Small regulatory RNA-induced growth rate heterogeneity of Bacillus subtilis

Ruben A T Mars, Pierre Nicolas, Mariano Ciccolini, Ewoud Reilman, Alexander Reder, Marc Schaffer, Ulrike Mäder, Uwe Völker, Jan Maarten van Dijl, Emma L Denham

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31 Citations (Scopus)

Abstract

Isogenic bacterial populations can consist of cells displaying heterogeneous physiological traits. Small regulatory RNAs (sRNAs) could affect this heterogeneity since they act by fine-tuning mRNA or protein levels to coordinate the appropriate cellular behavior. Here we show that the sRNA RnaC/S1022 from the Gram-positive bacterium Bacillus subtilis can suppress exponential growth by modulation of the transcriptional regulator AbrB. Specifically, the post-transcriptional abrB-RnaC/S1022 interaction allows B. subtilis to increase the cell-to-cell variation in AbrB protein levels, despite strong negative autoregulation of the abrB promoter. This behavior is consistent with existing mathematical models of sRNA action, thus suggesting that induction of protein expression noise could be a new general aspect of sRNA regulation. Importantly, we show that the sRNA-induced diversity in AbrB levels generates heterogeneity in growth rates during the exponential growth phase. Based on these findings, we hypothesize that the resulting subpopulations of fast- and slow-growing B. subtilis cells reflect a bet-hedging strategy for enhanced survival of unfavorable conditions.

Original languageEnglish
Article numbere1005046
Pages (from-to)1-27
Number of pages27
JournalPlos Genetics
Volume11
Issue number3
Early online date19 Mar 2015
DOIs
Publication statusPublished - 31 Mar 2015

Keywords

  • Bacillus subtilis/genetics
  • Bacterial Proteins/genetics
  • DNA-Binding Proteins/genetics
  • Gene Expression Regulation, Bacterial
  • Genetic Heterogeneity
  • Promoter Regions, Genetic
  • RNA/genetics
  • RNA, Messenger/biosynthesis
  • Transcription Factors/genetics

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Mars, R. A. T., Nicolas, P., Ciccolini, M., Reilman, E., Reder, A., Schaffer, M., Mäder, U., Völker, U., van Dijl, J. M., & Denham, E. L. (2015). Small regulatory RNA-induced growth rate heterogeneity of Bacillus subtilis. Plos Genetics, 11(3), 1-27. [e1005046]. https://doi.org/10.1371/journal.pgen.1005046