Suggestive evidence for Darwinian selection against asparagine-linked glycans of Plasmodium and Toxoplasma

Eukaryot Cell. 2009 Sep 25. [Epub ahead of print]

Suggestive evidence for Darwinian selection against asparagine-linked glycans of Plasmodium and Toxoplasma

Bushkin GG, Ratner DM, Cui J, Banerjee S, Duraisingh MT, Jennings CV, Dvorin JD, Gubbels MJ, Robertson SD, Steffen M, O'Keefe BR, Robbins PW, Samuelson J.

Department of Molecular and Cell Biology, Boston University Goldman School of Dental Medicine, Boston, Massachusetts 02118; Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, Massachusetts 02115; Department of Biology, Boston College, Chestnut Hill, Massachusetts 02467; Department of Pathology and Laboratory Medicine, Boston University Medical School, Boston, Massachusetts 02118; Molecular Targets Development Program, Center for Cancer Research, NCI-Frederick, Frederick, Maryland 21702.

We are interested in asparagine-linked glycans (N-glycans) of Plasmodium and Toxoplasma, because their N-glycan structures have been controversial and because we hypothesize that there might be selection against N-glycans in nucleus-encoded proteins that must pass through the ER prior to threading into the apicoplast. In support of our hypothesis, we observed the following. First, in protists with apicoplasts, there is extensive secondary loss of Alg enzymes that make lipid-linked precursors to N-glycans. Theileria makes no N-glycans, and Plasmodium makes a severely truncated N-glycan precursor composed of one or two GlcNAc residues. Second, secreted proteins of Toxoplasma, which uses its own 10-sugar precursor (Glc3Man5GlcNAc2) and the host 14-sugar precursor (Glc3Man9GlcNAc2) to make N-glycans, have very few sites for N-glycosylation, and there is additional selection against N-glycan sites in its apicoplast-targeted proteins. Third, while the GlcNAc-binding Griffonia simplicifolia lectin II labels ER, rhoptries, and surface of Plasmodia, there is no apicoplast labeling. Similarly, the anti-retroviral lectin cyanovirin-N, which binds to N-glycans of Toxoplasma, labels ER and rhoptries, but there is no apicoplast labeling. We conclude that possible selection against N-glycans in protists with apicoplasts occurs by eliminating N-glycans (Theileria), reducing their length (Plasmodium), or by reducing the number of N-glycan sites (Toxoplasma). In addition, occupation of N-glycan sites is markedly reduced in apicoplast proteins versus some secretory proteins in both Plasmodium and Toxoplasma.

PMID: 19783771 [PubMed - as supplied by publisher]