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

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.

doi:10.1128/mbio.00009-19

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

Journal Article · Mon Mar 04 23:00:00 EST 2019 · mBio (Online)

DOI:https://doi.org/10.1128/mbio.00009-19· OSTI ID:1626076

Will, W. Ryan ^[1]; Brzovic, Peter ^[2]; Le Trong, Isolde ^[3]; Stenkamp, Ronald E. ^[4]; Lawrenz, Matthew B. ^[5]; Karlinsey, Joyce E. ^[6]; Navarre, William W. ^[6]; Main-Hester, Kara ^[6]; Miller, Virginia L. ^[7]; Libby, Stephen J. ^[8]; ^[9]; Freitag, Nancy E. ^[10]

Univ. of Washington, Seattle, WA (United States). Dept. of Laboratory Medicine; DOE/OSTI
Univ. of Washington, Seattle, WA (United States). Dept. of Biochemistry
Univ. of Washington, Seattle, WA (United States). Dept. of Biological Structure
Univ. of Washington, Seattle, WA (United States). Dept. of Biochemistry Univ. of Washington, Seattle, WA (United States). Dept. of Biological Structure
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
Univ. of Washington, Seattle, WA (United States). Dept. of Microbiology
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
Univ. of Washington, Seattle, WA (United States). Dept. of Medicine
Univ. of Washington, Seattle, WA (United States). Dept. of Laboratory Medicine; Univ. of Washington, Seattle, WA (United States). Dept. of Microbiology
Univ. of Illinois, Chicago, IL (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Cancer Institute; National Institute of General Medical Sciences

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1626076

Alternate ID(s):: OSTI ID: 1834805

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 10; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (120)

