Variation in Genome Architecture and Epigenetic Modification Across the Microsporidia Phylogeny

Microsporidia are a model clade for studying intracellular parasitism, being well-known for their streamlined genomes and their extreme life history. Although microsporidia are highly diverse and ecologically important to a broad range of hosts, previous research on genome architecture has focused primarily on the mammal-infecting genus Encephalitozoon. Here, we expand that work, testing the universality of the patterns observed in Encephalitozoon by investigating and comparing variation in genetic and epigenetic architectures in the high-quality genome assemblies of several major microsporidia clades. Our comparison of nine genomes, including the first genome assemblies of Binucleata daphniae, Gurleya vavrai, and Conglomerata obtusa, and revised, improved assemblies of Glugoides intestinalis, Mitosporidium daphniae, and Ordospora colligata, found limited conservation of genetic and epigenetic architecture across all microsporidia, although many genomic characteristics, such as nucleotide composition and repeat content, were shared between genomes of the same or related clades. For example, rRNA genes were hypermethylated in most species, but their position close to chromosome ends was only found in the Encephalitozoon and its sister clade. GC-content varied widely, linked to genome size, phylogenetic position, and activity of repeat elements. These findings enhance our insight into genome evolution and, consistent with findings from other systems, suggest epigenetic modification as a regulatory mechanism of gene expression and repeat element activity in microsporidia. Our comparative genome analysis reveals high variation in genetic and epigenetic architecture among microsporidia, despite all of them adapting to a parasitic lifestyle within host cells.