Divergent Plastid Genomes in the Deepest-Branching Apicomplexan Parasites

Apicomplexans are widespread and diverse obligate symbionts of animals, and many-like the malaria-causing Plasmodium-are important human parasites. Some of the closest free-living relatives of apicomplexans are photosynthetic, and most apicomplexans retain a relict, nonphotosynthetic plastid called the apicoplast. The origin and evolution of this plastid has been studied extensively, but most data come from biomedically relevant taxa. There has been increasing interest in the diversity of plastids of other apicomplexans, which has revealed a complex picture of recurring, independent losses of plastids or their genomes in the deepest-branching apicomplexan lineages, Cryptosporidium and the gregarines. Indeed, the plastid is absent from many of these deep-branching apicomplexans, and those that retain it have almost all lost its genome. The single exception appears to be the archigregarines, the deepest-branching subgroup of gregarines, which are suspected to have retained a genome based on analyses of nuclear genes, but for which no plastid genome data are known. As the best potential representatives of plastid genomes in deep-branching apicomplexans, this lineage is an obvious missing piece of the evolutionary puzzle of the apicoplast. Here, we used single-cell sequencing to characterize the plastid genome from uncultivated representatives of all 4 known archigregarine lineages. The plastid genomes are all more divergent with lower GC-content than other apicoplast genomes, and encode a slightly different set of genes. There is no evidence of photosynthesis-related genes. These genomes fill a key gap in the diversity of apicomplexan plastid genomes, furthering our understanding of the complex evolution of the apicoplast.