Density of σ70 promoter-like sites in the intergenic regions dictates the redistribution of RNA polymerase during osmotic stress in Escherichia coli

Nucleic Acids Res. 2019 May 7;47(8):3970-3985. doi: 10.1093/nar/gkz159.

Abstract

RNA polymerase (RNAP), the transcription machinery, shows dynamic binding across the genomic DNA under different growth conditions. The genomic features that selectively redistribute the limited RNAP molecules to dictate genome-wide transcription in response to environmental cues remain largely unknown. We chose the bacterial osmotic stress response model to determine genomic features that direct genome-wide redistribution of RNAP during the stress. Genomic mapping of RNAP and transcriptome profiles corresponding to the different temporal states after salt shock were determined. We found rapid redistribution of RNAP across the genome, primarily at σ70 promoters. Three subsets of genes exhibiting differential salt sensitivities were identified. Sequence analysis using an information-theory based σ70 model indicates that the intergenic regions of salt-responsive genes are enriched with a higher density of σ70 promoter-like sites than those of salt-sensitive genes. In addition, the density of promoter-like sites has a positive linear correlation with RNAP binding at different salt concentrations. The RNAP binding contributed by the non-initiating promoter-like sites is important for gene transcription at high salt concentration. Our study demonstrates that hyperdensity of σ70 promoter-like sites in the intergenic regions of salt-responsive genes drives the RNAP redistribution for reprograming the transcriptome to counter osmotic stress.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Culture Media / chemistry
  • Culture Media / pharmacology
  • DNA, Bacterial / genetics*
  • DNA, Bacterial / metabolism
  • DNA, Intergenic / genetics*
  • DNA, Intergenic / metabolism
  • DNA-Directed RNA Polymerases / genetics*
  • DNA-Directed RNA Polymerases / metabolism
  • Escherichia coli / drug effects*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Gene Expression Regulation, Bacterial*
  • Information Theory
  • Models, Genetic
  • Osmotic Pressure
  • Potassium Chloride / pharmacology*
  • Promoter Regions, Genetic
  • Salinity
  • Sigma Factor / genetics*
  • Sigma Factor / metabolism
  • Transcription, Genetic

Substances

  • Culture Media
  • DNA, Bacterial
  • DNA, Intergenic
  • Sigma Factor
  • Potassium Chloride
  • RNA polymerase sigma 70
  • DNA-Directed RNA Polymerases