Abstract
Recent studies strongly suggest that in bacteria, both the genomic pattern of DNA thermodynamic stability and the order of genes along the chromosomal origin-to-terminus axis are highly conserved and that this spatial organization plays a crucial role in coordinating genomic transcription. In this article, we explore the relationship between genomic sequence organization and transcription in the commensal bacterium Escherichia coli and the plant pathogen Dickeya. We argue that, while in E. coli the gradient of DNA thermodynamic stability and gene order along the origin-to-terminus axis represent major organizational features orchestrating temporal gene expression, the genomic sequence organization of Dickeya is more complex, demonstrating extended chromosomal domains of thermodynamically distinct DNA sequences eliciting specific transcriptional responses to various kinds of stress encountered during pathogenic growth. This feature of the Dickeya genome is likely an adaptation to the pathogenic lifestyle utilizing differences in genomic sequence organization for the selective expression of virulence traits. We propose that the coupling of DNA thermodynamic stability and genetic function provides a common organizational principle for the coordinated expression of genes during both normal and pathogenic bacterial growth.
Highlights
Coordination of the bacterial chromosome structure and function is mediated by changes in genomic DNA supercoiling associated with DNA replication and its cessation and corresponding alterations of transcription
Positional effects on reporter gene expression were observed in Escherichia coli [7,8,9], consistent with the notion that genetic expression is regulated in digital mode—that is, by classical transcription factor (TF)–target gene (TG) interactions—and is subject to the analog mode of control, mediated by cell physiology-dependent changes of chromosomal DNA supercoiling [4,10,11,12,13,14,15]
The highly reproducible expression patterns of the CODOs observed under conditions of applied environmental stress or modulation of DNA topology by topoisomerase inhibitors and/or poisons suggest that functionally linked genes including virulence genes [23,24,80] are co-transcribed within a variable chromosomal context, which is beyond the detection capacity of the approaches examining the comparative fitness of individual mutants
Summary
Coordination of the bacterial chromosome structure and function is mediated by changes in genomic DNA supercoiling associated with DNA replication and its cessation and corresponding alterations of transcription. This superimposition of the gradients of DNA thermodynamic stability and supercoiling on a conserved chromosomal gene order with anabolic and catabolic functions, allocated respectively to the OriC and the Ter ends, provides a bona fide device for the spatiotemporal coordination of genomic expression during the E. coli growth cycle [73].
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