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Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes.

ABSTRACT: The genomes of various eubacteria were analyzed by Southern blot hybridization to detect sequences related to the segment of the defective lambdoid prophage Kim which encodes DicF RNA, an antisense inhibitor of cell division gene ftsZ in Escherichia coli K-12. Among the homologous sequences found, one fragment from E. coli B, similar to a piece of Rac prophage, and two fragments from Shigella flexneri were cloned and sequenced. dicF-like elements similar to transcriptional terminators were found in each sequence, but unlike dicF these had no effect on division in E. coli K-12. Like dicF, these sequences are flanked by secondary structures which form potential sites for RNase III recognition. Coding sequences located upstream from the dicF-like feature in E. coli B are related to gene sieB of bacteriophage lambda, while sequences downstream of the S. flexneri elements are similar to the immunity region of satellite bacteriophage P4. Under hybridization conditions in which only strong sequence homologies were detected in E. coli B and S. flexneri, the genomes of a large variety of microorganisms, including some gram-positive bacteria, hybridized to the dicF probe. Our results suggest that dicF and its flanking regions are markers of a widespread family of prophage-like elements of different origins.

SUBMITTER: Faubladier M

PROVIDER: S-EPMC205167 | biostudies-other | 1994 Feb

REPOSITORIES: biostudies-other

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Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes.

Faubladier M M Bouché J P JP

Journal of bacteriology 19940201 4

The genomes of various eubacteria were analyzed by Southern blot hybridization to detect sequences related to the segment of the defective lambdoid prophage Kim which encodes DicF RNA, an antisense inhibitor of cell division gene ftsZ in Escherichia coli K-12. Among the homologous sequences found, one fragment from E. coli B, similar to a piece of Rac prophage, and two fragments from Shigella flexneri were cloned and sequenced. dicF-like elements similar to transcriptional terminators were found ...[more]

PMID: 7508908

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Project description: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.

Dataset Information

Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes.

Publications

Division inhibition gene dicF of Escherichia coli reveals a widespread group of prophage sequences in bacterial genomes.

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