A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in Escherichia coli

Divya Balasubramanian, Preethi T. Ragunathan, Jingyi Fei, Carin K. Vanderpool

Research output: Contribution to journalArticle

Abstract

Hundreds of small RNAs (sRNAs) have been identified in diverse bacterial species, and while the functions of most remain unknown, some regulate key processes, particularly stress responses. The sRNA DicF was identified over 25 years ago as an inhibitor of cell division but since then has remained uncharacterized. DicF consists of 53 nucleotides and is encoded by a gene carried on a prophage (Qin) in the genomes of many Escherichia coli strains. We demonstrated that DicF inhibits cell division via direct base pairing with ftsZ mRNA to repress translation and prevent new synthesis of the bacterial tubulin homolog FtsZ. Systems analysis using computational and experimental methods identified additional mRNA targets of DicF: xylR and pykA mRNAs, encoding the xylose uptake and catabolism regulator and pyruvate kinase, respectively. Genetic analyses showed that DicF directly base pairs with and represses translation of these targets. Phenotypes of cells expressing DicF variants demonstrated that DicF-associated growth inhibition is not solely due to repression of ftsZ, indicating that the physiological consequences of DicF-mediated regulation extend beyond effects on cell division caused by reduced FtsZ synthesis. IMPORTANCE sRNAs are ubiquitous and versatile regulators of bacterial gene expression. A number of well-characterized examples in E. coli are highly conserved and present in the E. coli core genome. In contrast, the sRNA DicF (identified over 20 years ago but remaining poorly characterized) is encoded by a gene carried on a defective prophage element in many E. coli genomes. Here, we characterize DicF in order to better understand how horizontally acquired sRNA regulators impact bacterial gene expression and physiology. Our data confirm the long-hypothesized DicF-mediated regulation of ftsZ, encoding the bacterial tubulin homolog required for cell division. We further uncover DicF-mediated posttranscriptional control of metabolic gene expression. Ectopic production of DicF is highly toxic to E. coli cells, but the toxicity is not attributable to DicF regulation of ftsZ. Further work is needed to reveal the biological roles of and benefits for the host conferred by DicF and other products encoded by defective prophages.

Original languageEnglish (US)
Article numbere00021-15
JournalmSystems
Volume1
Issue number1
DOIs
StatePublished - Jan 1 2016

Fingerprint

Prophages
Cell Division
RNA
Metabolism
Escherichia coli
Escherichia Coli
cell division
Genes
metabolism
Cells
Gene expression
Regulator
Messenger RNA
Gene Expression
gene expression
Bacterial Genes
Genome
genome
Tubulin
tubulin

Keywords

  • Cryptic prophage
  • DicB
  • DicB
  • FtsZ
  • FtsZ
  • Hfq
  • Hfq
  • RNase E
  • RNase E

ASJC Scopus subject areas

  • Microbiology
  • Physiology
  • Biochemistry
  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Molecular Biology
  • Genetics
  • Computer Science Applications

Cite this

A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in Escherichia coli. / Balasubramanian, Divya; Ragunathan, Preethi T.; Fei, Jingyi; Vanderpool, Carin K.

In: mSystems, Vol. 1, No. 1, e00021-15, 01.01.2016.

Research output: Contribution to journalArticle

Balasubramanian, Divya ; Ragunathan, Preethi T. ; Fei, Jingyi ; Vanderpool, Carin K. / A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in Escherichia coli. In: mSystems. 2016 ; Vol. 1, No. 1.
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