Abstract
The Microsporidia are a major group of intracellular fungi and important parasites of animals including insects, fish, and immunocompromised humans. Microsporidian genomes have undergone extreme reductive evolution but there are major differences in genome size and structure within the group: some are prokaryote-like in size and organisation (<3 Mb of gene-dense sequence) while others have more typically eukaryotic genome architectures. To gain fine-scale, population-level insight into the evolutionary dynamics of these tiny eukaryotic genomes, we performed the broadest microsporidian population genomic study to date, sequencing geographically isolated strains of Spraguea, a marine microsporidian infecting goosefish worldwide. Our analysis revealed that population structure across the Atlantic Ocean is associated with a conserved difference in ploidy, with American and Canadian isolates sharing an ancestral whole genome duplication that was followed by widespread pseudogenisation and sorting-out of paralogue pairs. While past analyses have suggested de novo gene formation of microsporidian-specific genes, we found evidence for the origin of new genes from noncoding sequence since the divergence of these populations. Some of these genes experience selective constraint, suggesting the evolution of new functions and local host adaptation. Combining our data with published microsporidian genomes, we show that nucleotide composition across the phylum is shaped by a mutational bias favoring A and T nucleotides, which is opposed by an evolutionary force favoring an increase in genomic GC content. This study reveals ongoing dramatic reorganization of genome structure and the evolution of new gene functions in modern microsporidians despite extensive genomic streamlining in their common ancestor.
Highlights
The Microsporidia are a major group of obligate endoparasitic fungi (Vavra and Lukes 2013) that cause economically important diseases of fish, edible crustacea (Kent et al 1989; Campbell et al 2013; Stentiford et al 2013) and insects (Cornman et al 2009; Pan et al 2013), and serious opportunistic infections in immunocompromised humans (Hollister et al 1996; Didier and Weiss 2011)
The $1,800 protein-coding genes on the E. intestinalis genome are separated by highly reduced intergenic regions that have almost entirely lost promoters and regulatory elements; transcription of neighboring genes is often overlapping, suggesting that these motifs have moved within coding sequences in many cases (Williams et al 2005)
We find that the putative promoter regions of Spraguea genes, which we define as the 22 bp upstream motif described above, are significantly (v2 1⁄4 950.7, P 1⁄4 9.17 Â 10À209) conserved relative to the background intergenic level; this suggests that the regions immediately upstream of microsporidian coding sequences are enriched for functionally important regulatory elements, and is consistent with the idea that the “CCC” motif forms part of a core microsporidian promoter (Peyretaillade et al 2009; Heinz et al 2012)
Summary
The Microsporidia are a major group of obligate endoparasitic fungi (Vavra and Lukes 2013) that cause economically important diseases of fish, edible crustacea (Kent et al 1989; Campbell et al 2013; Stentiford et al 2013) and insects (Cornman et al 2009; Pan et al 2013), and serious opportunistic infections in immunocompromised humans (Hollister et al 1996; Didier and Weiss 2011). At 2.25 Mb, the microsporidian Encephalitozoon intestinalis has the smallest endoparasitic nuclear genome reported to date (Corradi et al 2010). This reduction has been driven by host dependency and the loss of metabolic pathways associated with a free-living lifestyle, and by a drastic compaction of classical eukaryotic genome architecture.
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