Abstract
Single-celled apicomplexan parasites are known to cause major diseases in humans and animals including malaria, toxoplasmosis, and coccidiosis. The presence of apicoplasts with the remnant of a plastid-like DNA argues that these parasites evolved from photosynthetic ancestors possibly related to the dinoflagellates. Toxoplasma gondii displays amylopectin-like polymers within the cytoplasm of the dormant brain cysts. Here we report a detailed structural and comparative analysis of the Toxoplasma gondii, green alga Chlamydomonas reinhardtii, and dinoflagellate Crypthecodinium cohnii storage polysaccharides. We show Toxoplasma gondii amylopectin to be similar to the semicrystalline floridean starch accumulated by red algae. Unlike green plants or algae, the nuclear DNA sequences as well as biochemical and phylogenetic analysis argue that the Toxoplasma gondii amylopectin pathway has evolved from a totally different UDP-glucose-based metabolism similar to that of the floridean starch accumulating red alga Cyanidioschyzon merolae and, to a lesser extent, to those of glycogen storing animals or fungi. In both red algae and apicomplexan parasites, isoamylase and glucan–water dikinase sequences are proposed to explain the appearance of semicrystalline starch-like polymers. Our results have built a case for the separate evolution of semicrystalline storage polysaccharides upon acquisition of photosynthesis in eukaryotes.
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Acknowledgments
For comments, logistical support, and invaluable technical assistance in the field and lab, we thank Michael Kibe, Marléne Mortuaire, Hervé Moreau, Christian Slomianny, Emmanuel Maes, Frédéric Chirat, Yves Leroy, Florence Dzierszinski, Brigitte Bouchet, and Bruno Pontoire. We acknowledge the Toxoplasma Genome Sequencing Consortium for making available the genome database: Preliminary genomic and/or cDNA sequence data were accessed via http://ToxoDB.org and/or http://www.tigr.org/tdb/t_gondii/. Genomic data were provided by The Institute for Genomic Research (supported by NIH Grant AI05093), and by the Sanger Center (Wellcome Trust). EST sequences were generated by Washington University (NIH Grant 1R01AI045806-01A1). This research was funded by the Centre National de la Recherche Scientifique (CNRS) through the Action Thématique Incitative sur Programme et Equipe (ATIPE), the Programme Inter-organisme de Microbiologie Fondamentale, and the Agence Nationale de la Recherche sur le Sida (ANRS).
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Coppin, A., Varré, JS., Lienard, L. et al. Evolution of Plant-Like Crystalline Storage Polysaccharide in the Protozoan Parasite Toxoplasma gondii Argues for a Red Alga Ancestry. J Mol Evol 60, 257–267 (2005). https://doi.org/10.1007/s00239-004-0185-6
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DOI: https://doi.org/10.1007/s00239-004-0185-6