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Marine gregarine genomes illuminate current understanding of apicomplexan glideosome

Apicomplexans, parasite protists of a very wide diversity of metazoan hosts, are mostly known from species infecting human. Absence or limited data for basal lineages prevents a comprehensive view of evolutionary history and adaptive capacities of Apicomplexa. Here, we characterized the genome of the marine eugregarine Porospora gigantea, remarkable for the gigantic size of its vegetative feeding forms (trophozoites) and their speed of gliding movement, the fastest so far recorded for an Apicomplexa. Not a single but two highly related genomes named A and B were assembled. Highly syntenic, of similar size (9 Mb) and coding capacities (∼5300 genes), they display a 10.8% divergence at nucleotide level corresponding to 16-38 My divergent time. Orthogroups analyses across 25 (proto)Apicomplexa including Gregarina niphandrodes showed that A and B are highly divergent from all other known apicomplexan species, revealing an unexpected diversity. These two related species branch in phylogenetic studies at the base of Cephaloidophoroidea, forming a new family in these crustacean gregarines. Gliding proteins data mining found a strong conservation of actin-related proteins, as well as of regulatory factors, within apicomplexan. In contrast, the conservation of core glideosome proteins and adhesion proteins appears to be highly variable among apicomplexan lineages, especially in gregarines. These results confirm the importance of studying gregarines to widen our biological and evolutionary view of apicomplexan parasites, to better apprehend species diversity and revise our understanding of the molecular bases of some key functions such as observed for the glideosome.