Evolutionary genomics of metchnikovella incurvata (metchnikovellidae): An early branching microsporidium

Abstract

Metchnikovellids are highly specialized hyperparasites, which infect and reproduce inside gregarines (Apicomplexa) inhabiting marine invertebrates. Their phylogenetic affiliation was under constant discussion until recently, when analysis of the first near-complete metchnikovellid genome, that of Amphiamblys sp., placed it in a basal position with respect to most Microsporidia. Microsporidia are a highly diversified lineage of extremely reduced parasites related to Rozellida (RozellosporidiaRozellomycotaCryptomycota) within the Holomycota clade of Opisthokonta. By sequencing DNA froma single-isolated infected gregarine cellwe obtained an almost complete genome of a secondmetchnikovellid species, and the first one of a taxonomically described and well-documented species, Metchnikovella incurvata. Our phylogenomic analyses show that, despite being considerably divergent from each other, M. Incurvata forms a monophyletic group with Amphiamplys sp., and confirmthatmetchnikovellids are one of the deep branches ofMicrosporidia. Comparative genomic analysis demonstrates that, like most Microsporidia, metchnikovellids lack mitochondrial genes involved in energy transduction and are thus incapable of synthesizing their own ATP viamitochondrial oxidative phosphorylation. They also lack the horizontally acquired ATP transporters widespread in most Microsporidia. We hypothesize that a family of mitochondrial carrier proteins evolved to transportATP fromthe host into themetchnikovellid cell.We observe the progressive reduction of genes involved inDNArepair pathways along the evolutionary path ofMicrosporidia,whichmight explain, at least partly, the extremely high evolutionary rate of themost derived species.Our data also suggest that genome reduction and acquisition of novel genes co-occurred during the adaptation of Microsporidia to their hosts.