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Vol. 17, Issue 2, 1006-1017, February 2006

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Depletion of Phosphatidylcholine in Yeast Induces Shortening and Increased Saturation of the Lipid Acyl Chains: Evidence for Regulation of Intrinsic Membrane Curvature in a Eukaryote

Henry A. Boumann ^*, Jacob Gubbens ^*, Martijn C. Koorengevel ^*, Chan-Seok Oh , Charles E. Martin , Albert J.R. Heck , Jana Patton-Vogt , Susan A. Henry ^||, Ben de Kruijff ^*, and Anton I.P.M. de Kroon ^*

^* Department of Biochemistry of Membranes, Bijvoet Institute and Institute of Biomembranes, Utrecht University, 3584 CH Utrecht, The Netherlands; Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854; Department of Biomolecular Mass Spectrometry, Bijvoet Center for Biomolecular Research and Institute for Pharmaceutical Sciences, 3584 CA Utrecht, The Netherlands; Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282; and ^|| Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853

Submitted April 25, 2005; Revised November 23, 2005; Accepted November 28, 2005
Monitoring Editor: Sean Munro

To study the consequences of depleting the major membrane phospholipid phosphatidylcholine (PC), exponentially growing cells of a yeast cho2opi3 double deletion mutant were transferred from medium containing choline to choline-free medium. Cell growth did not cease until the PC level had dropped below 2% of total phospholipids after four to five generations. Increasing contents of phosphatidylethanolamine (PE) and phosphatidylinositol made up for the loss of PC. During PC depletion, the remaining PC was subject to acyl chain remodeling with monounsaturated species replacing diunsaturated species, as shown by mass spectrometry. The remodeling of PC did not require turnover by the SPO14-encoded phospholipase D. The changes in the PC species profile were found to reflect an overall shift in the cellular acyl chain composition that exhibited a 40% increase in the ratio of C16 over C18 acyl chains, and a 10% increase in the degree of saturation. The shift was stronger in the phospholipid than in the neutral lipid fraction and strongest in the species profile of PE. The shortening and increased saturation of the PE acyl chains were shown to decrease the nonbilayer propensity of PE. The results point to a regulatory mechanism in yeast that maintains intrinsic membrane curvature in an optimal range.

Abbreviations used: DAG, diacylglycerol; DME, N,N-dimethylamino-ethanol; ESI-MS/MS, electrospray ionization tandem mass spectrometry; MME, 2-(methylamino)-ethanol; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PI, phosphatidylinositol; PS, phosphatidylserine.

Address correspondence to: Anton I.P.M. de Kroon (a.i.p.m.dekroon{at}chem.uu.nl).

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