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

G. Guy Bushkin, Daniel M. Ratner, Jike Cui, Sulagna Banerjee, Manoj T. Duraisingh, Cameron V. Jennings, Jeffrey D. Dvorin, Marc Jan Gubbels, Seth D. Robertson, Martin Steffen, Barry R. O'Keefe, Phillips W. Robbins, John Samuelson

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58 Scopus citations

Abstract

We are interested in asparagine-linked glycans (N-glycans) of Plasmodium falciparum and Toxoplasma gondii,because their N-glycan structures have been controversial and because we hypothesize that there might beselection against N-glycans in nucleus-encoded proteins that must pass through the endoplasmic reticulum(ER) prior to threading into the apicoplast. In support of our hypothesis, we observed the following. First, inprotists with apicoplasts, there is extensive secondary loss of Alg enzymes that make lipid-linked precursors toN-glycans. Theileria makes no N-glycans, and Plasmodium makes a severely truncated N-glycan precursorcomposed of one or two GlcNAc residues. Second, secreted proteins of Toxoplasma, which uses its own 10-sugarprecursor (Glc3Man5GlcNAc2) and the host 14-sugar precursor (Glc3Man9GlcNAc2) to make N-glycans, havevery few sites for N glycosylation, and there is additional selection against N-glycan sites in its apicoplasttargetedproteins. Third, while the GlcNAc-binding Griffonia simplicifolia lectin II labels ER, rhoptries, andsurface of plasmodia, there is no apicoplast labeling. Similarly, the antiretroviral lectin cyanovirin-N, whichbinds to N-glycans of Toxoplasma, labels ER and rhoptries, but there is no apicoplast labeling. We concludethat possible selection against N-glycans in protists with apicoplasts occurs by eliminating N-glycans (Theileria),reducing their length (Plasmodium), or 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 bothPlasmodium and Toxoplasma.

Original languageEnglish (US)
Pages (from-to)228-241
Number of pages14
JournalEukaryotic Cell
Volume9
Issue number2
DOIs
StatePublished - Feb 2010

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    Bushkin, G. G., Ratner, D. M., Cui, J., Banerjee, S., Duraisingh, M. T., Jennings, C. V., Dvorin, J. D., Gubbels, M. J., Robertson, S. D., Steffen, M., O'Keefe, B. R., Robbins, P. W., & Samuelson, J. (2010). Suggestive evidence for Darwinian selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii. Eukaryotic Cell, 9(2), 228-241. https://doi.org/10.1128/EC.00197-09