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 evolu tionary origin of these parasites. Phylogenetic analysis and the presence o f four surrounding membranes of the apicoplast provide important support fo r the hypothesis that apicomplexans have acquired their apicoplast by secon dary endosymbiosis, probably from a green alga. This suggests that genes en coding predicted homologs of proteins of green algae or related photosynthe tic lineages could have entered the nucleus of apicomplexan parasites by tr ansfer from the ancestor harboring the apicoplast, We describe here complem entary DNAs encoding two Toxoplasma gondii glycolytic enzymes, glucose-6-ph osphate isomerase (G6-PI) and enolase, which have considerable identities w ith 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, Plasmod ium falciparum, and land plants are closely related. Because these glycolyt ic enzymes are plant homologs, which differ from those of animals, they wil l be useful to trace the evolutionary origin of Apicomplexa and might offer novel chemotherapeutic targets in diseases caused by apicomplexan parasite s.