Genome Watch: How Apicomplexans Became Free-Riders

Home , Apicomplexa, Chromera velia, Vitrella brassicaformis

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GENOME WATCH How apicomplexans became free-riders Christian K. Owusu and Hayley M. Bennett

This month’s Genome Watch explores sterol biosynthesis — suggesting that meta- of the proto-apicomplexan ancestor (the last apicomplexan adaptation to parasitism. bolic pathways that are critical for free-living common ancestor of chromerids and apicom- organisms were lost as apicomplexan para- plexans) encoded functionally linked proteins The Apicomplexa, a group that includes sites evolved towards an intracellular lifestyle. that have been utilized differently by free-living pathogens such as Plasmodium falciparum By contrast, Woo et al. noted that specific and parasitic lineages. The authors noted that and Toxoplasma gondii, share common ances- genes were gained as Plasmodium spp. and the proto-apicomplexan ancestor possessed try with algae. Now, two studies1,2 compare Toxoplasma spp. diverged from common all known flagellar components — which are apicomplexan genomes and transcriptomes ancestors; in these species, the number of genes essential for motility of the free-living species with those of closely related free-living algae to encoding exported proteins has increased sig- — whereas these components were progres- explore the genomic changes that underpinned nificantly, suggesting that these genes might sively lost as individual apicomplexan lineages the transition of apicomplexans to parasitism. have emerged in the context of host–parasite differentiated, possibly owing to their adap- Chromerids are a recently discovered group interactions. tation to a parasitic lifestyle. However, this is of algae that can be maintained in the labora- Notably, both studies found that many api- not the case for all flagellar components; for tory as free-living photoautotrophs. They were complexan genes previously linked to parasit- example, the striated fibre assemblin (SFA) first reported in 2008, when Chromera velia ism were also present in chromerids, and that protein has been conserved in all apicomplexan was shown to be more closely related to api- chromerid genomes encode many proteins genomes. SFA was present in one of the co- complexans than any other known organism; that contain functional domains implicated in expression modules in C. velia that overlapped and, more recently, Vitrella brassicaformis was molecular processes of apicomplexan parasites. significantly with P. falciparum; the module the second chromerid to be characterized. In To investigate whether there are conserved also included many invasion-associated genes, contrast to the photosynthetic chromerids, gene expression modules between chromer- including genes encoding a rhoptry protein, colpodellids are predatory protists that are also ids and apicomplexans, Woo et al. measured apical sushi protein and two gliding motility close relatives of the Apicomplexa. changes in gene expression in C. velia cultured components. This finding, along with previ- Using Illumina sequencing, Janouškovec under different combinations of temperature, ous ultrastructural studies, has provided strong et al.1 analysed the transcriptomes of the two iron and salt. These data were then compared evidence to support the hypothesis that the known chromerid species and of three col- with publicly available transcriptome data apical complex invasion machinery, which is podellids species, and used a concatenated for P. falciparum that had been subjected to a key feature of Apicomplexa, originated from alignment of 85 predicted protein sequences growth perturbations. More than 80 homolo- the flagellar apparatus of a previous ancestor. to create a phylogenetic tree with these 5 spe- gous genes annotated as being implicated In summary, these two studies elucidate cies and 35 apicomplexans. The authors found in invasion showed statistically significant the origins of parasitism in Apicomplexa and that chromerids and colpodellids formed a sis- co-expression across different conditions in provide an elegant example of the flexibility ter clade to Apicomplexa, which is consistent both species, suggest- of evolution, suggesting that the repurposing with a similar, independently constructed ing that the genome and refinement of genes gave rise to a novel phylogeny by Woo et al.2, who analysed function in these organisms. 101 single-copy genes across 26 apicom- Christian K. Owusu and Hayley M. Bennett are at the plexan, chromerid and outgroup species. Sanger Institute, Wellcome Trust Genome Campus, Genomic comparison also elucidated Hinxton, Cambridge CB10 1SA, UK. e‑mail: [email protected] the role that gene loss and gain had in the doi:10.1038/nrmicro3551 evolution of the Apicomplexa. For exam- 1. Janouškovec, J. et al. Factors mediating plastid ple, both studies found that the transi- dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl tion from a free-living to parasitic Acad. Sci. USA 112, 10200–10207 (2015). lifestyle was predominantly charac- 2. Woo, Y. H. et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate terized by gene loss, particularly of intracellular parasites. eLife 4, e06974 (2015). genes associated with metabolic func- Competing interests statement The authors declare no competing interests. tion — such as photosynthesis and NPG