DNA twist as a transcriptional sensor for environmental changes

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Abstract
A variety of reports describe shifts in the environment which cause a corresponding change in the measured linking number of plasmid DNA isolated from bacterial cells. This change in linking number is often attributed to a change in superhelical density. This, coupled with the observation that transcription is often dependent upon the superhelical density of the DNA template seen in vitro, has led to the suggestion that superhelical density may control expression of certain genes. However, since many environmental changes could, in principle, influence DNA twist itself, then the measured differences in linking number, δLk, may simply be a consequence of variation in twist according to the relationship δLk=δTw+δWr, where δTw and δWr are changes in twist and writhe, respectively. In fact, we show that when an environmental change causes a change in the helical pitch of the DNA, and if the superhelical density of DNA is regulated to remain constant according to the homeostatic model of Menzel and Gellert, then δLkδTw. We have found that there are a number of published reports describing variation in promoter activity as a function of linking number that can be explained by considering twist. We suggest that there are classes of σ70 promoters whose ability to be recognized by RNA polymerase is exquisitely sensitive to the relative orientation of the -35 and -10 regions, and environmental conditions can control this relative orientation by changing DNA twist. The recA and proU promoters which are activated by cold shock and osmotic shock, respectively, behave as if they are twist-sensitive promoters. Consideration of DNA twist can also account for the change in activity of a number of other promoters when they are placed in bacterial strains defective in either DNA gyrase or topoisomerase.