Biogeochemistry

, Volume 2, Issue 2, pp 179–196 | Cite as

Sulfate inhibition of molybdate assimilation by planktonic algae and bacteria: some implications for the aquatic nitrogen cycle

  • Jonathan J. Cole
  • Robert W. Howarth
  • Scott S. Nolan
  • Roxanne Marino
Article

Abstract

Molybdenum is required for both dinitrogen fixation and nitrate assimilation. In oxic waters the primary form of molybdenum is the molybdate anion. Using radioactive [99Mol Na2MoO4, we have shown that the transport of molybdate by a natural assemblage of freshwater phytoplankton is light-dependent and follows typical saturation kinetics. The molybdate anion is strikingly similar to sulfate and we present data to show that sulfate is a competitive inhibitor of molybdate assimilation by planktonic algae and bacteria. The ability of freshwater phytoplankton to transport molybdate is inhibited at sulfate concentrations as low as 5% of those in seawater and at sulfate: molybdate ratios as low as 50 to 100 times lower than those found in seawater, Similarly, the growth of both a freshwater bacterium and a saltwater diatom was inhibited at sulfate: molybdate ratios lower than those in seawater.

The ratio of sulfate to molybdate is 10 to 100 times greater in seawater than in fresh water. This unfavorable sulfate: molybdate ratio may make molybdate less biologically available in the sea. The sulfate: molybdate ratio may explain, in part, the low rates of nitrogen fixation in N-limited salt waters.

Key words

molybdenum molybdate nutrient limitation phytoplankton 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alexander M (1977) Introduction to soil microbiology. J. Wiley & Sons, New York. 467 ppGoogle Scholar
  2. Bachmann R and Goldman CR (1964) The determination of microgram quantities of molybdenum in natural waters. Limnology and Oceanography 9: 143–146Google Scholar
  3. Boutros O, Caraco N, Denison W and Valiela I (1982) Effects of eutrophication on the increase of chlorophyll-a in phytoplankton from coastal water. Biological Bulletin 163: 362Google Scholar
  4. Boynton WR, Kemp WM and Keefe CW (1982) A comparative analysis of nutrients and other factors influencing phytoplankton production. pp 69–99 in Kennedy VS (ed.) Estuarine Comparisons, Academic Press, New YorkGoogle Scholar
  5. Capone DG and Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217–1140–1142Google Scholar
  6. Cardin CJ and Mason J (1976) Molybdate and tungstate transfer in rat ileum: competitive inhibition by sulphate. Biochimica Biophysica Acta 455: 937–946Google Scholar
  7. Codispoti LA (1984) Variation in the marine combined nitrogen inventory. Eos 65: 913Google Scholar
  8. Cotton FA and Wilkinson G (1972) Advanced Inorganic Chemistry, third edition. Wiley Interscience, New YorkGoogle Scholar
  9. Doremus C (1982) Geochemical control of dinitrogen fixation in the open ocean. Biological Oceanography 1: 429–436Google Scholar
  10. Elliott BB and Mortenson LE (1975) Transport of molybdate byClostridium pasteurianum. Journal of Bacteriology 124: 1295–1301Google Scholar
  11. Evans HT jr, Manheim FT and Landergren S (1978) Molybdenum. Chapter 42. In Handbook of Geochemistry. Volume II-5. New YorkGoogle Scholar
  12. Finstein MS and Delwiche CC (1965) Molybdenum as a micronutrient forNitrobacter. Journal of Bacteriology 89: 123–128Google Scholar
  13. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. pp 29–60. In Smith WL and Chanley MH (eds.) Culture of marine invertebrate animals, Plenum, New YorkGoogle Scholar
  14. Huisingh J and Matrone G (1975) Biological interactions of sulfate and molybdate. Environmental Health Perspectives 10: 265Google Scholar
  15. Howarth RW and Cole JJ (1985) Molybdenum availability, nitrogen limitation and phytoplankton growth in natural waters. Science 229: 653–655Google Scholar
  16. Knowles R (1982) Denitrification. Microbiological Reviews 46: 43–70Google Scholar
  17. Martinez LA, Silver MW, King JM and Alldredge AL (1983) Nitrogen fixation by floating diatom mats: A source of new nitrogen to oligotrophic ocean waters. Science 221: 152–154Google Scholar
  18. Nixon SW, Kelly JR, Furnas BN, Oviatt CA and Hale SS (1980) Phosphorus regeneration and the metabolism of coastal marine bottom communities. In Tenore KR and Coul BC (eds). Marine Benthic Dynamics. Univ. S. Carolina Press. pp 219–242Google Scholar
  19. Redfield A (1958) The biological control of chemical factors in the environment. American Scientist 46: 205–221Google Scholar
  20. Ryther JH and Dunstan WM (1971) Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008–1013Google Scholar
  21. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260–262Google Scholar
  22. Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnology and Oceanography 29: 1149–1160Google Scholar
  23. Stout PR and Meagher WR (1948) Studies of the molybdenum nutrition of plants with radioactive molybdenum. Science 108: 471–473Google Scholar
  24. Vince S and Valiela I (1973) The effects of ammonium and phosphate enrichments on chlorophyll-a, pigment ratio and species composition of phytoplankton of Vineyard Sound. Marine Biology 19: 69–73Google Scholar
  25. Wetzel RG (1975) Limnology. W.B. Saunder Co. Philadelphia. 743 ppGoogle Scholar
  26. Wright RT and Hobbie JE (1966) Use of glucose and acetate by bacteria and algae in aquatic ecosystems. Ecology 47: 447–464Google Scholar

Copyright information

© Martinus Nijhoff/Dr W. Junk Publishers 1986

Authors and Affiliations

  • Jonathan J. Cole
    • 1
  • Robert W. Howarth
    • 2
  • Scott S. Nolan
    • 1
  • Roxanne Marino
    • 2
  1. 1.Institute of Ecosystem StudiesMillbrookUSA
  2. 2.Section of Ecology and Systematics, Corson HallCornell UniversityIthacaUSA

Personalised recommendations