pp. New York: Plenum Press 1980

    Google Scholar 

  • 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 

  • 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 

  • Garibaldi, J. A. and J. B. Neilands: Formation of iron-binding compounds by microorganisms. Nature, Lond. 177, 526–527 (1956)

    Google Scholar 

  • Gillam, A. H., A. G. Lewis and R. J. Andersen: Quantitative determination of hydroxamate acids. Analyt. Chem. 53, 841–844 (1981)

    Google Scholar 

  • 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 

  • Gonye, E. R. and E. J. Carpenter: Production of iron-binding compounds by marine organisms. Limnol. Oceanogr. 19, 840–841 (1974)

    Google Scholar 

  • 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 

  • Hellebust, J. A.: Extracellular products. In: Algal physiology and biochemistry, pp 838–863. Ed. by W. D. P. Stewart. Berkeley: University of California Press 1974

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Lewin, J. and C. H. Chen: Available iron: a limiting factor for marine phytoplankton. Limnol. Oceanogr. 16, 670–675 (1971)

    Google Scholar 

  • 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 

  • 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 1974

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 1974

    Google Scholar 

  • Raymond, K. N. and C. J. Carrano: Coordination chemistry and microbial iron transport. Accts chem. Res. 12, 183–190 (1979)

    Google Scholar 

  • 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 

  • 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 

  • 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 1973

    Google Scholar 

  • Stuermer, D. H. and G. R. Harvey: Humic substances from seawater. Nature, Lond. 250, 480–481 (1974)

    Google Scholar 

  • Sugimura, Y., Y. Suzuki and Y. Miyake: The dissolved organic iron in seawater. Deep-Sea Res. 25, 309–314 (1978)

    Google Scholar 

  • 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 

  • 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 

  • 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 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by N. D. Holland, La Jolla

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trick, C.G., Andersen, R.J., Price, N.M. et al. Examination of hydroxamate-siderophore production by neritic eukaryotic marine phytoplankton. Mar. Biol. 75, 9–17 (1983). https://doi.org/10.1007/BF00392625

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00392625

Keywords

Navigation