Phytoplankton in the ocean substitute lipids in response to phosphorus scarcity

Van Mooy, B.A.S., Fredricks, H.F., Pedler, B.E., Dyhrman, S.T., Karl, D.M., Koblizek, M., Lomas, M.W., Mincer. T., Moore, L.R., Moutin, T., Rappé, M.S., and Webb, E.A.

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Percentages of total phosphate uptake allocated to phospholipid synthesis and their relationships with phosphate turnover times (a) and phosphate concentrations (b). Solid symbols for South and North Pacific are data from refs 2, 6 and 22. Open symbols for the North Pacific are data from incubations, which were amended with NH₄⁺ at a final concentration of 50 nmol l^-1 (see ref. 3; ambient concentrations are generally of the order of 30 nmol l^-1) in an attempt to increase rates of phosphate uptake. The linear regression in the bottom plot indicates that 36% of the variation in the use of phosphate for phospholipid synthesis can be explained by the variation in phosphate concentrations. This suggests there is a strong, fundamental and global-scale control on phosphate allocation within the planktonic communities in response to variations in phosphorus availability.

Nature. 458:69-72. (2009)

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 plusminus

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 plusminus

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.

Last updated: December 14, 2011