Patterns of genome evolution among the microsporidian parasites Encephalitozoon cuniculi, Antonospora locustae and Enterocytozoon bieneusi

Abstract

Background: Microsporidia are intracellular parasites that are highly-derived relatives of fungi. They have compacted genomes and, despite a high rate of sequence evolution, distantly related species can share high levels of gene order conservation. To date, only two species have been analysed in detail, and data from one of these largely consists of short genomic fragments. It is therefore difficult to determine how conservation has been maintained through microsporidian evolution, and impossible to identify whether certain regions are more prone to genomic stasis.

Principal findings: Here, we analyse three large fragments of the Enterocytozoon bieneusi genome (in total 429 kbp), a species of medical significance. A total of 296 ORFs were identified, annotated and their context compared with Encephalitozoon cuniculi and Antonospora locustae. Overall, a high degree of conservation was found between all three species, and interestingly the level of conservation was similar in all three pairwise comparisons, despite the fact that A. locustae is more distantly related to E. cuniculi and E. bieneusi than either are to each other.

Conclusions/significance: Any two genes that are found together in any pair of genomes are more likely to be conserved in the third genome as well, suggesting that a core of genes tends to be conserved across the entire group. The mechanisms of rearrangments identified among microsporidian genomes were consistent with a very slow evolution of their architecture, as opposed to the very rapid sequence evolution reported for these parasites.

Figure 1. Percentage of gene order conservation between E. bieneusi and E. cuniculi.

Each category displays the percentage of gene pairs in E. bieneusi that are adjacent, close neighbours, or nonsyntenic in E. cuniculi.

Figure 2. Analysis of contigs included in the scaffold SC_2384 and gene order comparisons between the E. bieneusi (A) and E. cuniculi (B) orthologues.

Coloured boxes represent orthologues in the same context in both genomes, and the chromosome on which each E. cuniculi segment is located is indicated by Roman numerals. Grey boxes represent genes that are not identifiably orthologous or are not conserved in context. Regions of both genomes transposed above or below the aligned regions represent blocks of genes in different contexts. The chromosomal location of the E. cuniculi orthologue of such genes from E. bieneusi is indicated by Arabic numerals above the boxes. The chromosomal location of syntenic ORFs in the genome of E. cuniculi is shown in the lower part of the figure and annotated with Roman numbers. Straight lines join the homologous ORFs. Red triangles represent boundaries between the contigs used to generate the scaffolds presented in these figures.

Figure 3. Analysis of contigs included in the scaffold SC_2496 and gene order comparisons between the E. bieneusi (A) and E. cuniculi (B) orthologues.

Figure 4. Analysis of contigs included in the scaffold SC_1888 and gene order comparisons between the E. bieneusi (A) and E. cuniculi (B) orthologues.

Figure 5. Schematic representation of phylogenetic relationships among microsporidian genera based on SSU rDNA sequences using Maximum Likelihood and genetic distances (Neighbor-Joining) ,

Colored boxes linking pairs of taxa indicate the percentage of conservation of adjacent pairs of genes. Blue boxes indicate the percentage of adjacent loci that are also adjacent in the third microsporidian species analysed in this study.