Lipidomic Analysis of Toxoplasma gondii Reveals Unusual Polar Lipids

Abstract

Analysis of the polar lipids of Toxoplasma gondii by electrospray ionization tandem mass spectrometry provides a detailed picture of the lipid molecular species of this parasitic protozoan. Most notably, T. gondii contains a relatively high level, estimated to about 2% of the total polar lipid, of ceramide phosphoethanolamine. The ceramide phosphoethanolamine has a fatty amide profile with only 16-and 18-carbon species. Compared with the host fibroblasts in which it was grown, T. gondii also has higher levels of phosphatidylcholine, but lower levels of sphingomyelin and phosphatidylserine. Analysis at the molecular species level indicated that T. gondii has greater amounts of shorter-chain fatty acid in its polar lipid molecular species than the host fibroblasts. Shorter-chain fatty acids with a combined total of 30 or fewer acyl carbons make up 21% of Toxoplasma's, but only 3% of the host's, diacyl phosphatidylcholine. Furthermore, diacyl phosphatidylcholine with two saturated acyl chains with 12, 14, or 16 carbons make up over 11% of parasite phosphatidylcholine, but less than 3% of the host phosphatidylcholine molecular species. The distinctive T. gondii tachyzoite lipid profile may be particularly suited to the function of parasitic membranes and the interaction of the parasite with the host cell and the host's immune system. Combined with T. gondii genomic data, these lipidomic data will assist in elucidation of metabolic pathways for lipid biosynthesis in this important human pathogen. † This work was supported by NIH NIAID R01s AI27530, AI43228, AI071319, the Research to Prevent Blindness Foundation, and gifts from the Kieweit, Blackmon, Brennan, Koshland, Langel, Morel, Rosenstein, Cussen, Kapnick, and Rooney-Alden families. Work and instrument acquisition at the Kansas Lipidomics Research Center Analytical Laboratory were supported by grants from NSF (MCB 0455318 and DBI 0521587) and NSF's EPSCoR program (EPS-0236913), with matching support from the State of Kansas through Kansas Technology Enterprise Corporation and Kansas State University, as well from NIH grant P20 RR016475 from the INBRE program of the National Center for Research Resources. This is contribution 07-308-J from the Kansas Agricultural Experiment Station.*To whom correspondence should be addressed: Rima McLeod, M.D., The University of Chicago, AMBH S206; 5841 S Maryland Avenue, Chicago, Illinois 60637, Email: rmcleod@midway.uchicago.edu. 1 Abbreviations: ceramide, Cer; ceramide phosphoethanolamine, PE-cer; dihexosylceramide, Dihex-cer; electrospray ionization, ESI; mass spectrometry, MS; phosphatidic acid, PA; phosphatidylcholine, PC; (alkyl or alkenyl)/acyl glycerophosphocholine, ePC; phosphatidylethanolamine, PE; (alkyl or alkenyl)/acyl glycerophosphoethanolamine, ePE; phosphatidylinositol, PI; (alkyl or alkenyl)/ acyl glycerophosphoserine, ePS; Hexosyl ceramide, Hex-cer; phosphatidylserine, PS; sphingomyelin, SM; tandem mass spectrometry, MS/MS. Toxoplasma gondii infects 2-3 billion people throughout the world and is known ...

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