Curli synthesis and biofilm formation in enteric bacteria are controlled by a dynamic small RNA module made up of a pseudoknot assisted by an RNA chaperone

Nucleic Acids Res. 2014 Apr;42(7):4682-96. doi: 10.1093/nar/gku098. Epub 2014 Feb 1.

Abstract

RydC pseudoknot aided by Hfq is a dynamic regulatory module. We report that RydC reduces expression of curli-specific gene D transcription factor required for adhesion and biofilm production in enterobacteria. During curli formation, csgD messenger RNA (mRNA) synthesis increases when endogenous levels of RydC are lacking. In Escherichia coli and Salmonella enterica, stimulation of RydC expression also reduces biofilm formation by impairing curli synthesis. Inducing RydC early on in growth lowers CsgA, -B and -D protein and mRNA levels. RydC's 5'-domain interacts with csgD mRNA translation initiation signals to prevent initiation. Translation inhibition occurs by an antisense mechanism, blocking the translation initiation signals through pairing, and that mechanism is facilitated by Hfq. Although Hfq represses csgD mRNA translation without a small RNA (sRNA), it forms a ternary complex with RydC and facilitates pseudoknot unfolding to interact with the csgD mRNA translation initiation signals. RydC action implies Hfq-assisted unfolding and mRNA rearrangements, but once the pseudoknot is disrupted, Hfq is unnecessary for regulation. RydC is the sixth sRNA that negatively controls CsgD synthesis. Hfq induces structural changes in the mRNA domains targeted by these six sRNAs. What we describe is an ingenious process whereby pseudoknot opening is orchestrated by a chaperone to allow RNA control of gene expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions
  • Bacterial Adhesion
  • Binding Sites
  • Biofilms / growth & development*
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli / physiology
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Gene Expression Regulation, Bacterial*
  • Host Factor 1 Protein / metabolism
  • Nucleic Acid Conformation
  • Peptide Chain Initiation, Translational*
  • RNA, Messenger / chemistry
  • RNA, Messenger / metabolism
  • RNA, Small Untranslated / biosynthesis
  • RNA, Small Untranslated / chemistry
  • RNA, Small Untranslated / metabolism*
  • Salmonella enterica / genetics*
  • Salmonella enterica / metabolism
  • Salmonella enterica / physiology
  • Trans-Activators / genetics
  • Trans-Activators / metabolism

Substances

  • 5' Untranslated Regions
  • CsgB protein, E coli
  • CsgD protein, E coli
  • Escherichia coli Proteins
  • Hfq protein, E coli
  • Host Factor 1 Protein
  • RNA, Messenger
  • RNA, Small Untranslated
  • Trans-Activators
  • csgA protein, E coli