Characterization of the Escherichia coli σS core regulon by Chromatin Immunoprecipitation-sequencing (ChIP-seq) analysis

Peano, Clelia; Wolf, Johannes; Demol, Julien; Rossi, Elio; Petiti, Luca; Bellis, Gianluca De; Geiselmann, Johannes; Egli, Thomas; Lacour, Stéphan; Landini, Paolo

doi:10.1038/srep10469

Cited by 61 publications

(48 citation statements)

References 61 publications

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“…The first study used ChIP-chip to identify 868 RpoS-bound regions (25), many more than were identified in our study but at considerably lower resolution (median peak length of 324 bp for RpoS ChIP-chip). The second study used ChIP-seq but identified relatively few RpoS-bound regions (26). Of the 63 RpoS-bound regions identified in the second study, 41 were shared with those from our study.…”

Section: Discussionmentioning

confidence: 66%

“…We combined the ChIP-seq and RNA-seq data to identify genes that are directly transcribed by RNA polymerase containing RpoS. From these data, we identified 123 RpoS-transcribed genes in 99 transcripts (see Table S5 in the supplemental material) and compared these findings to those of other published analyses (18)(19)(20)(24)(25)(26)(27)(28). In some cases, we identified RpoS-bound regions upstream of genes that were not detected as being RpoS regulated by RNA-seq.…”

Section: Resultsmentioning

confidence: 72%

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Genome-Wide Transcriptional Response to Varying RpoS Levels in Escherichia coli K-12

et al. 2017

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The alternative sigma factor RpoS is a central regulator of many stress responses in Escherichia coli. The level of functional RpoS differs depending on the stress. The effect of these differing concentrations of RpoS on global transcriptional responses remains unclear. We investigated the effect of RpoS concentration on the transcriptome during stationary phase in rich media. We found that 23% of genes in the E. coli genome are regulated by RpoS, and we identified many RpoS-transcribed genes and promoters. We observed three distinct classes of response to RpoS by genes in the regulon: genes whose expression changes linearly with increasing RpoS level, genes whose expression changes dramatically with the production of only a little RpoS ("sensitive" genes), and genes whose expression changes very little with the production of a little RpoS ("insensitive"). We show that sequences outside the core promoter region determine whether an RpoS-regulated gene is sensitive or insensitive. Moreover, we show that sensitive and insensitive genes are enriched for specific functional classes and that the sensitivity of a gene to RpoS corresponds to the timing of induction as cells enter stationary phase. Thus, promoter sensitivity to RpoS is a mechanism to coordinate specific cellular processes with growth phase and may also contribute to the diversity of stress responses directed by RpoS. IMPORTANCEThe sigma factor RpoS is a global regulator that controls the response to many stresses in Escherichia coli. Different stresses result in different levels of RpoS production, but the consequences of this variation are unknown. We describe how changing the level of RpoS does not influence all RpoS-regulated genes equally. The cause of this variation is likely the action of transcription factors that bind the promoters of the genes. We show that the sensitivity of a gene to RpoS levels explains the timing of expression as cells enter stationary phase and that genes with different RpoS sensitivities are enriched for specific functional groups. Thus, promoter sensitivity to RpoS is a mechanism that coordinates specific cellular processes in response to stresses. KEYWORDS RpoS, promoters, S , stress response, transcriptional regulation, transcriptome G enome-wide measurements of RNA levels have revolutionized our understanding of how cells organize their patterns of transcription. These studies have given us snapshots of how patterns of gene expression change in response to changes in the external environment. They have also allowed us to define the regulons controlled by specific transcription factors (TFs). A major weakness of the vast majority of these

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Section: Discussionmentioning

confidence: 66%

Section: Resultsmentioning

confidence: 72%

Genome-Wide Transcriptional Response to Varying RpoS Levels in Escherichia coli K-12

et al. 2017

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“…SdsR is an enterobacterial core sRNA and an integral part of the large regulon controlled by the stationary phase sigma factor, σ S (40). Additional bacterial regulators such as GadY, SraL and SdsN sRNAs are also controlled by σ S (78–80), and recent experiments in E. coli identified σ S -binding to the promoter sequences of the two Hfq-dependent sRNAs, SdsR and OmrA (81). OmrA is a regulator of membrane homeostasis and biofilm formation in E. coli and, in addition to σ S , transcription of omrA is controlled by the EnvZ/OmpR TCS (82–84).…”

