Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae

Abstract

Gene duplication and subsequent evolutionary divergence have allowed conserved proteins to develop unique roles. The MarR family of transcription factors (TFs) has undergone extensive duplication and diversification in bacteria, where they act as environmentally responsive repressors of genes encoding efflux pumps that confer resistance to xenobiotics, including many antimicrobial agents. We have performed structural, functional, and genetic analyses of representative members of the SlyA/RovA lineage of MarR TFs, which retain some ancestral functions, including repression of their own expression and that of divergently transcribed multidrug efflux pumps, as well as allosteric inhibition by aromatic carboxylate compounds. However, SlyA and RovA have acquired the ability to countersilence horizontally acquired genes, which has greatly facilitated the evolution of Enterobacteriaceaeby horizontal gene transfer. SlyA/RovA TFs in different species have independently evolved novel regulatory circuits to provide the enhanced levels of expression required for their new role. Moreover, in contrast to MarR, SlyA is not responsive to copper. These observations demonstrate the ability of TFs to acquire new functions as a result of evolutionary divergence of bothcis-regulatory sequences and intransinteractions with modulatory ligands. IMPORTANCEBacteria primarily evolve via horizontal gene transfer, acquiring new traits such as virulence and antibiotic resistance in single transfer events. However,more » newly acquired genes must be integrated into existing regulatory networks to allow appropriate expression in new hosts. This is accommodated in part by the opposing mechanisms of xenogeneic silencing and countersilencing. An understanding of these mechanisms is necessary to understand the relationship between gene regulation and bacterial evolution. Here we examine the functional evolution of an important lineage of countersilencers belonging to the ancient MarR family of classical transcriptional repressors. We show that although members of the SlyA lineage retain some ancestral features associated with the MarR family, theircis-regulatory sequences have evolved significantly to support their new function. Understanding the mechanistic requirements for countersilencing is critical to understanding the pathoadaptation of emerging pathogens and also has practical applications in synthetic biology.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [6];  [6];  [7];  [8]; ORCiD logo [9];  [10]
+ Show Author Affiliations
  1. Univ. of Washington, Seattle, WA (United States). Dept. of Laboratory Medicine
  2. Univ. of Washington, Seattle, WA (United States). Dept. of Biochemistry
  3. Univ. of Washington, Seattle, WA (United States). Dept. of Biological Structure
  4. Univ. of Washington, Seattle, WA (United States). Dept. of Biochemistry Univ. of Washington, Seattle, WA (United States). Dept. of Biological Structure
  5. Univ. of Louisville School of Medicine, Louisville, KY (United States). Dept. of Microbiology and Immunology and the Center for Predictive Medicine for Biodefense and Emerging Infectious Diseases
  6. Univ. of Washington, Seattle, WA (United States). Dept. of Microbiology
  7. Univ. of North Carolina School of Medicine, Chapel Hill, NC (United States). Dept.of Microbiology and Immunology; Univ. of North Carolina School of Medicine, Chapel Hill, NC (United States). Dept.of Genetics
  8. Univ. of Washington, Seattle, WA (United States). Dept. of Medicine
  9. Univ. of Washington, Seattle, WA (United States). Dept. of Laboratory Medicine; Univ. of Washington, Seattle, WA (United States). Dept. of Microbiology
  10. Univ. of Illinois, Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Cancer Institute (NCI); National Institute of General Medical Sciences
OSTI Identifier:
1626076
Grant/Contract Number:  
AC02-06CH11357; ACB-12002; AGM-12006
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 10; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
Microbiology; SlyA, countersilencing; evolution; gene regulation; transcription factors

