Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase

J Mol Biol. 2000 Jul 7;300(2):291-305. doi: 10.1006/jmbi.2000.3848.

Abstract

The two-component system is a signal communication network generally consisting of a sensor kinase that receives inputs from the environment and modifies the phosphorylated state of a response regulator that executes an adaptive behavior. PhoP is a response regulator that controls virulence gene expression in Salmonella enterica. Transcription of PhoP-regulated genes is modulated by the Mg(2+) levels detected by the sensor PhoQ. Here, we describe a PhoP mutant protein, PhoP*, that functions in the absence of its cognate sensor, thereby allowing transcription of PhoP-activated genes independently of the Mg(2+ )concentration in the environment. The PhoP* protein harbors a S93N substitution in the response regulator receiver domain. PhoP*-mediated transcription is abolished by either mutation of the aspartate residue that is conserved among response regulators as the site of phosphorylation or inactivation of the pta-encoded phosphotransacetylase. This enzyme mediates the production of acetyl phosphate, which has been shown to serve as a low molecular mass phosphate donor for certain response regulators. The purified PhoP* protein autophosphorylated from acetyl phosphate more efficiently than the wild-type PhoP protein in vitro. The PhoP* protein retained the capacity to interact with the PhoQ protein, which promoted phosphorylation of the PhoP* protein in vitro and abolished PhoP*-mediated transcription under high Mg(2+ )concentrations in vivo. Cumulatively, our results uncover a role of PhoQ in transcriptional repression during growth in millimolar Mg(2+ )and define a mutant response regulator form with an increased capacity to be phosphorylated by acetyl phosphate.

Publication types

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

MeSH terms

  • Alleles
  • Amino Acid Substitution / genetics
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Environment
  • Gene Expression Regulation, Bacterial / drug effects*
  • Genes, Bacterial / genetics
  • Genes, Regulator / genetics
  • Magnesium / pharmacology
  • Membrane Proteins / chemistry
  • Methyl-Accepting Chemotaxis Proteins
  • Models, Molecular
  • Mutation / genetics*
  • Operon / genetics
  • Organophosphates / pharmacology*
  • Phosphorylation
  • Protein Binding
  • Protein Biosynthesis / drug effects
  • Protein Structure, Tertiary
  • Recombinant Fusion Proteins
  • Salmonella enterica / drug effects
  • Salmonella enterica / enzymology
  • Salmonella enterica / genetics*
  • Salmonella enterica / growth & development
  • Trans-Activators / chemistry
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription, Genetic / drug effects

Substances

  • Bacterial Proteins
  • Membrane Proteins
  • Methyl-Accepting Chemotaxis Proteins
  • Organophosphates
  • PhoQ protein, Bacteria
  • Recombinant Fusion Proteins
  • Trans-Activators
  • PhoP protein, Bacteria
  • acetyl phosphate
  • Magnesium