A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>

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 re...

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Autores principales:	Divya Balasubramanian, Preethi T. Ragunathan, Jingyi Fei, Carin K. Vanderpool
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	DicB FtsZ Hfq Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/24445ba7236140899805ff0c53899f68
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spelling	oai:doaj.org-article:24445ba7236140899805ff0c53899f682021-12-02T18:15:43ZA Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mSystems.00021-152379-5077https://doaj.org/article/24445ba7236140899805ff0c53899f682016-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00021-15https://doaj.org/toc/2379-5077ABSTRACT 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.Divya BalasubramanianPreethi T. RagunathanJingyi FeiCarin K. VanderpoolAmerican Society for MicrobiologyarticleDicBDicBFtsZFtsZHfqHfqMicrobiologyQR1-502ENmSystems, Vol 1, Iss 1 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	DicB DicB FtsZ FtsZ Hfq Hfq Microbiology QR1-502
spellingShingle	DicB DicB FtsZ FtsZ Hfq Hfq Microbiology QR1-502 Divya Balasubramanian Preethi T. Ragunathan Jingyi Fei Carin K. Vanderpool A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
description	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.
format	article
author	Divya Balasubramanian Preethi T. Ragunathan Jingyi Fei Carin K. Vanderpool
author_facet	Divya Balasubramanian Preethi T. Ragunathan Jingyi Fei Carin K. Vanderpool
author_sort	Divya Balasubramanian
title	A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	prophage-encoded small rna controls metabolism and cell division in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/24445ba7236140899805ff0c53899f68
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A Prophage-Encoded Small RNA Controls Metabolism and Cell Division in <named-content content-type="genus-species">Escherichia coli</named-content>

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