Transcriptome-wide probing reveals RNA thermometers that regulate translation of glycerol permease genes in Bacillus subtilis

RNA structure regulates bacterial gene expression by several distinct mechanisms via environmental and cellular stimuli, one of which is temperature. While some genome-wide studies have focused on heat shock treatments and the subsequent transcriptomic changes, soil bacteria are less likely to experience such rapid and extreme temperature changes. Though RNA thermometers (RNATs) have been found in 5′ untranslated leader regions (5′ UTRs) of heat shock and virulence-associated genes, this RNA-controlled mechanism could regulate other genes as well. Using Structure-seq2 and the chemical probe dimethyl sulfate (DMS) at four growth temperatures ranging from 23°C to 42°C, we captured a dynamic response of the Bacillus subtilis transcriptome to temperature. Our transcriptome-wide results show RNA structural changes across all four temperatures and reveal nonmonotonic reactivity trends with increasing temperature. Then, focusing on subregions likely to contain regulatory RNAs, we examined 5′ UTRs to identify large, local reactivity changes. This approach led to the discovery of RNATs that control the expression of glpF (glycerol permease) and glpT (glycerol-3-phosphate permease); expression of both genes increased with increased temperature. Results with mutant RNATs indicate that both genes are controlled at the translational level. Increased import of glycerols at high temperatures could provide thermoprotection to proteins.

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Work Title Transcriptome-wide probing reveals RNA thermometers that regulate translation of glycerol permease genes in Bacillus subtilis
Access
Open Access
Creators
  1. Elizabeth A. Jolley
  2. Helen Yakhnin
  3. David C. Tack
  4. Paul Babitzke
  5. Philip C. Bevilacqua
Keyword
  1. RNA thermometers
  2. RNA–protein
  3. Structure-seq
  4. Glycerol permease
License In Copyright (Rights Reserved)
Work Type Article
Publisher
  1. RNA
Publication Date May 22, 2023
Publisher Identifier (DOI)
  1. https://doi.org/10.1261/rna.079652.123
Deposited March 14, 2025

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Version 1
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  • Created
  • Added RNA-2023-Jolley-rna.079652.123-1.pdf
  • Added Creator Elizabeth A Jolley
  • Added Creator Helen Yakhnin
  • Added Creator E B Yakhnin
  • Added Creator David C Tack
  • Added Creator Paul Babitzke
  • Added Creator Philip C. Bevilacqua
  • Published
  • Updated
  • Updated Keyword Show Changes
    Keyword
    • RNA thermometers, RNA–protein, Structure-seq, Glycerol permease
  • Deleted Creator E B Yakhnin
  • Renamed Creator Elizabeth A. Jolley Show Changes
    • Elizabeth A Jolley
    • Elizabeth A. Jolley
  • Renamed Creator David C. Tack Show Changes
    • David C Tack
    • David C. Tack
  • Updated Creator Paul Babitzke
  • Updated Creator Philip C. Bevilacqua