Small noncoding RNA GcvB is a novel regulator of acid resistance in Escherichia coli

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Abstract

Background

The low pH environment of the human stomach is lethal for most microorganisms; but not Escherichia coli, which can tolerate extreme acid stress. Acid resistance in E. coli is hierarchically controlled by numerous regulators among which are small noncoding RNAs (sncRNA).

Results

In this study, we individually deleted seventy-nine sncRNA genes from the E. coli K12-MG1655 chromosome, and established a single-sncRNA gene knockout library. By systematically screening the sncRNA mutant library, we show that the sncRNA GcvB is a novel regulator of acid resistance in E. coli. We demonstrate that GcvB enhances the ability of E. coli to survive low pH by upregulating the levels of the alternate sigma factor RpoS.

Conclusion

GcvB positively regulates acid resistance by affecting RpoS expression. These data advance our understanding of the sncRNA regulatory network involved in modulating acid resistance in E. coli.

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Most cited references 24

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MaGe: a microbial genome annotation system supported by synteny results

David Vallenet, Laurent Labarre, Zoe Rouy … (2006)

Magnifying Genomes (MaGe) is a microbial genome annotation system based on a relational database containing information on bacterial genomes, as well as a web interface to achieve genome annotation projects. Our system allows one to initiate the annotation of a genome at the early stage of the finishing phase. MaGe's main features are (i) integration of annotation data from bacterial genomes enhanced by a gene coding re-annotation process using accurate gene models, (ii) integration of results obtained with a wide range of bioinformatics methods, among which exploration of gene context by searching for conserved synteny and reconstruction of metabolic pathways, (iii) an advanced web interface allowing multiple users to refine the automatic assignment of gene product functions. MaGe is also linked to numerous well-known biological databases and systems. Our system has been thoroughly tested during the annotation of complete bacterial genomes (Acinetobacter baylyi ADP1, Pseudoalteromonas haloplanktis, Frankia alni) and is currently used in the context of several new microbial genome annotation projects. In addition, MaGe allows for annotation curation and exploration of already published genomes from various genera (e.g. Yersinia, Bacillus and Neisseria). MaGe can be accessed at .

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Translational control and target recognition by Escherichia coli small RNAs in vivo

Johannes Urban, Jörg Vogel (2007)

Small non-coding RNAs (sRNAs) are an emerging class of regulators of bacterial gene expression. Most of the regulatory Escherichia coli sRNAs known to date modulate translation of trans-encoded target mRNAs. We studied the specificity of sRNA target interactions using gene fusions to green fluorescent protein (GFP) as a novel reporter of translational control by bacterial sRNAs in vivo. Target sequences were selected from both monocistronic and polycistronic mRNAs. Upon expression of the cognate sRNA (DsrA, GcvB, MicA, MicC, MicF, RprA, RyhB, SgrS and Spot42), we observed highly specific translation repression/activation of target fusions under various growth conditions. Target regulation was also tested in mutants that lacked Hfq or RNase III, or which expressed a truncated RNase E (rne701). We found that translational regulation by these sRNAs was largely independent of full-length RNase E, e.g. despite the fact that ompA fusion mRNA decay could no longer be promoted by MicA. This is the first study in which multiple well-defined E.coli sRNA target pairs have been studied in a uniform manner in vivo. We expect our GFP fusion approach to be applicable to sRNA targets of other bacteria, and also demonstrate that Vibrio RyhB sRNA represses a Vibrio sodB fusion when co-expressed in E.coli.

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A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites.

Titia Plantinga, M. Sharma, Jörg Vogel … (2007)

The interactions of numerous regulatory small RNAs (sRNAs) with target mRNAs have been characterized, but how sRNAs can regulate multiple, structurally unrelated mRNAs is less understood. Here we show that Salmonella GcvB sRNA directly acts on seven target mRNAs that commonly encode periplasmic substrate-binding proteins of ABC uptake systems for amino acids and peptides. Alignment of GcvB homologs of distantly related bacteria revealed a conserved G/U-rich element that is strictly required for GcvB target recognition. Analysis of target gene fusion regulation in vivo, and in vitro structure probing and translation assays showed that GcvB represses its target mRNAs by binding to extended C/A-rich regions, which may also serve as translational enhancer elements. In some cases (oppA, dppA), GcvB repression can be explained by masking the ribosome-binding site (RBS) to prevent 30S subunit binding. However, GcvB can also effectively repress translation by binding to target mRNAs at upstream sites, outside the RBS. Specifically, GcvB represses gltI mRNA translation at the C/A-rich target site located at positions -57 to -45 relative to the start codon. Taken together, our study suggests highly conserved regions in sRNAs and mRNA regions distant from Shine-Dalgarno sequences as important elements for the identification of sRNA targets.

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Author and article information

Journal

Journal ID (nlm-ta): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central

ISSN (Electronic): 1471-2164

Publication date Collection: 2009

Publication date (Electronic): 20 April 2009

Volume: 10

Page: 165

Affiliations

[1 ]Department of Biochemistry, Li Ka Shing Faculty of Medicine, University of Hong Kong, Pok Fu Lam, Hong Kong SAR, PR China

[2 ]Oral Biosciences, Faculty of Dentistry, University of Hong Kong, Pok Fu Lam, Hong Kong SAR, PR China

[3 ]Genetics of Bacterial Genomes, CNRS URA2171, Institut Pasteur, 28, rue du Docteur Roux, Paris Cedex 15, 75724, France

Article

Publisher ID: 1471-2164-10-165

DOI: 10.1186/1471-2164-10-165

PMC ID: 2676305

PubMed ID: 19379489

SO-VID: 73e579bf-549e-4e2e-89bf-2ed33c6c91ea

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Small noncoding RNA GcvB is a novel regulator of acid resistance in Escherichia coli

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Most cited references 24

MaGe: a microbial genome annotation system supported by synteny results

Translational control and target recognition by Escherichia coli small RNAs in vivo

A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites.

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