Citation Formats

Will, W. Ryan, Brzovic, Peter, Le Trong, Isolde, Stenkamp, Ronald E., Lawrenz, Matthew B., Karlinsey, Joyce E., Navarre, William W., Main-Hester, Kara, Miller, Virginia L., Libby, Stephen J., Fang, Ferric C., and Freitag, Nancy E. The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae. United States: N. p., 2019. Web. doi:10.1128/mbio.00009-19.
Copy to clipboard
Will, W. Ryan, Brzovic, Peter, Le Trong, Isolde, Stenkamp, Ronald E., Lawrenz, Matthew B., Karlinsey, Joyce E., Navarre, William W., Main-Hester, Kara, Miller, Virginia L., Libby, Stephen J., Fang, Ferric C., & Freitag, Nancy E. The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae. United States. https://doi.org/10.1128/mbio.00009-19
Copy to clipboard
Will, W. Ryan, Brzovic, Peter, Le Trong, Isolde, Stenkamp, Ronald E., Lawrenz, Matthew B., Karlinsey, Joyce E., Navarre, William W., Main-Hester, Kara, Miller, Virginia L., Libby, Stephen J., Fang, Ferric C., and Freitag, Nancy E. Tue . "The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae". United States. https://doi.org/10.1128/mbio.00009-19. https://www.osti.gov/servlets/purl/1626076.
Copy to clipboard
@article{osti_1626076,
title = {The Evolution of SlyA/RovA Transcription Factors from Repressors to Countersilencers in Enterobacteriaceae},
author = {Will, W. Ryan and Brzovic, Peter and Le Trong, Isolde and Stenkamp, Ronald E. and Lawrenz, Matthew B. and Karlinsey, Joyce E. and Navarre, William W. and Main-Hester, Kara and Miller, Virginia L. and Libby, Stephen J. and Fang, Ferric C. and Freitag, Nancy E.},
abstractNote = {Gene duplication and subsequent evolutionary divergence have allowed conserved proteins to develop unique roles. The MarR family of transcription factors (TFs) has undergone extensive duplication and diversification in bacteria, where they act as environmentally responsive repressors of genes encoding efflux pumps that confer resistance to xenobiotics, including many antimicrobial agents. We have performed structural, functional, and genetic analyses of representative members of the SlyA/RovA lineage of MarR TFs, which retain some ancestral functions, including repression of their own expression and that of divergently transcribed multidrug efflux pumps, as well as allosteric inhibition by aromatic carboxylate compounds. However, SlyA and RovA have acquired the ability to countersilence horizontally acquired genes, which has greatly facilitated the evolution of Enterobacteriaceaeby horizontal gene transfer. SlyA/RovA TFs in different species have independently evolved novel regulatory circuits to provide the enhanced levels of expression required for their new role. Moreover, in contrast to MarR, SlyA is not responsive to copper. These observations demonstrate the ability of TFs to acquire new functions as a result of evolutionary divergence of bothcis-regulatory sequences and intransinteractions with modulatory ligands. IMPORTANCEBacteria primarily evolve via horizontal gene transfer, acquiring new traits such as virulence and antibiotic resistance in single transfer events. However, newly acquired genes must be integrated into existing regulatory networks to allow appropriate expression in new hosts. This is accommodated in part by the opposing mechanisms of xenogeneic silencing and countersilencing. An understanding of these mechanisms is necessary to understand the relationship between gene regulation and bacterial evolution. Here we examine the functional evolution of an important lineage of countersilencers belonging to the ancient MarR family of classical transcriptional repressors. We show that although members of the SlyA lineage retain some ancestral features associated with the MarR family, theircis-regulatory sequences have evolved significantly to support their new function. Understanding the mechanistic requirements for countersilencing is critical to understanding the pathoadaptation of emerging pathogens and also has practical applications in synthetic biology.},
doi = {10.1128/mbio.00009-19},
journal = {mBio (Online)},
number = 2,
volume = 10,
place = {United States},
year = {Tue Mar 05 00:00:00 EST 2019},
month = {Tue Mar 05 00:00:00 EST 2019}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mbio.00009-19
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

Figures / Tables:

