Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli

Mol Microbiol. 2007 Sep;65(6):1518-33. doi: 10.1111/j.1365-2958.2007.05888.x.

Abstract

Amino sugars are essential precursor molecules for the biosynthesis of bacterial cell walls. Their synthesis pathway is initiated by glucosamine-6-phosphate (GlcN-6-P) synthase (GlmS) which catalyses the rate limiting reaction. We report here that expression of the Escherichia coli glmS gene is negatively feedback regulated by its product GlcN-6-P at the post-transcriptional level. Initially, we observed that mutants defective for yhbJ, a gene of the rpoN operon, overproduce GlmS. Concomitantly, a glmS mRNA accumulates that is derived from processing of the primary glmUS transcript at the glmU stop codon by RNase E. A transposon mutagenesis screen in the yhbJ mutant identified the small RNA GlmZ (formerly RyiA or SraJ) to be required for glmS mRNA accumulation. GlmZ, which is normally processed, accumulates in its full-length form in the yhbJ mutant. In the wild type, a decrease of the intracellular GlcN-6-P concentration induces accumulation of the glmS transcript in a GlmZ-dependent manner. Concomitantly, GlmZ accumulates in its unprocessed form. Hence, we conclude that the biological function of GlmZ is to positively control the glmS mRNA in response to GlcN-6-P concentrations and that YhbJ negatively regulates GlmZ. As in yhbJ mutants GlcN-6-P has no effect, YhbJ is essential for sensing this metabolite.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Codon, Terminator / genetics
  • Endoribonucleases / metabolism
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Escherichia coli Proteins / metabolism*
  • Feedback, Physiological*
  • Gene Deletion
  • Gene Expression Regulation, Bacterial
  • Glucosamine / analogs & derivatives
  • Glucosamine / metabolism
  • Glucose-6-Phosphate / analogs & derivatives
  • Glucose-6-Phosphate / metabolism
  • Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing) / metabolism*
  • Host Factor 1 Protein / metabolism
  • Models, Biological
  • Mutation / genetics
  • Operon / genetics
  • RNA Polymerase Sigma 54
  • RNA Processing, Post-Transcriptional
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Nuclear / metabolism*
  • RNA-Binding Proteins
  • Recombinant Fusion Proteins / metabolism
  • Substrate Specificity
  • Up-Regulation / genetics
  • beta-Galactosidase / metabolism

Substances

  • Codon, Terminator
  • Escherichia coli Proteins
  • Hfq protein, E coli
  • Host Factor 1 Protein
  • RNA, Messenger
  • RNA, Small Nuclear
  • RNA-Binding Proteins
  • Recombinant Fusion Proteins
  • YhbJ protein, E coli
  • rpoN protein, E coli
  • glucosamine 6-phosphate
  • Glucose-6-Phosphate
  • Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing)
  • RNA Polymerase Sigma 54
  • Endoribonucleases
  • ribonuclease E
  • beta-Galactosidase
  • Glucosamine