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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Geider, R. J. & La Roche, J. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 37, 1–17 (2002)
Van Mooy, B. A. S., Rocap, G., Fredricks, H. F., Evans, C. T. & Devol, A. H. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl Acad. Sci. USA 103, 8607–8612 (2006)
Van Mooy, B. A. S. & Devol, A. H. Assessing nutrient limitation of Prochlorococcus in the North Pacific subtropical gyre by using an RNA capture method. Limnol. Oceanogr. 53, 78–88 (2008)
Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003)
Krauk, J. M., Villareal, T. A., Sohm, J. A., Montoya, J. P. & Capone, D. G. Plasticity of N:P ratios in laboratory and field populations of Trichodesmium spp. Aquat. Microb. Ecol. 42, 243–253 (2006)
Van Mooy, B. A. S., Moutin, T., Duhamel, S., Rimmelin, P. & Van Wambeke, F. Phospholipid synthesis rates in the eastern subtropical South Pacific Ocean. Biogeosciences 5, 133–139 (2008)
Wu, J., Sunda, W., Boyle, E. A. & Karl, D. M. Phosphate depletion in the western North Atlantic Ocean. Science 289, 759–762 (2000)
Zubkov, M. V. et al. Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ. Microbiol. 9, 2079–2089 (2007)
Sanudo-Wilhelmy, S. A. et al. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66–69 (2001)
Mills, M. M., Ridame, C., Davey, M. & La Roche, J. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004)
Thingstad, T. F. et al. Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309, 1068–1071 (2005)
Moore, C. M. et al. Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean. Limnol. Oceanogr. 53, 291–305 (2008)
McGillicuddy, D. J. et al. Eddy/wind interactions stimulate extraordinary mid-ocean plankton blooms. Science 316, 1021–1026 (2007)
Björkman, K. & Karl, D. M. Bioavailability of dissolved organic phosphorus in the euphotic zone at station ALOHA, North Pacific subtropical gyre. Limnol. Oceanogr. 48, 1049–1057 (2003)
Moore, L. R., Ostrowski, M., Scanlan, D. J., Feren, K. & Sweetsir, T. Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria. Aquat. Microb. Ecol. 39, 257–269 (2005)
Lomas, M. W., Swain, A., Shelton, R. & Ammerman, J. W. Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton. Limnol. Oceanogr. 49, 2302–2310 (2004)
Dyhrman, S. T. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium . Nature 439, 68–71 (2006)
Webb, E., Jakuba, R., Moffet, J. & Dyhrman, S. Molecular assessment of phosphorus and iron physiology in Trichodesmium populations from the western central and western South Atlantic. Limnol. Oceanogr. 52, 2221–2232 (2007)
Benning, C., Beatty, J. T., Prince, R. C. & Somerville, C. R. The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc. Natl Acad. Sci. USA 90, 1561–1565 (1993)
Sato, N., Hagio, M., Wada, H. & Tsuzuki, M. in Recent Advances in the Biochemistry of Plant Lipids (eds Harwood, J. L. & Quinn, P. J.) (Portland Press, 2000)
Ammerman, J. W., Hood, R. R., Case, D. A. & Cotner, J. B. Phosphorus deficiency in the Atlantic: an emerging paradigm in oceanography. Eos 84, 165–170 (2003)
Moutin, T. et al. Phosphate availability and the ultimate control of new nitrogen input by nitrogen fixation in the tropical Pacific Ocean. Biogeosciences 5, 95–109 (2008)
Güller, S., Essigmann, B. & Benning, C. A cyanobacterial gene, sqdX, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglycerol. J. Bacteriol. 182, 543–545 (2000)
Koblížek, M., Mašín, M., Ras, J., Poulton, A. J. & Prášil, O. Rapid growth rates of aerobic anoxygenic phototrophs in the ocean. Environ. Microbiol. 9, 2401–2406 (2007)
Rappé, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, J. Cultivation of ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002)
Riekhof, W. R., Andre, C. & Benning, C. Two enzymes, BtaA and BtaB, are sufficient for betaine lipid biosynthesis in bacteria. Arch. Biochem. Biophys. 441, 96–105 (2005)
Weissenmayer, B. & Gao, J.-L. I. M. L.-L. &. Geiger, O. Identification of a gene required for the biosynthesis of ornithine-derived lipids. Mol. Microbiol. 45, 721–733 (2002)
Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005)
Carlson, C. A., Ducklow, H. W. & Sleeter, T. D. Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep-Sea Res. II 43, 491–515 (1996)
Mills, M. M. et al. Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol. Oceanogr. 53, 824–834 (2008)
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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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). https://doi.org/10.1038/nature07659
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