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Background  Changes in transcriptional orientation (“CTOs”) occur frequently in prokaryotic genomes. Such changes usually result from genomic inversions, which may cause a conflict between the directions of replication and transcription and an increase in mutation rate. However, CTOs do not always lead to the replication-transcription confrontation. Furthermore, CTOs may cause deleterious disruptions of operon structure and/or gene regulations. The currently existing CTOs may indicate relaxation of selection pressure. Therefore, it is of interest to investigate whether CTOs have an independent effect on the evolutionary rates of the affected genes, and whether these genes are subject to any type of selection pressure in prokaryotes.    Methods  Three closely related enterbacteria,  Escherichia coli ,  Klebsiella pneumoniae  and  Salmonella enterica serovar Typhimurium , were selected for comparisons of synonymous ( dS ) and nonsynonymous ( dN ) substitution rate between the genes that have experienced changes in transcriptional orientation (changed-orientation genes, “COGs”) and those that do not (same-orientation genes, “SOGs”). The  dN / dS  ratio was also derived to evaluate the selection pressure on the analyzed genes. Confounding factors in the estimation of evolutionary rates, such as gene essentiality, gene expression level, replication-transcription confrontation, and decreased  dS  at gene terminals were controlled in the COG-SOG comparisons.    Results  We demonstrate that COGs have significantly higher  dN  and  dS  than SOGs when a series of confounding factors are controlled. However, the  dN / dS  ratios are similar between the two gene groups, suggesting that the increase in  dS  can sufficiently explain the increase in  dN  in COGs. Therefore, the increases in evolutionary rates in COGs may be mainly mutation-driven.    Conclusions  Here we show that CTOs can increase the evolutionary rates of the affected genes. This effect is independent of the replication-transcription confrontation, which is suggested to be the major cause of inversion-associated evolutionary rate increases. The real cause of such evolutionary rate increases remains unclear but is worth further explorations.

Changes in transcriptional orientation are associated with increases in evolutionary rates of enterobacterial genes