FIG 1 FIG 1: SlyA retains the ancestral functions of MarR family TFs. To determine whether SlyA is an autorepressor like other members of the MarR family, in vitro transcription (IVT) assays were performed on supercoiled template DNA containing slyA and the divergently expressed ydhI gene in the presence of increasing SlyAmore » concentrations (A). Reactions were performed with or without 2 mM sodium salicylate to determine whether SlyA is inhibited by small aromatic carboxylate compounds like other MarR TFs. To determine whether SlyA exhibits a dose-dependent response to salicylate, IVT assays were performed on ydhI in the presence of 2 μM SlyA and increasing concentrations of sodium salicylate (B). To confirm that SlyA does not function as an activator at upregulated targets, IVT assays of the model SlyA target gene, pagC, were performed in the presence of increasing concentrations of SlyA (C). All IVT data represent the mean ± SEM (n ≥ 3). Wild-type, slyA, ydhIJK, and slyA ydhIJK cultures were grown in the presence of 30 μg/ml fusaric acid, and cell density (OD600) was measured over time to determine if ydhIJK encodes a functional antimicrobial efflux pump (D). Data represent the mean (solid line) from three independent experiments, each consisting of three replicates. Dashed lines represent the SD. The control plot represents the growth curve of each strain in the absence of fusaric acid. To determine whether salicylate also inhibits SlyA countersilencing activity, pagC transcripts were quantified by qRT-PCR from early-stationary-phase (OD600 ≈2.0) cultures in minimal N-medium containing 10 μM MgCl2 in the presence or absence of 2 mM sodium salicylate (E). Transcript levels are normalized to rpoD, and data represent the mean ± SD (n ≥ 3). Asterisk indicates P = 0.05.« less
All figures and tables (8 total)
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Evolutionary expansion of a regulatory network by counter-silencing
journal, October 2014

  • Will, W. Ryan; Bale, Denise H.; Reid, Philip J.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6270

MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
journal, May 2018

  • Kumar, Sudhir; Stecher, Glen; Li, Michael
  • Molecular Biology and Evolution, Vol. 35, Issue 6
  • DOI: 10.1093/molbev/msy096

Molecular Mechanisms of Ligand-Mediated Attenuation of DNA Binding by MarR Family Transcriptional Regulators
journal, August 2010

  • Perera, I. C.; Grove, A.
  • Journal of Molecular Cell Biology, Vol. 2, Issue 5
  • DOI: 10.1093/jmcb/mjq021

Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997

  • Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
  • DOI: 10.1107/S0907444996012255

Evolution by Gene Duplication
book, January 1970

Analysis of RovA, a Transcriptional Regulator of Yersinia pseudotuberculosis Virulence That Acts through Antirepression and Direct Transcriptional Activation
journal, October 2005

  • Tran, Hien J.; Heroven, Ann Kathrin; Winkler, Lars
  • Journal of Biological Chemistry, Vol. 280, Issue 51
  • DOI: 10.1074/jbc.M504464200

Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis
journal, September 2004

  • Chain, P. S. G.; Carniel, E.; Larimer, F. W.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 38
  • DOI: 10.1073/pnas.0404012101

Discrimination and Integration of Stress Signals by Pathogenic Bacteria
journal, August 2016

Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences.
journal, June 1995

  • Martin, R. G.; Rosner, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 12
  • DOI: 10.1073/pnas.92.12.5456

An Improved General Amino Acid Replacement Matrix
journal, April 2008

Structural characterization of the DNA-binding mechanism underlying the copper(II)-sensing MarR transcriptional regulator
journal, January 2017

  • Zhu, Rongfeng; Hao, Ziyang; Lou, Hubing
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 5
  • DOI: 10.1007/s00775-017-1442-7

Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli
journal, September 1988

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2015

  • Caspi, Ron; Billington, Richard; Ferrer, Luciana
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1164

Regulation of Metabolic Pathways by MarR Family Transcription Factors
journal, January 2017

RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague
journal, August 2006

  • Cathelyn, J. S.; Crosby, S. D.; Lathem, W. W.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 36
  • DOI: 10.1073/pnas.0603456103

An umbra-related virus found in babaco (Vasconcellea × heilbornii)
journal, May 2021

