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Genome rearrangement by replication-directed translocation
Elisabeth R.M. Tillier & Richard A. Collins
Gene order in bacteria is poorly conserved during evolution1–3. For example, although many homologous genes are shared by the proteobacteria Escherichia coli, Haemophilus influenzae and Helicobacter pylori, their relativepositions are very different in each genome, except local functional clusters such as operons3–6. The complete sequences of the more closely related bacterial genomes, such as pairs of Chlamydia7–9, H. pylori10,11 and Mycobacterium species12, now allow identification of the processes and mechanisms involved in genome evolution. Here we provide evidence that a substantial proportion of rearrangements ingene order results from recombination sites that are determined by the positions of the replication forks. Our observations suggest that replication has a major role in directing genome evolution.

tion in both genomes, as indicated by their lying on a diagonal line with a slope of approximately 1 (Fig. 1b, filled squares). The 274 genes that are located in a different relative position compriseat least 22 distinct clusters, and are not randomly distributed throughout the genome. Instead, the genes that have moved form a perpendicular diagonal line with a slope of –1 (Fig. 1b, open circles) that intersects the first line at approximately the position of the termination of replication. A similar pattern has been noted independently in a comparison of C. pneumonia AR39 and C. trachomatisMoPn (ref. 9). This pattern indicates that almost all of the non-collinear genes have been inverted and translocated to the ‘opposite side’ of the genome: a mirror-image position across an axis defined by the putative origin and termination of replication (the ‘replication axis’; Fig. 2). We also found this pattern of gene translocation for 6 clusters We determined plots for the relative positionsof unique orthologous pairs of genes in pairwise comparisons of bacterial genomes containing 147 of 1,145 orthologues identified in the H. pylori (Fig. 1). Comparison of H. pylori 26696 with Campylobacter strains 26695 and J99 (Fig. 1c). An analysis of homologous jejuni13 (Fig. 1a) showed a high degree of rearrangement of the sequences in the Mycobacterium tuberculosis genome and the order of 748identified orthologues. In contrast, a plot of the rela- recently completed, but not yet annotated, Mycobacterium leprae tive positions of 732 pairs of orthologues in Chlamydia pneumo- sequence revealed that the gene order in the two Mycobacterium nia CWL029 and Chlamydia trachomatis serovar D showed that genomes is substantially more rearranged than that in the Chlamymost (458) are located at thesame relative position and orienta- dia or Helicobacter genomes (Fig. 1d). Even with approximately 35% difference in genome length, however, the pattern of perpendicular diagoa b nals is still apparent, indicating that many of the gene-order differences involve exchange across the replication axis. At the scale of the whole genome, the translocation of genes across the replication axis appears to bequite symmetrical, forming almost straight lines (Fig. 1b–d). We found three instances in Chlamydia (Fig. 3a) and one in Helicobacter (data not shown) of a block of genes from one side of the genome exchanging with a block from the other side, consistent with two c d reciprocal recombination events, either simultaneous or consecutive. A closer examination of the genome rearrangements revealedthat only a few are this straightforward (Figs 2 and 3a). Many cases appear to result from a series of recombination events with slightly asymmetrical breakpoints. We diagrammed the arrangement of the regions of the genome flanked by xerD and htrB, and by hflX and ycbF (Fig. 3b). Although these two blocks of genes Fig. 1 Plots of the position of genes in related genomes. The x and y axes represent...
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