The apicomplexan plastid and its evolution

Abstract

Protistan species belonging to the phylum Apicomplexa have a non-photosynthetic secondary plastid-the apicoplast. Although its tiny genome and even the entire nuclear genome has been sequenced for several organisms bearing the organelle, the reason for its existence remains largely obscure. Some of the functions of the apicoplast, including housekeeping ones, are significantly different from those of other plastids, possibly due to the organelle's unique symbiotic origin.

Fig. 1

Apicomplexans and the plastid. a Phylogeny of alveolates and distribution of the plastid. The phylogenetic tree was drawn based on the nuclear-encoded 18S rRNA sequences of representative species available in the databases and suggests only topological relationships between taxa. Distribution of the plastid in most Gregarinasina species has not yet been studied (see text). b Phylogeny of the plastids and their variety. Like red plastids (purple), apicoplasts (red, orange, yellow) have the genome encoding sufB, while organisms with green plastids (green) have the gene encoded in the nucleus. Unlike other plastids, the apicoplast genomes lack 5S rRNA gene (rnf). Like other plastid-bearing organisms, Toxoplasma, Eimeria, and Plasmodium have the Suf system incorporating the SufBCD complex, while Babesia and Theileria lack genes specifying the components of the complex. Toxoplasma, Eimeria, and Plasmodium have a unique hybrid-type heme pathway that involves mitochondrial ALA syntase (ALAS). Although Babesia lacks the heme pathway, it has the PBGS gene forming a tight gene cluster with the SPP gene in the nuclear genome like Toxoplasma, Eimeria, and Plasmodium. Unlike other organisms, Eimeria lacks the intron in the trnL(UAA) gene in the plastid genome

Fig. 2

Evolution of heme biosynthesis in organisms with secondary plastids (hypothesis). The plastid-less ancestor had a non-plastid (N) type heme pathway whereas the algal endosymbiont, which donated the secondary plastid, had a distinct pathway in the plastid (P). Algal genes were transferred to the host nuclear genome one by one. The ancestral organism with a secondary plastid initially had both P- and N-type pathways, but subsequently, one of the two was selected and the other wiped out as redundant. Because chlorophyll synthesis depends on the P-type heme pathway, photosynthetic organisms chose the P-type, throwing the N-type away. By contrast, organisms that were not dependent on photosynthesis kept the N-type; this was often accompanied by loss of the plastid. The apicomplexan ancestor was non-photosynthetic and would lose the P-type. However, the gene complex of PBGS and SPP in the nuclear genome made the loss incomplete, giving rise to a unique P/N hybrid heme pathway (thick line). Thereafter some apicomplexans lost the entire pathway