Silencing of DNase Colicin E8 Gene Expression by a Complex Nucleoprotein Assembly Ensures Timely Colicin Induction

PLoS Genet. 2015 Jun 26;11(6):e1005354. doi: 10.1371/journal.pgen.1005354. eCollection 2015 Jun.

Abstract

Colicins are plasmid-encoded narrow spectrum antibiotics that are synthesized by strains of Escherichia coli and govern intraspecies competition. In a previous report, we demonstrated that the global transcriptional factor IscR, co dependently with the master regulator of the DNA damage response, LexA, delays induction of the pore forming colicin genes after SOS induction. Here we show that IscR is not involved in the regulation of nuclease colicins, but that the AsnC protein is. We report that AsnC, in concert with LexA, is the key controller of the temporal induction of the DNA degrading colicin E8 gene (cea8), after DNA damage. We demonstrate that a large AsnC nucleosome-like structure, in conjunction with two LexA molecules, prevent cea8 transcription initiation and that AsnC binding activity is directly modulated by L asparagine. We show that L-asparagine is an environmental factor that has a marked impact on cea8 promoter regulation. Our results show that AsnC also modulates the expression of several other DNase and RNase colicin genes but does not substantially affect pore-forming colicin K gene expression. We propose that selection pressure has "chosen" highly conserved regulators to control colicin expression in E. coli strains, enabling similar colicin gene silencing among bacteria upon exchange of colicinogenic plasmids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Asparagine / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Colicins / genetics*
  • Colicins / metabolism
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / genetics*
  • Escherichia coli Proteins / metabolism
  • Gene Expression Regulation, Bacterial*
  • Nucleoproteins / genetics
  • Nucleoproteins / metabolism
  • Promoter Regions, Genetic
  • SOS Response, Genetics
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism
  • Trans-Activators / genetics*
  • Trans-Activators / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • AsnC protein, E coli
  • Bacterial Proteins
  • Colicins
  • Escherichia coli Proteins
  • IscR protein, E coli
  • LexA protein, Bacteria
  • Nucleoproteins
  • Trans-Activators
  • Transcription Factors
  • immE8 protein, E coli
  • Asparagine
  • Serine Endopeptidases