Coordinated and differential expression of histone-like proteins in Escherichia coli: regulation and function of the H-NS analog StpA. Sonden, B.; Uhlin, B. E. The EMBO Journal, Vol. 15, Issue 18 https://doi.org/10.1002/j.1460-2075.1996.tb00877.x	journal	September 1996
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/bf00197809	journal	November 1995
NMR View: A computer program for the visualization and analysis of NMR data Johnson, Bruce A.; Blevins, Richard A. Journal of Biomolecular NMR, Vol. 4, Issue 5 https://doi.org/10.1007/bf00404272	journal	September 1994
Recognition of Antimicrobial Peptides by a Bacterial Sensor Kinase Bader, Martin W.; Sanowar, Sarah; Daley, Margaret E. Cell, Vol. 122, Issue 3 https://doi.org/10.1016/j.cell.2005.05.030	journal	August 2005
An Infection-Relevant Transcriptomic Compendium for Salmonella enterica Serovar Typhimurium Kröger, Carsten; Colgan, Aoife; Srikumar, Shabarinath Cell Host & Microbe, Vol. 14, Issue 6 https://doi.org/10.1016/j.chom.2013.11.010	journal	December 2013
Discrimination and Integration of Stress Signals by Pathogenic Bacteria Fang, Ferric C.; Frawley, Elaine R.; Tapscott, Timothy Cell Host & Microbe, Vol. 20, Issue 2 https://doi.org/10.1016/j.chom.2016.07.010	journal	August 2016
Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea Pérez-Rueda, Ernesto; Collado-Vides, Julio; Segovia, Lorenzo Computational Biology and Chemistry, Vol. 28, Issue 5-6 https://doi.org/10.1016/j.compbiolchem.2004.09.004	journal	December 2004
Regulation of Metabolic Pathways by MarR Family Transcription Factors Grove, Anne Computational and Structural Biotechnology Journal, Vol. 15 https://doi.org/10.1016/j.csbj.2017.06.001	journal	January 2017
Structural Insight on the Mechanism of Regulation of the MarR Family of Proteins: High-Resolution Crystal Structure of a Transcriptional Repressor from Methanobacterium thermoautotrophicum Saridakis, Vivian; Shahinas, Dea; Xu, Xiaohui Journal of Molecular Biology, Vol. 377, Issue 3 https://doi.org/10.1016/j.jmb.2008.01.001	journal	March 2008
Integrated circuits: how transcriptional silencing and counter-silencing facilitate bacterial evolution Will, W. Ryan; Navarre, William W.; Fang, Ferric C. Current Opinion in Microbiology, Vol. 23 https://doi.org/10.1016/j.mib.2014.10.005	journal	February 2015
Structure of an OhrR-ohrA Operator Complex Reveals the DNA Binding Mechanism of the MarR Family Hong, Minsun; Fuangthong, Mayuree; Helmann, John D. Molecular Cell, Vol. 20, Issue 1 https://doi.org/10.1016/j.molcel.2005.09.013	journal	October 2005
Activation of the Bacterial Sensor Kinase PhoQ by Acidic pH Prost, Lynne R.; Daley, Margaret E.; Le Sage, Valerie Molecular Cell, Vol. 26, Issue 2 https://doi.org/10.1016/j.molcel.2007.03.008	journal	April 2007
Mg2+ as an Extracellular Signal: Environmental Regulation of Salmonella Virulence Véscovi, Eleonora García; Soncini, Fernando C.; Groisman, Eduardo A. Cell, Vol. 84, Issue 1 https://doi.org/10.1016/s0092-8674(00)81003-x	journal	January 1996
A set of temperature sensitive-replication/-segregation and temperature resistant plasmid vectors with different copy numbers and in an isogenic background (chloramphenicol, kanamycin, lacZ, repA, par, polA) Hashimoto-Gotoh, Tamotsu; Yamaguchi, Miki; Yasojima, Koji Gene, Vol. 241, Issue 1 https://doi.org/10.1016/s0378-1119(99)00434-5	journal	January 2000
The mar regulon: multiple resistance to antibiotics and other toxic chemicals Alekshun, Michael N.; Levy, Stuart B. Trends in Microbiology, Vol. 7, Issue 10 https://doi.org/10.1016/s0966-842x(99)01589-9	journal	October 1999
Chance and necessity in the genome evolution of endosymbiotic bacteria of insects Sabater-Muñoz, Beatriz; Toft, Christina; Alvarez-Ponce, David The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.18	journal	March 2017
The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli Hao, Ziyang; Lou, Hubing; Zhu, Rongfeng Nature Chemical Biology, Vol. 10, Issue 1 https://doi.org/10.1038/nchembio.1380	journal	November 2013
Evolutionary expansion of a regulatory network by counter-silencing Will, W. Ryan; Bale, Denise H.; Reid, Philip J. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6270	journal	October 2014
Gene regulatory network growth by duplication Teichmann, Sarah A.; Babu, M. Madan Nature Genetics, Vol. 36, Issue 5 https://doi.org/10.1038/ng1340	journal	April 2004
Design of stable and self-regulated microbial consortia for chemical synthesis Li, Xianglai; Zhou, Zhao; Li, Wenna Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29215-6	journal	March 2022
The Rap and Hor proteins of Erwinia, Serratia and Yersinia : a novel subgroup in a growing superfamily of proteins regulating diverse physiological processes in bacterial pathogens Thomson, N. R.; Cox, A.; Bycroft, B. W. Molecular Microbiology, Vol. 26, Issue 3 https://doi.org/10.1046/j.1365-2958.1997.5981976.x	journal	October 1997
RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague Cathelyn, J. S.; Crosby, S. D.; Lathem, W. W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 36 https://doi.org/10.1073/pnas.0603456103	journal	August 2006
Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function Osborne, S. E.; Walthers, D.; Tomljenovic, A. M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 10 https://doi.org/10.1073/pnas.0811669106	journal	February 2009
Emr, an Escherichia coli locus for multidrug resistance. Lomovskaya, O.; Lewis, K. Proceedings of the National Academy of Sciences, Vol. 89, Issue 19 https://doi.org/10.1073/pnas.89.19.8938	journal	October 1992
Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences. Martin, R. G.; Rosner, J. L. Proceedings of the National Academy of Sciences, Vol. 92, Issue 12 https://doi.org/10.1073/pnas.92.12.5456	journal	June 1995
Structural assignments to the Mycoplasma genitalium proteins show extensive gene duplications and domain rearrangements Teichmann, S. A.; Park, J.; Chothia, C. Proceedings of the National Academy of Sciences, Vol. 95, Issue 25 https://doi.org/10.1073/pnas.95.25.14658	journal	December 1998
Crystal Structures of SlyA Protein, a Master Virulence Regulator of Salmonella , in Free and DNA-bound States Dolan, Kyle T.; Duguid, Erica M.; He, Chuan Journal of Biological Chemistry, Vol. 286, Issue 25 https://doi.org/10.1074/jbc.m111.245258	journal	May 2011
SlyA Protein Activates fimB Gene Expression and Type 1 Fimbriation in Escherichia coli K-12 McVicker, Gareth; Sun, Lei; Sohanpal, Baljinder K. Journal of Biological Chemistry, Vol. 286, Issue 37 https://doi.org/10.1074/jbc.m111.266619	journal	July 2011
SlyA and H-NS Regulate Transcription of the Escherichia coli K5 Capsule Gene Cluster, and Expression of slyA in Escherichia coli Is Temperature-dependent, Positively Autoregulated, and Independent of H-NS Corbett, David; Bennett, Hayley J.; Askar, Hamdia Journal of Biological Chemistry, Vol. 282, Issue 46 https://doi.org/10.1074/jbc.m703465200	journal	September 2007
Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica Perez, J. Christian; Latifi, Tammy; Groisman, Eduardo A. Journal of Biological Chemistry, Vol. 283, Issue 16 https://doi.org/10.1074/jbc.m709843200	journal	February 2008
T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension Di Tommaso, P.; Moretti, S.; Xenarios, I. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr245	journal	May 2011
RegulonDB version 9.0: high-level integration of gene regulation, coexpression, motif clustering and beyond Gama-Castro, Socorro; Salgado, Heladia; Santos-Zavaleta, Alberto Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1156	journal	November 2015
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Caspi, Ron; Billington, Richard; Ferrer, Luciana Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1164	journal	November 2015
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/s0907444904019158	journal	November 2004
Assessment of phase accuracy by cross validation: the free R value. Methods and applications Brünger, A. T. Acta Crystallographica Section D Biological Crystallography, Vol. 49, Issue 1 https://doi.org/10.1107/s0907444992007352	journal	January 1993
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/s0907444994003112	journal	September 1994
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/s0907444996012255	journal	May 1997
RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis: H-NS-mediated silencing of rovA and inv expression in Yersinia Heroven, Ann Kathrin; Nagel, Geraldine; Tran, Hien J. Molecular Microbiology, Vol. 53, Issue 3 https://doi.org/10.1111/j.1365-2958.2004.04162.x	journal	June 2004
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 Cathelyn, Jason S.; Ellison, Damon W.; Hinchliffe, Stewart J. Molecular Microbiology, Vol. 66, Issue 1 https://doi.org/10.1111/j.1365-2958.2007.05907.x	journal	October 2007
SlyA Regulates Type III Secretion System (T3SS) Genes in Parallel with the T3SS Master Regulator HrpL in Dickeya dadantii 3937 Zou, Lifang; Zeng, Quan; Lin, Haiping Applied and Environmental Microbiology, Vol. 78, Issue 8 https://doi.org/10.1128/aem.07021-11	journal	January 2012
Ferrioxamine-Mediated Iron(III) Utilization by Salmonella enterica Kingsley, Robert A.; Reissbrodt, Rolf; Rabsch, Wolfgang Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/aem.65.4.1610-1618.1999	journal	April 1999
A Novel Autotransporter Adhesin Is Required for Efficient Colonization during Bubonic Plague Lawrenz, Matthew B.; Lenz, Jonathan D.; Miller, Virginia L. Infection and Immunity, Vol. 77, Issue 1 https://doi.org/10.1128/iai.01206-08	journal	October 2008
Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid Bölin, I.; Norlander, L.; Wolf-Watz, H. Infection and Immunity, Vol. 37, Issue 2 https://doi.org/10.1128/iai.37.2.506-512.1982	journal	August 1982
Comparative Analysis of the Regulation of rovA from the Pathogenic Yersiniae Lawrenz, Matthew B.; Miller, Virginia L. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/jb.00528-07	journal	June 2007