  • Cornejo-Franco, Juan F.; Flores, Francisco; Mollov, Dimitre
  • Archives of Virology, Vol. 166, Issue 8
  • DOI: 10.1007/s00705-021-05117-8

Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans
journal, January 1999

  • Dale, Colin; Maudlin, Ian
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 1
  • DOI: 10.1099/00207713-49-1-267

EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB.
journal, January 1995

Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12
journal, November 2007

The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli
journal, November 2013

  • Hao, Ziyang; Lou, Hubing; Zhu, Rongfeng
  • Nature Chemical Biology, Vol. 10, Issue 1
  • DOI: 10.1038/nchembio.1380

Activation of the Bacterial Sensor Kinase PhoQ by Acidic pH
journal, April 2007

Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea
journal, December 2004

Structure of an OhrR-ohrA Operator Complex Reveals the DNA Binding Mechanism of the MarR Family
journal, October 2005

Phenolic Compounds and Their Role in Disease Resistance
journal, September 1992

The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome
journal, October 2007

The CCP4 suite programs for protein crystallography
journal, September 1994

MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures
journal, October 1991

RegulonDB version 9.0: high-level integration of gene regulation, coexpression, motif clustering and beyond
journal, November 2015

  • Gama-Castro, Socorro; Salgado, Heladia; Santos-Zavaleta, Alberto
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1156

Improved Fourier coefficients for maps using phases from partial structures with errors
journal, May 1986

  • Read, R. J.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 42, Issue 3
  • DOI: 10.1107/S0108767386099622

Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function
journal, February 2009

  • Osborne, S. E.; Walthers, D.; Tomljenovic, A. M.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 10
  • DOI: 10.1073/pnas.0811669106

Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway.
journal, January 1993

RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more
journal, November 2012

  • Salgado, Heladia; Peralta-Gil, Martin; Gama-Castro, Socorro
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1201

Global Transcriptional Start Site Mapping Using Differential RNA Sequencing Reveals Novel Antisense RNAs in Escherichia coli
journal, September 2014

  • Thomason, Maureen K.; Bischler, Thorsten; Eisenbart, Sara K.
  • Journal of Bacteriology, Vol. 197, Issue 1
  • DOI: 10.1128/JB.02096-14

Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
journal, July 1995

Identification and expression of the BAHD family during development, ripening, and stress response in banana
journal, January 2021

SWISS-MODEL: an automated protein homology-modeling server
journal, July 2003

An Infection-Relevant Transcriptomic Compendium for Salmonella enterica Serovar Typhimurium
journal, December 2013

SlyA, a MarR Family Transcriptional Regulator, Is Essential for Virulence in Dickeya dadantii 3937
journal, June 2009

  • Haque, M. M.; Kabir, M. S.; Aini, L. Q.
  • Journal of Bacteriology, Vol. 191, Issue 17
  • DOI: 10.1128/JB.00240-09

NMR View: A computer program for the visualization and analysis of NMR data
journal, September 1994

  • Johnson, Bruce A.; Blevins, Richard A.
  • Journal of Biomolecular NMR, Vol. 4, Issue 5
  • DOI: 10.1007/BF00404272

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Chromatin Immunoprecipitation for Determining the Association of Proteins with Specific Genomic Sequences In Vivo
journal, January 2005

  • Aparicio, Oscar; Geisberg, Joseph V.; Sekinger, Edward
  • Current Protocols in Molecular Biology, Vol. 69, Issue 1
  • DOI: 10.1002/0471142727.mb2103s69

Integrated circuits: how transcriptional silencing and counter-silencing facilitate bacterial evolution
journal, February 2015

  • Will, W. Ryan; Navarre, William W.; Fang, Ferric C.
  • Current Opinion in Microbiology, Vol. 23
  • DOI: 10.1016/j.mib.2014.10.005

Identification of new members of the Escherichia coli K-12 MG1655 SlyA regulon
journal, March 2017

  • Curran, Thomas D.; Abacha, Fatima; Hibberd, Stephen P.
  • Microbiology, Vol. 163, Issue 3
  • DOI: 10.1099/mic.0.000423

