This month's Genome Watch explores apicomplexan adaptation to parasitism.
The Apicomplexa, a group that includes pathogens such as Plasmodium falciparum and Toxoplasma gondii, share common ancestry with algae. Now, two studies1,2 compare apicomplexan genomes and transcriptomes with those of closely related free-living algae to explore the genomic changes that underpinned the transition of apicomplexans to parasitism.
Chromerids are a recently discovered group of algae that can be maintained in the laboratory as free-living photoautotrophs. They were first reported in 2008, when Chromera velia was shown to be more closely related to apicomplexans than any other known organism; and, more recently, Vitrella brassicaformis was the second chromerid to be characterized. In contrast to the photosynthetic chromerids, colpodellids are predatory protists that are also close relatives of the Apicomplexa.
Using Illumina sequencing, Janouškovec et al.1 analysed the transcriptomes of the two known chromerid species and of three colpodellids species, and used a concatenated alignment of 85 predicted protein sequences to create a phylogenetic tree with these 5 species and 35 apicomplexans. The authors found that chromerids and colpodellids formed a sister clade to Apicomplexa, which is consistent with a similar, independently constructed phylogeny by Woo et al.2, who analysed 101 single-copy genes across 26 apicomplexan, chromerid and outgroup species.
Genomic comparison also elucidated the role that gene loss and gain had in the evolution of the Apicomplexa. For example, both studies found that the transition from a free-living to parasitic lifestyle was predominantly characterized by gene loss, particularly of genes associated with metabolic function — such as photosynthesis and sterol biosynthesis — suggesting that metabolic pathways that are critical for free-living organisms were lost as apicomplexan parasites evolved towards an intracellular lifestyle. By contrast, Woo et al. noted that specific genes were gained as Plasmodium spp. and Toxoplasma spp. diverged from common ancestors; in these species, the number of genes encoding exported proteins has increased significantly, suggesting that these genes might have emerged in the context of host–parasite interactions.
Notably, both studies found that many apicomplexan genes previously linked to parasitism were also present in chromerids, and that chromerid genomes encode many proteins that contain functional domains implicated in molecular processes of apicomplexan parasites. To investigate whether there are conserved gene expression modules between chromerids and apicomplexans, Woo et al. measured changes in gene expression in C. velia cultured under different combinations of temperature, iron and salt. These data were then compared with publicly available transcriptome data for P. falciparum that had been subjected to growth perturbations. More than 80 homologous genes annotated as being implicated in invasion showed statistically significant co-expression across different conditions in both species, suggesting that the genome of the proto-apicomplexan ancestor (the last common ancestor of chromerids and apicomplexans) encoded functionally linked proteins that have been utilized differently by free-living and parasitic lineages. The authors noted that the proto-apicomplexan ancestor possessed all known flagellar components — which are essential for motility of the free-living species — whereas these components were progressively lost as individual apicomplexan lineages differentiated, possibly owing to their adaptation to a parasitic lifestyle. However, this is not the case for all flagellar components; for example, the striated fibre assemblin (SFA) protein has been conserved in all apicomplexan genomes. SFA was present in one of the co-expression modules in C. velia that overlapped significantly with P. falciparum; the module also included many invasion-associated genes, including genes encoding a rhoptry protein, apical sushi protein and two gliding motility components. This finding, along with previous ultrastructural studies, has provided strong evidence to support the hypothesis that the apical complex invasion machinery, which is a key feature of Apicomplexa, originated from the flagellar apparatus of a previous ancestor.
In summary, these two studies elucidate the origins of parasitism in Apicomplexa and provide an elegant example of the flexibility of evolution, suggesting that the repurposing and refinement of genes gave rise to a novel function in these organisms.
Janouškovec, J. et al. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl Acad. Sci. USA 112, 10200–10207 (2015).
Woo, Y. H. et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife 4, e06974 (2015).
The authors declare no competing financial interests.
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Owusu, C., Bennett, H. How apicomplexans became free-riders. Nat Rev Microbiol 13, 603 (2015). https://doi.org/10.1038/nrmicro3551