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Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity

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Phosphorus is an obligate requirement for the growth of all organisms; major biochemical reservoirs of phosphorus in marine plankton include nucleic acids and phospholipids1,2,3. However, eukaryotic phytoplankton and cyanobacteria (that is, ‘phytoplankton’ collectively) have the ability to decrease their cellular phosphorus content when phosphorus in their environment is scarce1,4,5. The biochemical mechanisms that allow phytoplankton to limit their phosphorus demand and still maintain growth are largely unknown. Here we show that phytoplankton, in regions of oligotrophic ocean where phosphate is scarce, reduce their cellular phosphorus requirements by substituting non-phosphorus membrane lipids for phospholipids. In the Sargasso Sea, where phosphate concentrations were less than 10 nmol l-1, we found that only 1.3 ± 0.6% of phosphate uptake was used for phospholipid synthesis; in contrast, in the South Pacific subtropical gyre, where phosphate was greater than 100 nmol l-1, plankton used 17 ± 6% (ref. 6). Examination of the planktonic membrane lipids at these two locations showed that classes of sulphur- and nitrogen-containing membrane lipids, which are devoid of phosphorus, were more abundant in the Sargasso Sea than in the South Pacific. Furthermore, these non-phosphorus, ‘substitute lipids’ were dominant in phosphorus-limited cultures of all of the phytoplankton species we examined. In contrast, the marine heterotrophic bacteria we examined contained no substitute lipids and only phospholipids. Thus heterotrophic bacteria, which compete with phytoplankton for nutrients in oligotrophic regions like the Sargasso Sea, appear to have a biochemical phosphorus requirement that phytoplankton avoid by using substitute lipids. Our results suggest that phospholipid substitutions are fundamental biochemical mechanisms that allow phytoplankton to maintain growth in the face of phosphorus limitation.

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Figure 1: Relationships between phosphate and phospholipid synthesis.
Figure 2: Relative phosphorus and nitrogen contents of membrane lipids expressed as atomic ratios to carbon.

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  • 05 March 2009

    The AOP version of this paper contained an inaccuracy in the affiliations


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We thank the captains and crews of the RVs L’Atalante, Atlantic Explorer, Kilo Moana and Ka’imikai-o-Kanaloa. J. Dacey, R. Johnson, N. Levine, T. Gregory, D. Sadler, H. Claustre and A. Sciandra provided access and logistical support for our cruises. K. Björkman and P. Rimmelin provided phosphate data. N. Trowbridge, M. Brandon, S. Haley, E. Orchard and K. Roache-Johnson assisted with cultures. D. Glover provided input on data treatment and presentation. This research was supported by grants from the National Science Foundation (OCE-0646944 to B.A.S.V.M., OCE-0451419 to S.T.D., OCE-0326616 to D.M.K., OCE-0453023 to M.W.L., OCE-0453019 to L.R.M. and DEB-0207085 to M.S.R.), the Office of Naval Research (N00014-06-1-0134 to B.A.S.V.M.) and Czech Republic research grants (GACR-206/07/0241 and GAAV-1QS500200570 to M.K.). The BIOSOPE campaign was a contribution of the French LEFE-CYBER program funded by the Centre National de la Recherche Scientifique and the Institut des Sciences de l’Univers. Funding was also provided by the Gordon and Betty Moore Foundation, the Center for Microbial Oceanography: Research and Education, the Woods Hole Oceanographic Institution Ocean Life Institute and the Woods Hole Oceanographic Institution Mary Sears Travel Fund.

Author Contributions B.A.S.V.M. designed the study, conducted experiments and collected samples at sea, and wrote the manuscript. All of the other authors made essential, substantive contributions to the original and/or revised manuscripts. In addition, H.F.F. analysed lipids by mass spectrometry. B.E.P. assisted with lipid analyses and prepared samples in the laboratory and at sea. S.T.D., M.K., L.R.M., M.S.R. and E.A.W. each contributed to the design of the study and conducted experiments with cultures under phosphorus-limiting and -replete conditions. D.M.K., M.W.L. and T.M. provided data from the cruises and facilitated the work at sea.

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Correspondence to Benjamin A. S. Van Mooy.

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Van Mooy, B., Fredricks, H., Pedler, B. et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009).

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