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Highlights d The origin of apicomplexans from algae occurred at least three times independently d Piridium and Platyproteum form distinct lineages of obligate animal parasites d They both retain cryptic plastids that are highly convergent with apicomplexans

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The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to have a single origin. Here, we use single-cell genomics from natural samples combined with phylogenomics to infer the evolutionary origin of the phylum Picozoa, a globally distributed but seemingly rare group of marine microbial heterotrophic eukaryotes. Strikingly, the analysis of 43 single-cell genomes shows that Picozoa belong to Archaeplastida, specifically related to red algae and the phagotrophic rhodelphids. These picozoan genomes support the hypothesis that Picozoa lack a plastid, and further reveal no evidence of an early cryptic endosymbiosis with cyanobacteria. These findings change our understanding of plastid evolution as they either represent the first complete plastid loss in a free-living taxon, or indicate that red algae and rhodelphids obtained their plastids independently of other archaeplastids.

Apicomplexans are a diverse group of globally important parasites, that include pathogens like Plasmodium, the causative agent of malaria. Despite their current obligate parasitic nature, apicomplexans evolved from photosynthetic algae and retain a remnant plastid (chloroplast). Such a complex evolutionary transition was unexpected, but here we show that it occurred at least three times independently. Using single-cell genomics and transcriptomics from 25 diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the loss of photosynthesis and the transition to a morphologically similar parasitic lifestyle, resulting in 30 multiple lineages of highly convergent animal parasites. Main Text:The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis) and Cryptosporidium (cryptosporidiosis)(1). They are united by a complex and distinctive suite of cytoskeletal and secretory structures related to 35 infection called the apical complex, which are used to recognize and gain entry into animal host cells. Apicomplexans are known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic, but houses a number of other essential metabolic pathways(2). The closest relatives of apicomplexans includes a mix of both photosynthetic algae (chromerids) as well as non-photosynthetic microbial predators 40 (colpodellids)(3), and genomic analyses of these free-living relatives have revealed a great deal about how such a dramatic transition may have taken place, as well as how parasitism originates more generally(4). 45