Hyperosmotic shock induces the sigma32 and sigmaE stress regulons of Escherichia coli

Mol Microbiol. 1999 Dec;34(5):1029-38. doi: 10.1046/j.1365-2958.1999.01664.x.

Abstract

The rise in the levels of sigmaS that accompanies hyperosmotic shock plays an important role in Escherichia coli survival by increasing the transcription of genes involved in the synthesis and transport of osmoprotectants. To determine if other stress regulons collaborate with sigmaS in dealing with high osmolality, we used single copy fusions of lacZ to representative promoters induced by protein misfolding in the cytoplasm (dnaK and ibp ), extracytoplasmic stress [P3rpoH and htrA(degP )] and cold shock (cspA). Both the sigma32-dependent, dnaK and ibp, promoters, and the sigmaE-dependent, P3rpoH and htrA, promoters were rapidly but transiently induced when mid-exponential phase cells were treated with 0.464 M sucrose. The cspA promoter, however, did not respond to the same treatment. Overproduction of the cytoplasmic domain of the sigmaE anti-sigma factor, RseA, reduced the magnitude of osmotic induction in lambdaphi(P3rpoH:lacZ ) lysogens, but had no effect on the activation of the dnaK and ibp promoters. Similarly, induction of the dnaK:lacZ and ibp:lacZ fusions was not altered in either rpoS or ompR genetic backgrounds. Osmotic upshift led to a twofold increase in the enzymatic activity of the lambdaTLF247 rpoH:lacZ translational fusion whether or not the cells were treated with rifampicin, indicating that both heat shock and exposure to high osmolality trigger a transient increase in rpoH translation. Our results suggest that the sigma32, sigmaE and sigmaS regulons closely co-operate in the managment of hyperosmotic stress. Induction of the sigma32 and sigmaE regulons appears to be an emergency response required to repair protein misfolding and facilitate the proper folding of proteins that are rapidly synthesized following loss of turgor, while providing a mechanism to increase the activity of sigmaS, the primary stress factor in osmoadaptation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacterial Outer Membrane Proteins / genetics
  • Bacterial Outer Membrane Proteins / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / physiology*
  • Escherichia coli Proteins*
  • Gene Expression Regulation, Bacterial*
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / metabolism
  • Heat-Shock Proteins / genetics*
  • Heat-Shock Proteins / metabolism
  • Heat-Shock Response
  • Lac Operon / genetics
  • Multienzyme Complexes*
  • Osmolar Concentration
  • Osmotic Pressure
  • Promoter Regions, Genetic
  • Protein Biosynthesis
  • Regulon / genetics*
  • Sigma Factor / genetics*
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription, Genetic

Substances

  • Bacterial Outer Membrane Proteins
  • Escherichia coli Proteins
  • HSP70 Heat-Shock Proteins
  • Heat-Shock Proteins
  • Multienzyme Complexes
  • Sigma Factor
  • Transcription Factors
  • heat-shock sigma factor 32
  • sporulation-specific sigma factors
  • envZ protein, E coli
  • dnaK protein, E coli