XtalView/Xfit—A Versatile Program for Manipulating Atomic Coordinates and Electron Density
journal, April 1999

Chance and necessity in the genome evolution of endosymbiotic bacteria of insects
journal, March 2017

  • Sabater-Muñoz, Beatriz; Toft, Christina; Alvarez-Ponce, David
  • The ISME Journal, Vol. 11, Issue 6
  • DOI: 10.1038/ismej.2017.18

Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli.
journal, June 1995

A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist: Truncated H-NS protein from EPEC
journal, February 2005

NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995

  • Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
  • Journal of Biomolecular NMR, Vol. 6, Issue 3
  • DOI: 10.1007/BF00197809

Structural assignments to the Mycoplasma genitalium proteins show extensive gene duplications and domain rearrangements
journal, December 1998

  • Teichmann, S. A.; Park, J.; Chothia, C.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
  • DOI: 10.1073/pnas.95.25.14658

One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000

  • Datsenko, K. A.; Wanner, B. L.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
  • DOI: 10.1073/pnas.120163297

A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist: Truncated H-NS protein from EPEC
journal, December 2004

T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension
journal, May 2011

  • Di Tommaso, P.; Moretti, S.; Xenarios, I.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr245

MOLREP an Automated Program for Molecular Replacement
journal, December 1997

Recognition of Antimicrobial Peptides by a Bacterial Sensor Kinase
journal, August 2005

Emr, an Escherichia coli locus for multidrug resistance.
journal, October 1992

  • Lomovskaya, O.; Lewis, K.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 19
  • DOI: 10.1073/pnas.89.19.8938

Structural Basis for Intrinsic Thermosensing by the Master Virulence Regulator RovA of Yersinia
journal, August 2012

  • Quade, Nick; Mendonca, Chriselle; Herbst, Katharina
  • Journal of Biological Chemistry, Vol. 287, Issue 43
  • DOI: 10.1074/jbc.M112.379156

[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997

Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases
journal, January 2021

Gene regulatory network growth by duplication
journal, April 2004

  • Teichmann, Sarah A.; Babu, M. Madan
  • Nature Genetics, Vol. 36, Issue 5
  • DOI: 10.1038/ng1340

Characterization of SlyA in Shigella flexneri Identifies a Novel Role in Virulence
journal, February 2016

  • Weatherspoon-Griffin, Natasha; Wing, Helen J.
  • Infection and Immunity, Vol. 84, Issue 4
  • DOI: 10.1128/IAI.00806-15

Gene duplications in H. influenzae
journal, November 1995

  • Brenner, Steven E.; Hubbard, Tim; Murzin, Alexey
  • Nature, Vol. 378, Issue 6553
  • DOI: 10.1038/378140a0

Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis.
journal, January 1997

Expression during Host Infection and Localization of Yersinia pestis Autotransporter Proteins
text, January 2011

  • L., Miller, V.; M., Palacios,; B., Lawrenz, M.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/8kyg-ak46

Swiss-model : an automated protein homology-modeling server
text, January 2003

Recognition of Antimicrobial Peptides by a Bacterial Sensor Kinase
journal, August 2005

An Infection-Relevant Transcriptomic Compendium for Salmonella enterica Serovar Typhimurium
journal, December 2013

Discrimination and Integration of Stress Signals by Pathogenic Bacteria
journal, August 2016

Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea
journal, December 2004

Regulation of Metabolic Pathways by MarR Family Transcription Factors
journal, January 2017

Integrated circuits: how transcriptional silencing and counter-silencing facilitate bacterial evolution
journal, February 2015

  • Will, W. Ryan; Navarre, William W.; Fang, Ferric C.
  • Current Opinion in Microbiology, Vol. 23
  • DOI: 10.1016/j.mib.2014.10.005

Structure of an OhrR-ohrA Operator Complex Reveals the DNA Binding Mechanism of the MarR Family
journal, October 2005

