Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red alga ancestry.
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.
Coppin
Alexandra
A
Laboratoire de Chimie Biologique, CNRS UMR 8576, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq cedex, France.
Varré
Jean-Stéphane
JS
Lienard
Luc
L
Dauvillée
David
D
Guérardel
Yann
Y
Soyer-Gobillard
Marie-Odile
MO
Buléon
Alain
A
Ball
Steven
S
Tomavo
Stanislas
S
D000595:Amino Acid Sequence; D000818:Animals; D016825:Chlamydomonas reinhardtii / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D003460:Crystallization; D004141:Dinoflagellida / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D019143:Evolution, Molecular; D006004:Glycogen Debranching Enzyme System / Q000235:genetics; D006801:Humans; D008854:Microscopy, Electron; D010802:Phylogeny; D011134:Polysaccharides / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism*; D000461:Rhodophyta / Q000235:genetics* / Q000378:metabolism* / Q000648:ultrastructure; D017386:Sequence Homology, Amino Acid; D014122:Toxoplasma / Q000235:genetics* / Q000378:metabolism* / Q000472:pathogenicity / Q000648:ultrastructure
D006004:Glycogen Debranching Enzyme System; D011134:Polysaccharides