σN-dependent control of acid resistance and the locus of enterocyte effacement in enterohemorrhagic Escherichia coli is activated by acetyl phosphate in a manner requiring flagellar regulator FlhDC and the σS antagonist FliZ

In enterohemorrhagic Escherichia coli (EHEC), sigma factor N (σN) regulates glutamate‐dependent acid resistance (GDAR) and the locus of enterocyte effacement (LEE); discrete genetic systems that are required for transmission and virulence of this intestinal pathogen. Regulation of these systems requires nitrogen regulatory protein C, NtrC, and is a consequence of NtrC‐σN‐dependent reduction in the activity of sigma factor S (σS). This study elucidates pathway components and stimuli for σN‐directed regulation of GDAR and the LEE in EHEC. Deletion of fliZ, the product of which reduces σS activity, phenocopied rpoN (σN) and ntrC null strains for GDAR and LEE control, acid resistance, and adherence. Upregulation of fliZ by NtrC‐σN was shown to be indirect and required an intact flagellar regulator flhDC. Activation of flhDC by NtrC‐σN and FlhDC‐dependent regulation of GDAR and the LEE was dependent on σN‐promoter flhDP2, and a newly described NtrC upstream activator sequence. Addition of ammonium chloride significantly altered expression of GDAR and LEE, acid resistance, and adherence, independently of rpoN, ntrC, and the NtrC sensor kinase, ntrB. Altering the availability of NtrC phosphodonor acetyl phosphate by growth without glucose, with acetate addition, or by deletion of acetate kinase ackA, abrogated NtrC‐σN‐dependent control of flhDC, fliZ, GDAR, and the LEE.

• Publication year

  2014

• Venue

  MicrobiologyOpen

• Publication date

  2014-06-16

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1002/mbo3.183PMID 24931910PMCID 4287178
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2011influential reference
• Inactivation of alternative sigma factor 54 (RpoN) leads to increased acid resistance, and alters locus of enterocyte effacement (LEE) expression in Escherichia coli O157 : H7.

  2010cited by this paper
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  2010cited by this paper
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  2009cited by this paper
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  2009cited by this paper
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  2009cited by this paper
• Characterization of the Escherichia coli O157:H7 Sakai GadE Regulon

  2008cited by this paper
• Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks

  2008cited by this paper
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  2008cited by this paper
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  2008cited by this paper
• Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli.

  2008cited by this paper
• Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine‐tuner of σs activity and levels

  2007cited by this paper
• Evidence that RpoS (sigmaS) in Borrelia burgdorferi is controlled directly by RpoN (sigma54/sigmaN).

  2007cited by this paper
• The GrlR-GrlA Regulatory System Coordinately Controls the Expression of Flagellar and LEE-Encoded Type III Protein Secretion Systems in Enterohemorrhagic Escherichia coli

  2006cited by this paper
• Evidence that RpoS (σS) in Borrelia burgdorferi Is Controlled Directly by RpoN (σ54/σN)

  2006cited by this paper
• Concert of regulators to switch on LEE expression in enterohemorrhagic Escherichia coli O157:H7: interplay between Ler, GrlA, HNS and RpoS.

  2006influential reference
• The Acetate Switch

  2005cited by this paper
• ClpXP controls the expression of LEE genes in enterohaemorrhagic Escherichia coli.

  2005cited by this paper
• Mouse Intestine Selects Nonmotile flhDC Mutants of Escherichia coli MG1655 with Increased Colonizing Ability and Better Utilization of Carbon Sources

  2005cited by this paper
• Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002

  2005cited by this paper
• ClpXP Protease Controls Expression of the Type III Protein Secretion System through Regulation of RpoS and GrlR Levels in Enterohemorrhagic Escherichia coli

  2005cited by this paper
• Crl, a Low Temperature-induced Protein in Escherichia coli That Binds Directly to the Stationary Phase σ Subunit of RNA Polymerase*

  2004cited by this paper
• Dose Response for Infection by Escherichia coli O157:H7 from Outbreak Data

  2004cited by this paper
• Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals.

  2004cited by this paper
• Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli O157 : H7 to HEp-2 cells.

  2004cited by this paper
• Escherichia coli acid resistance: tales of an amateur acidophile

  2004cited by this paper
• RcsCDB His‐Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli

  2003cited by this paper
• Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli

  2003cited by this paper
• pH-Dependent Modulation of Cyclic AMP Levels and GadW-Dependent Repression of RpoS Affect Synthesis of the GadX Regulator and Escherichia coli Acid Resistance

  2003influential reference
• Nitrogen assimilation and global regulation in Escherichia coli.