Activation of the Bacterial Sensor Kinase PhoQ by Acidic pH
journal, April 2007

Mg2+ as an Extracellular Signal: Environmental Regulation of Salmonella Virulence
journal, January 1996

The mar regulon: multiple resistance to antibiotics and other toxic chemicals
journal, October 1999

Chance and necessity in the genome evolution of endosymbiotic bacteria of insects
journal, March 2017

  • Sabater-Muñoz, Beatriz; Toft, Christina; Alvarez-Ponce, David
  • The ISME Journal, Vol. 11, Issue 6
  • DOI: 10.1038/ismej.2017.18

The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli
journal, November 2013

  • Hao, Ziyang; Lou, Hubing; Zhu, Rongfeng
  • Nature Chemical Biology, Vol. 10, Issue 1
  • DOI: 10.1038/nchembio.1380

Evolutionary expansion of a regulatory network by counter-silencing
journal, October 2014

  • Will, W. Ryan; Bale, Denise H.; Reid, Philip J.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6270

Gene regulatory network growth by duplication
journal, April 2004

  • Teichmann, Sarah A.; Babu, M. Madan
  • Nature Genetics, Vol. 36, Issue 5
  • DOI: 10.1038/ng1340

Design of stable and self-regulated microbial consortia for chemical synthesis
journal, March 2022

RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague
journal, August 2006

  • Cathelyn, J. S.; Crosby, S. D.; Lathem, W. W.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 36
  • DOI: 10.1073/pnas.0603456103

Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function
journal, February 2009

  • Osborne, S. E.; Walthers, D.; Tomljenovic, A. M.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 10
  • DOI: 10.1073/pnas.0811669106

Emr, an Escherichia coli locus for multidrug resistance.
journal, October 1992

  • Lomovskaya, O.; Lewis, K.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 19
  • DOI: 10.1073/pnas.89.19.8938

Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences.
journal, June 1995

  • Martin, R. G.; Rosner, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 12
  • DOI: 10.1073/pnas.92.12.5456

Structural assignments to the Mycoplasma genitalium proteins show extensive gene duplications and domain rearrangements
journal, December 1998

  • Teichmann, S. A.; Park, J.; Chothia, C.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
  • DOI: 10.1073/pnas.95.25.14658

Crystal Structures of SlyA Protein, a Master Virulence Regulator of Salmonella , in Free and DNA-bound States
journal, May 2011

  • Dolan, Kyle T.; Duguid, Erica M.; He, Chuan
  • Journal of Biological Chemistry, Vol. 286, Issue 25
  • DOI: 10.1074/jbc.m111.245258

SlyA Protein Activates fimB Gene Expression and Type 1 Fimbriation in Escherichia coli K-12
journal, July 2011

  • McVicker, Gareth; Sun, Lei; Sohanpal, Baljinder K.
  • Journal of Biological Chemistry, Vol. 286, Issue 37
  • DOI: 10.1074/jbc.m111.266619

Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica
journal, February 2008

  • Perez, J. Christian; Latifi, Tammy; Groisman, Eduardo A.
  • Journal of Biological Chemistry, Vol. 283, Issue 16
  • DOI: 10.1074/jbc.m709843200

T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension
journal, May 2011

  • Di Tommaso, P.; Moretti, S.; Xenarios, I.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr245

RegulonDB version 9.0: high-level integration of gene regulation, coexpression, motif clustering and beyond
journal, November 2015

  • Gama-Castro, Socorro; Salgado, Heladia; Santos-Zavaleta, Alberto
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1156

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2015

  • Caspi, Ron; Billington, Richard; Ferrer, Luciana
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1164

Assessment of phase accuracy by cross validation: the free R value. Methods and applications
journal, January 1993

  • Brünger, A. T.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 49, Issue 1
  • DOI: 10.1107/s0907444992007352

The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome
journal, October 2007

SlyA Regulates Type III Secretion System (T3SS) Genes in Parallel with the T3SS Master Regulator HrpL in Dickeya dadantii 3937
journal, January 2012

