Host shifting and novel genome features of the microbial pathogen Nosema

Abstract

Nosema is a diverse fungal genus of unicellular, obligate symbionts of insects and other arthropods. We conducted a comparative genomic analysis of N. muscidifuracis, a Nosema species infecting parasitoid wasp genus Muscidifurax, along with six other genome-sequenced species found in bees, wasps, moths, butterflies, and amphipods. Phylogenomic analyses revealed incongruency in the Nosema and host species trees, suggesting a host switch event between wasps and bees. In contrast to an outgroup species Encephalitozoon cuniculi (GC-content 47.5%), Nosema genomes are much lower in GC-content (24.8%~34.8%), indicating an evolutionary tendency toward highly AT-rich genomes. A sequence motif containing at least three consecutive Cs was significantly enriched immediately upstream of start codons in all seven Nosema genomes. Interestingly, this motif is present in ~90% of highly expressed genes, compared to ~20% in lowly expressed genes N. muscidifuracis, which may function as a cis-regulatory element for controlling and regulating gene expression. Telomeric prediction identified TTAGG as the telomeric repeat unit in Encephalitozoon and N. ceranae, which is the ancestral form. In N. muscidifuracis, novel composite telomere repeats were discovered, suggesting diverse telomeric motifs in Nosema. As an intracellular parasite, there is significant reduction of the N. muscidifuracis genome, with ~47% of genes compared to the free-living yeast genome. Not all pathways are equally affected: genes related to oxidative phosphorylation and mitochondrial function are entirely absent, and the genes associated with endocytosis are significantly diminished compared to other pathways. Our study significantly advanced the understanding of the genetic architecture, gene regulation, and evolution of Nosema.