Genome Compaction and Stability in Microsporidian Intracellular Parasites

Claudio H Slamovits, Naomi M Fast, Joyce S Law, Patrick J Keeling
2004 Current Biology  
Genome Compaction and Stability in Microsporidian Intracellular Parasites probability of fixation of both nucleotide and chromosomal mutations are affected by the same genetic and life-history factor [4-6, 15]. Although this trend is also found in many prokaryotes, deviations from this correlation are also common in bacterial endosymbionts [9][10][11]. University of British Columbia 3529-6270 University Boulevard One eukaryotic group with exceptional genomic characteristics is the group of
more » ... ate intracellular parasites, Vancouver, BC V6T 1Z4 Canada microsporidia. Their genomes are among the most highly reduced in eukaryotes and their genes are among the most rapidly evolving at the sequence level [1-3], yet nothing is known about their genomic plasticity. Given a Summary correlation between sequence evolution and genome plasticity, microsporidia would be predicted to have ex-Microsporidian genomes are extraordinary among euperienced a high rate of genome reshuffling during their karyotes for their extreme reduction: although they evolution. To explore the dynamics of this process in are similar in form to other eukaryotic genomes, they these atypical eukaryotic genomes, we sequenced 729 are typically smaller than many prokaryotic genomes fragments from a random genomic library of A. locustae [1, 2]. At the same time, their rates of sequence evolu-(prepared according to [18, 19]), resulting in 685 Kbp of tion are among the highest for eukaryotic organisms genomic sequence and 183 genes. Of these, 175 show [3]. To explore the effects of compaction on nuclear significant similarity to E. cuniculi homologs, three show genome evolution, we sequenced 685,000 bp of the significant similarity to homologs in other organisms, Antonospora locustae genome (formerly Nosema lobut not E. cuniculi, and four are putative A. locustaecustae) and compared its organization with the respecific genes. As in E. cuniculi, the genome of A. locently completed genome of the human parasite custae is highly compact, with gene density in the gene-Encephalitozoon cuniculi [1, 2]. Despite being very disrich regions of the A. locustae and E. cuniculi genomes tantly related, the genomes of these two microsporibeing 0.94 and 0.97 genes per kilobase, respectively. dian species have retained an unexpected degree of Selecting fragments containing more than one partial or synteny: 13% of genes are in the same context, and complete coding region yielded 44 fragments pos-30% of the genes were separated by a small number of sessing two to six genes, for a total of 122 genes or 94 short rearrangements. Microsporidian genomes are, gene couples (see Table S1 ). The degree of conservation therefore, paradoxically composed of rapidly evolving of gene order between A. locustae and E. cuniculi was sequences harbored within a slowly evolving genome, measured as the percentage of gene couples in A. loalthough these two processes are sometimes considcustae that were also adjacent or close neighbors in ered to be coupled [4-7]. Microsporidian genomes E. cuniculi. Figures 1A and 1B show examples of consershow that eukaryotic genomes (like genes) do not vation in order and direction over several genes. Figures evolve in a clock-like fashion, and genome stability 1C and 1D show two generally conserved regions with may result from compaction in addition to a lack of a few long-range and short-range rearrangements causrecombination, as has been traditionally thought to ing changes in order and orientation (see also Figure occur in bacterial and organelle genomes [8-11]. S1). In over 94 A. locustae gene couples, 13% were also adjacent in E. cuniculi, an additional 17% were close Results and Discussion neighbors in E. cuniculi, and 43% of the A. locustae couples are located on the same chromosome in Eukaryotic genomes are dynamic in their organization, E. cuniculi (Figure 2). Recent data from yeasts [20], such that gene order is typically conserved only among plants [21], nematodes [5], and mammals [22] show that closely related species [12], but the forces that control a high proportion of small inversions are characteristic genome plasticity are poorly understood [13]. Moreover, in eukaryotic genome evolution, whereas the opposite recent comparative genomic studies show that rates of occurs in prokaryotes[23]. We examined the relative origenome structure evolution are variable among major entation of conserved couples in E. cuniculi and A. loanimal lineages [5-7, 14, 15], although deeper, interkingcustae and found that 12 of 27 adjacent or neighbor dom comparisons are underexplored. Examples of gene couples were inverted. Of these, eight arrangements order conservation at deep levels of divergence are could be explained by one inversion and four by two known in a few cases where synteny is maintained either inversions, some involving one or a few genes. This by chance [16] or because the proteins are part of a proportion of small inversions is consistent with the becomplex regulatory pathway [17]. In nuclear genomes havior of other eukaryotic genomes and might reinforce of eukaryotes, rates of genome evolution appear to corthe expectation that the gene order of microsporidia relate with the overall rate of sequence evolution within would be highly scrambled: while long-range rea genome, probably because the occurrence and/or the arrangements alter gross genome structure, small inversions tend to quickly disrupt short-range gene orders [21]. In contrast, however, E. cuniculi and A. locustae
doi:10.1016/j.cub.2004.04.041 pmid:15186746 fatcat:yotkto2byba2bcft4k5b3jzixi