Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Modulation of cadmium uptake in phytoplankton by seawater CO2 concentration


The vertical distribution of cadmium in the ocean is characteristic of an algal nutrient1,2, although an underlying physiological basis remains undiscovered. The strong correlation between dissolved cadmium and phosphorus concentrations in sea water has nevertheless been exploited for reconstructing past nutrient distributions in the ocean3,4,5. In culture experiments, the addition of cadmium accelerates the growth of some marine phytoplankton6,7,8,9 and increases the activity of carbonic anhydrase, normally a zinc-based metalloenzyme that is involved in inorganic carbon acquisition7,9. Here we show that the concentration of a Cd-carbonic-anhydrase—distinct from Zn-carbonic-anhydrases—in a marine diatom is regulated by the CO2 partial pressure ( p CO 2 ) as well as by the zinc concentration. Field studies in intensely productive coastal waters off central California demonstrate that cadmium content in natural phytoplankton populations similarly increases as surface-water p CO 2 decreases. Incubation experiments confirm that cadmium uptake by natural phytoplankton is inversely related to seawater p CO 2 and zinc concentration. We thus propose that biological removal of cadmium from ocean surface waters is related to its utilization in carbonic anhydrase, and is regulated by dissolved CO2 and zinc concentrations. The dissolved seawater Cd/P ratio would therefore vary with atmospheric p CO 2 , complicating the use of cadmium as a tracer of past nutrient concentrations in the upper ocean.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: Modulation of Cd-carbonic-anhydrase (Cd-CA) by p CO 2 and Zn.
Figure 2: Phytoplankton Cd/P and chlorophyll a fluorescence versus p CO 2 in field samples.
Figure 3: Cd/P versus Zn/P for phytoplankton off central California.
Figure 4: Cd/C uptake of phytoplankton grown at varying p CO 2 and [Zn(aq.)].


  1. Boyle,E. A., Sclater,F. & Edmond,J. M. On the marine geochemistry of cadmium. Nature 263, 42–44 (1976).

    Article  ADS  CAS  Google Scholar 

  2. Bruland,K. W. Oceanographic distributions of cadmium, zinc, nickel, and copper in the north Pacific. Earth Planet. Sci. Lett. 47, 176–198 (1980).

    Article  ADS  CAS  Google Scholar 

  3. Boyle,E. A. Cd and 13C paleochemical ocean distributions during the stage 2 glacial maximum. Annu. Rev. Earth Planet. Sci. 20, 245–287 (1992).

    Article  ADS  CAS  Google Scholar 

  4. van Geen,A. et al. Evidence from Cd/Ca ratios in foraminifera for greater upwelling of California 40,000 years ago. Nature 358, 54–56 (1992).

    Article  ADS  CAS  Google Scholar 

  5. Rosenthal,Y., Boyle,E. A. & Labeyrie,L. Last glacial maximum paleochemistry and deepwater circulation in the Southern Ocean: Evidence from foraminiferal cadmium. Paleoceanography 12, 778–787 (1997).

    Article  ADS  Google Scholar 

  6. Price,N. M. & Morel,F. M. M. Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344, 658–660 (1990).

    Article  ADS  CAS  Google Scholar 

  7. Morel,F. M. M. et al. Zinc and carbon colimitation of marine phytoplankton. Nature 369, 740–742 (1994).

    Article  ADS  CAS  Google Scholar 

  8. Lee,J. G. & Morel,F. M. M. Replacement of zinc by cadmium in marine phytoplankton. Mar. Ecol. Prog. Ser. 127, 305–309 (1995).

    Article  ADS  CAS  Google Scholar 

  9. Lee,J. G., Roberts,S. B. & Morel,F. M. M. Cadmium: a nutrient for the marine diatom Thalassiosira weissflogii. Limnol. Oceanogr. 40, 1056–1063 (1995).

    Article  ADS  CAS  Google Scholar 

  10. Bruland,K. W. Complexation of cadmium by natural organic ligands in the central North Pacific. Limnol. Oceanogr. 37, 1008–1017 (1992).

    Article  ADS  CAS  Google Scholar 

  11. Bruland,K. W. Oceanic zinc speciation: complexation of zinc by natural organic ligands in the central North Pacific. Limnol. Oceanogr. 34, 267–283 (1989).

    Article  ADS  Google Scholar 

  12. Sunda,W. G. & Huntsman,S. A. Control of cadmium concentrations in a coastal diatom by interactions among free ionic Cd, Zn, and Mn in seawater. Environ. Sci. Technol. 32, 2961–2968 (1998).

