The protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans.
The recent discovery of a vestigial, nonphotosynthetic plastid ("apicoplast") in the Apicomplexa has considerably modified our perception of the evolutionary origin of these parasites. Phylogenetic analysis and the presence of four surrounding membranes of the apicoplast provide important support for the hypothesis that apicomplexans have acquired their apicoplast by secondary endosymbiosis, probably from a green alga. This suggests that genes encoding predicted homologs of proteins of green algae or related photosynthetic lineages could have entered the nucleus of apicomplexan parasites by transfer from the ancestor harboring the apicoplast. We describe here complementary DNAs encoding two Toxoplasma gondii glycolytic enzymes, glucose-6-phosphate isomerase (G6-PI) and enolase, which have considerable identities with land plant counterparts. Both cDNAs of T. gondii complement Escherichia coli mutants lacking G6-PI and enolase genes and lead to the expression of active enzymes. In the drug untreatable encysted bradyzoites of T. gondii, G6-PI and enolase genes are overexpressed or exclusively expressed at both transcriptional and protein levels. Moreover, three-dimensional models and protein phylogeny confirmed that G6-PIs and enolases of T. gondii, Plasmodium falciparum, and land plants are closely related. Because these glycolytic enzymes are plant homologs, which differ from those of animals, they will be useful to trace the evolutionary origin of Apicomplexa and might offer novel chemotherapeutic targets in diseases caused by apicomplexan parasites.
Dzierszinski
F
F
Laboratoire de Chimie Biologique, CNRS UMR 111, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, France.
Popescu
O
O
Toursel
C
C
Slomianny
C
C
Yahiaoui
B
B
Tomavo
S
S
D000595:Amino Acid Sequence; D000818:Animals; D003001:Cloning, Molecular; D019143:Evolution, Molecular; D005786:Gene Expression Regulation; D005816:Genetic Complementation Test; D005956:Glucose-6-Phosphate Isomerase / Q000737:chemistry / Q000235:genetics*; D006019:Glycolysis / Q000235:genetics; D008958:Models, Molecular; D008969:Molecular Sequence Data; D009154:Mutation; D010751:Phosphopyruvate Hydratase / Q000737:chemistry / Q000235:genetics*; D010788:Photosynthesis / Q000235:genetics; D010802:Phylogeny; D011994:Recombinant Proteins / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D016415:Sequence Alignment; D014122:Toxoplasma / Q000201:enzymology* / Q000472:pathogenicity
D011994:Recombinant Proteins; D010751:Phosphopyruvate Hydratase; D005956:Glucose-6-Phosphate Isomerase