1. Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA
2. Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA
3. Department of Oceanography, University of Hawaii, Honolulu, Hawaii, USA
4. Institute of Microbiology, Czech Academy of Sciences, Tebo, Czech Republic
5. Institute of Physical Biology, University of South Bohemia, Nové Hrady, Czech Republic
6. Bermuda Institute of Ocean Sciences, St. George, Bermuda
7. Department of Biological Sciences, University of Southern Maine, Portland, Maine, USA
8. Laboratoire d'Océanographie Physique et Biogéochimique, Centre d'Océanologie de Marseille, Aix-Marseille University, France
9. Hawaii Institute of Marine Biology, University of Hawaii, Kaneohe, Hawaii, USA
10. Department of Biological Sciences, University of Southern California, Los Angeles, California, USA
11. Present address: Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California, USA.

Correspondence to: Benjamin A. S. Van Mooy¹ Correspondence and requests for materials should be addressed to B.A.S.V.M. (Email: bvanmooy@whoi.edu).

Abstract

Phosphorus is an obligate requirement for the growth of all organisms; major biochemical reservoirs of phosphorus in marine plankton include nucleic acids and phospholipids^{1, 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 scarce^{1, 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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