    Article  ADS  CAS  Google Scholar 

  13. Riebesell,U., Wolf-Gladrow,D. A. & Smetacek,V. Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361, 249–251 (1993).

    Article  ADS  CAS  Google Scholar 

  14. Goldman,J. C. Potential role of large oceanic diatoms in new primary production. Deep-Sea Res. I 40, 159–168 (1993).

    Article  Google Scholar 

  15. Dugdale,R. C. & Wilkerson,F. P. Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391, 270–273 (1998).

    Article  ADS  CAS  Google Scholar 

  16. Smetacek,V. Diatoms and the silicate factor. Nature 391, 224–225 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Frew,R. D. & Hunter,K. A. Influence of Southern Ocean waters on the cadmium-phosphate properties of the global ocean. Nature 360, 144–146 (1992).

    Article  ADS  CAS  Google Scholar 

  18. Löscher,B. M., de Jong,J. T. M. & de Baar,H. J. W. The distribution and preferential biological uptake of cadmium at 6°W in the Southern Ocean. Mar. Chem. 62, 259–286 (1998).

    Article  Google Scholar 

  19. Nolting,R. F. & de Baar,H. J. W. Behaviour of nickel, copper, zinc and cadmium in the upper 300m of a transect in the Southern Ocean (57°–62°S, 49°W). Mar. Chem. 45, 225–242 (1994).

    Article  CAS  Google Scholar 

  20. Takahashi,T. et al. Global air-sea flux of CO2: An estimate based on measurements of sea-air pCO2 difference. Proc. Natl Acad. Sci. 94, 8292–8299 (1997).

    Article  ADS  CAS  Google Scholar 

  21. de Baar,H. J. W., Saager,P. M., Notling,R. F. & van der Meer,J. Cadmium versus phosphate in the world ocean. Mar. Chem. 46, 261–281 (1994).

    Article  CAS  Google Scholar 

  22. Rutgers van der Loeff,M., Helmers,E. & Kattner,G. Continuous transects of cadmium, copper, and aluminium in surface waters of the Atlantic Ocean, 50°N to 50°S: Correspondence and contrast with nutrient-like behaviour. Geochim. Cosmochim. Acta 61, 47–61 (1997).

    Article  ADS  CAS  Google Scholar 

  23. Fischer,H., Wahlen,M., Smith,J., Mastroianni,D. & Deck,B. Ice core records of atmospheric CO2 around the last three glacial terminations. Science 283, 1712–1714 (1999).

    Article  ADS  CAS  Google Scholar 

  24. Petit,J. R. et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436 (1999).

    Article  ADS  CAS  Google Scholar 

  25. Kumar,N. et al. Increased biological productivity and export production in the glacial Southern Ocean. Nature 378, 675–680 (1995).

    Article  ADS  CAS  Google Scholar 

  26. Rickaby,R. E. M. & Elderfield,H. Planktonic foraminiferal Cd/Ca: Paleonutrients or paleotemperature? Paleoceanography 14, 293–303 (1999).

    Article  ADS  Google Scholar 

  27. Roberts,S. B., Lane,T. W. & Morel,F. M. M. Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J. Phycol. 33, 845–850 (1997).

    Article  CAS  Google Scholar 

  28. Cullen,J. T. & Sherrell,R. M. Techniques for determination of trace metals in small samples of size-fractionated particulate matter: phytoplankton metals off central California. Mar. Chem. (in the press).

  29. Feely,R. A. et al. Hydrothermal plume particles and dissolved phosphate over the superfast-spreading southern East Pacific Rise. Geochim. Cosmochim. Acta 60, 2297–2323 (1996).

    Article  ADS  CAS  Google Scholar 

Download references


We thank A. van Geen and M. Wells for providing shipboard space and supporting data; T. Takahashi and C. Sweeney for underway p CO 2 measurements; Y. Rosenthal, P. Falkowski, I. Berman-Frank and M. Behrenfeld for comments on an earlier version of the manuscript; P. Tortell for assistance at sea; and P. Field and I. Shaperdoth for assistance in the laboratory. This work was supported by the NSF and the DOE.

Author information

Authors and Affiliations


Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cullen, J., Lane, T., Morel, F. et al. Modulation of cadmium uptake in phytoplankton by seawater CO2 concentration. Nature 402, 165–167 (1999).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing