Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments

Abstract

There is growing evidence that dissolved phosphorus can regulate planktonic production in the oceans' subtropical gyres, yet there is little quantitative information about the biochemical fate of phosphorus in planktonic communities. We observed in the North Pacific Subtropical Gyre (NPSG) that the synthesis of membrane lipids accounted for 18-28% of the phosphate (PO4(3-)) taken up by the total planktonic community. Paradoxically, Prochlorococcus, the cyanobacterium that dominates NPSG phytoplankton, primarily synthesizes sulfoquinovosyldiacylglycerol (SQDG), a lipid that contains sulfur and sugar instead of phosphate. In axenic cultures of Prochlorococcus, it was observed that <1% of the total PO4(3-) uptake was incorporated into membrane lipids. Liquid chromatography/mass spectrometry of planktonic lipids in the NPSG confirmed that SQDG was the dominant membrane lipid. Furthermore, the analyses of SQDG synthesis genes from the Sargasso Sea environmental genome showed that the use of sulfolipids in subtropical gyres was confined primarily to picocyanobacteria; no sequences related to known heterotrophic bacterial SQDG lineages were found. This biochemical adaptation by Prochlorococcus must be a significant benefit to these organisms, which compete against phospholipid-rich heterotrophic bacteria for PO4(3-). Thus, evolution of this "sulfur-for-phosphorus" strategy set the stage for the success of picocyanobacteria in oligotrophic environments and may have been a major event in Earth's early history when the relative availability of sulfate and PO4(3-) were significantly different from today's ocean.

Fig. 1.

The fraction of total ³³PO₄³⁻ uptake that was recovered as phospholipids in incubations of NPSG total plankton (striped), Prochlorococcus cultures (white), AP bacteria cultures (gray), and heterotrophic bacteria cultures (black).

Fig. 2.

HPLC/ESI-IT-MSⁿ base peak chromatograms of membrane lipids for Prochlorococcus 9312 (Upper) and the total planktonic community from the NPSG (Lower). The vertical axis approximates relative abundance, although the MS is more sensitive to PG than SQDG, which exaggerates the relative size of the PG peaks. Fractions of each membrane lipid are listed in Table 1. Broad or doublet peaks are due to variations in fatty acid chain length. Generic formulas are used to represent common fatty acid tail groups of the intact lipid molecules. Abbreviations for chemical names are given in the text.

Fig. 3.

Tree of SqdB sequences from the Sargasso Sea environmental genome (denoted SSEG) (33) and representative phytoplankton and heterotrophic bacteria. UDP-galactose 4-epimerases are used as outgroups. The quantities of closely related SSEG sequences are indicated in parentheses. (Scale bar indicates substitutions site⁻¹.)