  • Zou, Lifang; Zeng, Quan; Lin, Haiping
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/aem.07021-11

Ferrioxamine-Mediated Iron(III) Utilization by Salmonella enterica
journal, April 1999

A Novel Autotransporter Adhesin Is Required for Efficient Colonization during Bubonic Plague
journal, October 2008

  • Lawrenz, Matthew B.; Lenz, Jonathan D.; Miller, Virginia L.
  • Infection and Immunity, Vol. 77, Issue 1
  • DOI: 10.1128/iai.01206-08

Comparative Analysis of the Regulation of rovA from the Pathogenic Yersiniae
journal, June 2007

  • Lawrenz, Matthew B.; Miller, Virginia L.
  • Journal of Bacteriology, Vol. 189, Issue 16
  • DOI: 10.1128/jb.00528-07

H-NS Represses inv Transcription in Yersinia enterocolitica through Competition with RovA and Interaction with YmoA
journal, July 2006

  • Ellison, Damon W.; Miller, Virginia L.
  • Journal of Bacteriology, Vol. 188, Issue 14
  • DOI: 10.1128/jb.00862-05

SlyA, a MarR Family Transcriptional Regulator, Is Essential for Virulence in Dickeya dadantii 3937
journal, November 2009

  • Haque, M. Manjurul; Kabir, M. Shahinur; Aini, Luqman Qurata
  • Journal of Bacteriology, Vol. 191, Issue 22
  • DOI: 10.1128/jb.01205-09

Where To Begin? Mapping Transcription Start Sites Genome-Wide in Escherichia coli
journal, January 2015

Expression during Host Infection and Localization of Yersinia pestis Autotransporter Proteins
journal, August 2011

  • Lenz, J. D.; Lawrenz, M. B.; Cotter, D. G.
  • Journal of Bacteriology, Vol. 193, Issue 21
  • DOI: 10.1128/jb.05877-11

Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway.
journal, January 1993

Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli.
journal, June 1995

EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB.
journal, January 1995

Regulation of Escherichia coli Hemolysin E Expression by H-NS and Salmonella SlyA
journal, March 2004

Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of Salmonella by Nitrate Respiration
journal, June 2012

  • Lopez, Christopher A.; Winter, Sebastian E.; Rivera-Chávez, Fabian
  • mBio, Vol. 3, Issue 3
  • DOI: 10.1128/mbio.00143-12

Phenolic Compounds and Their Role in Disease Resistance
journal, September 1992

An insight into misidentification of the small-subunit ribosomal RNA (18S rRNA) gene sequences of Theileria spp. as Theileria annulata
journal, December 2022

Swiss-model : an automated protein homology-modeling server
text, January 2003

    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

    MarR Family Transcription Factors from Burkholderia Species: Hidden Clues to Control of Virulence-Associated Genes
    journal, February 2019

    • Gupta, Ashish; Pande, Anuja; Sabrin, Afsana
    • Microbiology and Molecular Biology Reviews, Vol. 83, Issue 1
    • DOI: 10.1128/mmbr.00039-18

    The MarR-Type Regulator MalR Is Involved in Stress-Responsive Cell Envelope Remodeling in Corynebacterium glutamicum
    journal, May 2019

    SlyA Transcriptional Regulator Is Not Directly Affected by ppGpp Levels
    journal, August 2020

    • Bartoli, Julia; Viala, Julie Pamela; Bouveret, Emmanuelle
    • Frontiers in Microbiology, Vol. 11
    • DOI: 10.3389/fmicb.2020.01856
      Sort by:
      [ × clear filter / sort ]

      Figures / Tables found in this record:

      FIG 1 (p. 4)figure
      FIG. 2 (p. 5)figure
      FIG 3 (p. 6)figure
      FIG 4 (p. 8)figure
      FIG 5 (p. 9)figure
      FIG 6 (p. 11)figure
      FIG 7 (p. 12)figure
      FIG 8 (p. 14)figure
        [ × clear filter / sort ]
        Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

        Similar Records in DOE PAGES and OSTI.GOV collections: