A eukaryotic-like 3' untranslated region in Salmonella enterica hilD mRNA

Nucleic Acids Res. 2014 May;42(9):5894-906. doi: 10.1093/nar/gku222. Epub 2014 Mar 20.

Abstract

Long 3' untranslated regions (3'UTRs) are common in eukaryotic mRNAs. In contrast, long 3'UTRs are rare in bacteria, and have not been characterized in detail. We describe a 3'UTR of 310 nucleotides in hilD mRNA, a transcript that encodes a transcriptional activator of Salmonella enterica pathogenicity island 1 (SPI-1). Deletion of the hilD 3'UTR increases the hilD mRNA level, suggesting that the hilD 3'UTR may play a role in hilD mRNA turnover. Cloning of the hilD 3'UTR downstream of the green fluorescent protein (gfp) gene decreases green fluorescent protein (GFP) activity in both Escherichia coli and S. enterica, indicating that the hilD 3'UTR can act as an independent module. S. enterica mutants lacking either ribonuclease E or polynucleotide phosphorylase contain similar amounts of hilD and hilD Δ3'UTR mRNAs, suggesting that the hilD 3'UTR is a target for hilD mRNA degradation by the degradosome. The hilD 3'UTR is also necessary for modulation of hilD and SPI-1 expression by the RNA chaperone Hfq. Overexpression of SPI-1 in the absence of the hilD 3'UTR retards Salmonella growth and causes uncontrolled invasion of epithelial cells. Based on these observations, we propose that the S. enterica hilD 3'UTR is a cis-acting element that contributes to cellular homeostasis by promoting hilD mRNA turnover.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Base Sequence
  • Endoribonucleases / physiology
  • Gene Expression Regulation, Bacterial
  • Inverted Repeat Sequences
  • Molecular Sequence Data
  • Multienzyme Complexes / physiology
  • Polyribonucleotide Nucleotidyltransferase / physiology
  • RNA Helicases / physiology
  • RNA Stability
  • RNA, Bacterial / genetics*
  • RNA, Bacterial / metabolism
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • Salmonella typhimurium / genetics*
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • 3' Untranslated Regions
  • Bacterial Proteins
  • HilD protein, Salmonella typhimurium
  • Multienzyme Complexes
  • RNA, Bacterial
  • RNA, Messenger
  • Transcription Factors
  • degradosome
  • Polyribonucleotide Nucleotidyltransferase
  • Endoribonucleases
  • RNA Helicases