Section: Discussionmentioning

confidence: 99%

“…Its broad conservation amongst the enterobacteria together with the global role of several of the here identified targets make SdsR a fascinating sRNA to study further. Indeed, SdsR has now become the subject of intensive research (40,81,87,88,91), and it is likely that a deeper understanding of this sRNA will provide important leads towards the mechanisms of target regulation by Hfq-dependent sRNAs and stationary phase physiology of Gram-negative bacteria.…”

Section: Discussionmentioning

confidence: 99%

The target spectrum of SdsR small RNA inSalmonella

et al. 2016

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Model enteric bacteria such as Escherichia coli and Salmonella enterica express hundreds of small non-coding RNAs (sRNAs), targets for most of which are yet unknown. Some sRNAs are remarkably well conserved, indicating that they serve cellular functions that go beyond the necessities of a single species. One of these ‘core sRNAs’ of largely unknown function is the abundant ∼100-nucleotide SdsR sRNA which is transcribed by the general stress σ-factor, σS and accumulates in stationary phase. In Salmonella, SdsR was known to inhibit the synthesis of the species-specific porin, OmpD. However, sdsR genes are present in almost all enterobacterial genomes, suggesting that additional, conserved targets of this sRNA must exist. Here, we have combined SdsR pulse-expression with whole genome transcriptomics to discover 20 previously unknown candidate targets of SdsR which include mRNAs coding for physiologically important regulators such as the carbon utilization regulator, CRP, the nucleoid-associated chaperone, StpA and the antibiotic resistance transporter, TolC. Processing of SdsR by RNase E results in two cellular SdsR variants with distinct target spectra. While the overall physiological role of this orphan core sRNA remains to be fully understood, the new SdsR targets present valuable leads to determine sRNA functions in resting bacteria.

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“…Their genes (Argaman et al, 2001;Wassarman et al, 2001;Vogel et al, 2003) are transcriptionally activated by the OmpR-EnvZ two-component system, e.g., under high osmolarity conditions (Guillier & Gottesman, 2006;Brosse et al, 2016). OmrA, but not OmrB, is additionally under the control of the stress sigma factor r s (rpoS; Lévi-Meyrueis et al, 2014;Peano et al, 2015;Colgan et al, 2016). Both sRNAs associate with Hfq in vitro (Holmqvist et al, 2010) and in vivo (Wassarman et al, 2001;Zhang et al, 2003;Chao et al, 2012;Tree et al, 2014;Holmqvist et al, 2016); the sRNAs are destabilized in Δhfq cells (Holmqvist et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Hfq‐dependent mRNA unfolding promotes sRNA ‐based inhibition of translation

et al. 2019

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Small RNAs post‐transcriptionally regulate many processes in bacteria. Base‐pairing of sRNAs near ribosome‐binding sites in mRNAs inhibits translation, often requiring the RNA chaperone Hfq. In the canonical model, Hfq simultaneously binds sRNAs and mRNA targets to accelerate pairing. Here, we show that the Escherichia coli sRNAs OmrA and OmrB inhibit translation of the diguanylate cyclase DgcM (previously: YdaM), a player in biofilm regulation. In OmrA/B repression of dgcM, Hfq is not required as an RNA interaction platform, but rather unfolds an inhibitory RNA structure that impedes OmrA/B binding. This restructuring involves distal face binding of Hfq and is supported by RNA structure mapping. A corresponding mutant protein cannot support inhibition in vitro and in vivo; proximal and rim mutations have negligible effects. Strikingly, OmrA/B‐dependent translational inhibition in vitro is restored, in complete absence of Hfq, by a deoxyoligoribonucleotide that base‐pairs to the biochemically mapped Hfq site in dgcM mRNA. We suggest that Hfq‐dependent RNA structure remodeling can promote sRNA access, which represents a mechanism distinct from an interaction platform model.

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Characterization of the Escherichia coli σS core regulon by Chromatin Immunoprecipitation-sequencing (ChIP-seq) analysis

Cited by 61 publications

References 61 publications

Genome-Wide Transcriptional Response to Varying RpoS Levels in Escherichia coli K-12

Genome-Wide Transcriptional Response to Varying RpoS Levels in Escherichia coli K-12

The target spectrum of SdsR small RNA inSalmonella

Hfq‐dependent mRNA unfolding promotes sRNA ‐based inhibition of translation

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