Plasmodium vinckei genomes provide insights into the pan-genome and evolution of rodent malaria parasites

Background Rodent malaria parasites (RMPs) serve as tractable tools to study malaria parasite biology and host-parasite-vector interactions. Plasmodium vinckei is the most geographically widespread of the four RMP species with isolates collected in five countries in sub-Saharan Central Africa between 1940s and 1970s. Several P. vinckei isolates are available but are relatively less characterized compared to other RMPs thus hampering its exploitation as rodent malaria models. We have generated a comprehensive resource for P. vinckei comprising of high-quality reference genomes, genotypes, gene expression profiles and growth phenotypes for ten P. vinckei isolates. This also allows for a comprehensive pan-genome analysis of the reference-quality genomes of RMPs. Results Plasmodium vinckei isolates display a large degree of phenotypic and genotypic diversity and potentially constitute a valuable resource to study parasite virulence and immunogenicity. The P. vinckei subspecies have diverged widely from their common ancestor and have undergone genomic structural variations. The subspecies from Katanga, P. v. vinckei, is unique among the P. vinckei isolates with a smaller genome size and a reduced multigene family repertoire. P. v. vinckei infections provide good schizont yields and is amenable to genetic manipulation, making it an ideal vinckei group parasite for reverse genetics. Comparing P. vinckei genotypes reveal region-specific selection pressures particularly on genes involved in mosquito transmission. RMP multigene family expansions observed in P. chabaudi and P. vinckei have occurred in their common ancestor prior to speciation. The erythrocyte membrane antigen 1 (ema1) and fam-c families have considerably expanded among the lowland forests-dwelling P. vinckei parasites with, however, most of the ema1 genes pseudogenised. Genetic crosses can be established in P. vinckei but are limited at present by low transmission success under the experimental conditions tested in this study. Conclusions We observe significant diversity among P. vinckei isolates making them particularly useful for the identification of genotype-phenotype relationships. Inclusion of P. vinckei genomes provide new insights into the evolution of RMPs and their multigene families. Plasmodium vinckei parasites are amenable to experimental genetic crosses and genetic manipulation, making them suitable for classical and functional genetics to study Plasmodium biology.