  2003cited by this paper
• Bicarbonate Ion Stimulates the Expression of Locus of Enterocyte Effacement-Encoded Genes in Enterohemorrhagic Escherichia coli O157:H7

  2002cited by this paper
• Signal Transduction and Regulatory Mechanisms Involved in Control of the σS (RpoS) Subunit of RNA Polymerase

  2002cited by this paper
• Metabolic context and possible physiological themes of sigma(54)-dependent genes in Escherichia coli.

  2001cited by this paper
• Metabolic Context and Possible Physiological Themes of ς54-Dependent Genes in Escherichia coli

  2001cited by this paper
• Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN–RpoS regulatory pathway

  2001cited by this paper
• Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

  2001cited by this paper
• One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.

  2000cited by this paper
• VTEC enteropathogenicity

  2000cited by this paper
• Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A.

  2000cited by this paper
• Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation.

  2000cited by this paper
• Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays.

  2000cited by this paper
• Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli

  1999influential reference
• Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli.

  1999cited by this paper
• Molecular Evolution of a Pathogenicity Island from Enterohemorrhagic Escherichia coli O157:H7

  1998cited by this paper
• The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69

  1998cited by this paper
• The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69.

  1998cited by this paper
• Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli

  1998cited by this paper
• Crl stimulates RpoS activity during stationary phase

  1998cited by this paper
• A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K‐12

  1997cited by this paper
• Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract

  1997cited by this paper
• Differential regulation of fasA and fasH expression of Escherichia coli 987P fimbriae by environmental cues

  1997cited by this paper
• Signal sensing by σ54‐dependent regulators: derepression as a control mechanism

  1996cited by this paper
• The bundle‐forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals

  1996cited by this paper
• Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels.

  1996cited by this paper
• Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter

  1995cited by this paper
• Investigation of enterohemorrhagic Escherichia coli O157:H7 adherence characteristics and invasion potential reveals a new attachment pattern shared by intestinal E. coli

  1995cited by this paper
• Acetyl phosphate and the activation of two-component response regulators.

  1994cited by this paper
• Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli

  1994cited by this paper
• Bacterial overgrowth of the gastrointestinal tract.

  1993cited by this paper
• Bacterial overgrowth of the gastrointestinal tract.

  1993cited by this paper
• Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli

  1992influential reference
• Activation of glnA transcription by nitrogen regulator I (NRI)-phosphate in Escherichia coli: evidence for a long-range physical interaction between NRI-phosphate and RNA polymerase

  1989cited by this paper
• Changes in the intracellular concentration of acetyl-CoA and malonyl-CoA in relation to the carbon and energy metabolism of Escherichia coli K12.

  1988cited by this paper
• Mutations that create new promoters suppress the sigma 54 dependence of glnA transcription in Escherichia coli

  1987influential reference
• Nitrogen regulation in Salmonella typhimurium. Identification of an ntrC protein‐binding site and definition of a consensus binding sequence.

  1985cited by this paper
• Nitrogen Regulation in Salmonella typhimurium

  1980cited by this paper
• Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid

  1978cited by this paper
• Culture Medium for Enterobacteria

  1974cited by this paper
• Enzymatic phosphorylation of acetate.

  1954cited by this paper

• Metabolic Regulation and Engineering Strategies of Carbon and Nitrogen Metabolism in Escherichia coli.

  2025cites this paper
• The RNA polymerase gene specificity factor σ54 is required for homogeneous non-planktonic growth of uropathogenic Escherichia coli

  2022cites this paper
• A Role for the RNA Polymerase Gene Specificity Factor σ54 in the Uniform Colony Growth of Uropathogenic Escherichia coli

  2022cites this paper
• Regulation Mechanisms of Virulence Genes in Enterohemorrhagic Escherichia coli

  2022cites this paper
• Prediction and Inferred Evolution of Acid Tolerance Genes in the Biotechnologically Important Acidihalobacter Genus

  2022cites this paper
• The Role of Alternative Sigma Factors in Pathogen Virulence

  2017cites this paper
• Regulation of Escherichia coli Pathogenesis by Alternative Sigma Factor N

  2017cites this paper
• Biophysics of Infection

  2016cites this paper
• Staphylococcus aureus SufT: an essential iron‐sulphur cluster assembly factor in cells experiencing a high‐demand for lipoic acid

  2016cites this paper
• Transcription Regulation and Membrane Stress Management in Enterobacterial Pathogens.

  2016cites this paper
• Global Regulator of Virulence A (GrvA) Coordinates Expression of Discrete Pathogenic Mechanisms in Enterohemorrhagic Escherichia coli through Interactions with GadW-GadE

  2015cites this paper
• Glycolysis for Microbiome Generation

  2015cites this paper
• The role for TolA in enterohemorrhagic Escherichia coli pathogenesis and virulence gene transcription.

  2014cites this paper
• Investigating the genetic regulation of the ECF sigma factor σS in Staphylococcus aureus

  2014cites this paper