H-NS Represses inv Transcription in Yersinia enterocolitica through Competition with RovA and Interaction with YmoA Ellison, Damon W.; Miller, Virginia L. Journal of Bacteriology, Vol. 188, Issue 14 https://doi.org/10.1128/jb.00862-05	journal	July 2006
SlyA, a MarR Family Transcriptional Regulator, Is Essential for Virulence in Dickeya dadantii 3937 Haque, M. Manjurul; Kabir, M. Shahinur; Aini, Luqman Qurata Journal of Bacteriology, Vol. 191, Issue 22 https://doi.org/10.1128/jb.01205-09	journal	November 2009
Where To Begin? Mapping Transcription Start Sites Genome-Wide in Escherichia coli Wade, Joseph T. Journal of Bacteriology, Vol. 197, Issue 1 https://doi.org/10.1128/jb.02410-14	journal	January 2015
Expression during Host Infection and Localization of Yersinia pestis Autotransporter Proteins Lenz, J. D.; Lawrenz, M. B.; Cotter, D. G. Journal of Bacteriology, Vol. 193, Issue 21 https://doi.org/10.1128/jb.05877-11	journal	August 2011
Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline George, A. M.; Levy, S. B. Journal of Bacteriology, Vol. 155, Issue 2 https://doi.org/10.1128/jb.155.2.531-540.1983	journal	August 1983
Early and late responses of TOL promoters to pathway inducers: identification of postexponential promoters in Pseudomonas putida with lacZ-tet bicistronic reporters. de Lorenzo, V.; Cases, I.; Herrero, M. Journal of Bacteriology, Vol. 175, Issue 21 https://doi.org/10.1128/jb.175.21.6902-6907.1993	journal	January 1993
Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway. Cohen, S. P.; Levy, S. B.; Foulds, J. Journal of Bacteriology, Vol. 175, Issue 24 https://doi.org/10.1128/jb.175.24.7856-7862.1993	journal	January 1993
Plasmids bearing hfq and the hns-like gene stpA complement hns mutants in modulating arginine decarboxylase gene expression in Escherichia coli. Shi, X.; Bennett, G. N. Journal of Bacteriology, Vol. 176, Issue 21 https://doi.org/10.1128/jb.176.21.6769-6775.1994	journal	January 1994
Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. Seoane, A. S.; Levy, S. B. Journal of Bacteriology, Vol. 177, Issue 12 https://doi.org/10.1128/jb.177.12.3414-3419.1995	journal	June 1995
EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. Lomovskaya, O.; Lewis, K.; Matin, A. Journal of bacteriology, Vol. 177, Issue 9 https://doi.org/10.1128/jb.177.9.2328-2334.1995	journal	January 1995
Genome Size Determination and Coding Capacity of Sodalis glossinidius, an Enteric Symbiont of Tsetse Flies, as Revealed by Hybridization to Escherichia coliGene Arrays Akman, Leyla; Rio, Rita V. M.; Beard, Charles B. Journal of Bacteriology, Vol. 183, Issue 15 https://doi.org/10.1128/jb.183.15.4517-4525.2001	journal	August 2001
Regulation of Escherichia coli Hemolysin E Expression by H-NS and Salmonella SlyA Wyborn, Neil R.; Stapleton, Melanie R.; Norte, Valia A. Journal of Bacteriology, Vol. 186, Issue 6 https://doi.org/10.1128/jb.186.6.1620-1628.2004	journal	March 2004
Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of Salmonella by Nitrate Respiration Lopez, Christopher A.; Winter, Sebastian E.; Rivera-Chávez, Fabian mBio, Vol. 3, Issue 3 https://doi.org/10.1128/mbio.00143-12	journal	June 2012
Phenolic Compounds and Their Role in Disease Resistance Nicholson, R. L.; Hammerschmidt, R. Annual Review of Phytopathology, Vol. 30, Issue 1 https://doi.org/10.1146/annurev.py.30.090192.002101	journal	September 1992
An insight into misidentification of the small-subunit ribosomal RNA (18S rRNA) gene sequences of Theileria spp. as Theileria annulata Nehra, Anil Kumar; Kumari, Ansu; Moudgil, Aman Dev BMC Veterinary Research, Vol. 18, Issue 1 https://doi.org/10.1186/s12917-022-03540-w	journal	December 2022
Swiss-model : an automated protein homology-modeling server Schwede, T.; Kopp, J.; Guex, N. Oxford University Press https://doi.org/10.5451/unibas-ep3388	text	January 2003
Chromatin Immunoprecipitation for Determining the Association of Proteins with Specific Genomic Sequences In Vivo Aparicio, Oscar; Geisberg, Joseph V.; Sekinger, Edward Current Protocols in Molecular Biology, Vol. 69, Issue 1 https://doi.org/10.1002/0471142727.mb2103s69	journal	January 2005
XtalView/Xfit—A Versatile Program for Manipulating Atomic Coordinates and Electron Density McRee, Duncan E. Journal of Structural Biology, Vol. 125, Issue 2-3 https://doi.org/10.1006/jsbi.1999.4094	journal	April 1999
Evolution by Gene Duplication Ohno, Susumu Springer Berlin, Heidelberg https://doi.org/10.1007/978-3-642-86659-3	book	January 1970
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
NMR View: A computer program for the visualization and analysis of NMR data Johnson, Bruce A.; Blevins, Richard A. Journal of Biomolecular NMR, Vol. 4, Issue 5 https://doi.org/10.1007/BF00404272	journal	September 1994
An umbra-related virus found in babaco (Vasconcellea × heilbornii) Cornejo-Franco, Juan F.; Flores, Francisco; Mollov, Dimitre Archives of Virology, Vol. 166, Issue 8 https://doi.org/10.1007/s00705-021-05117-8	journal	May 2021
Structural characterization of the DNA-binding mechanism underlying the copper(II)-sensing MarR transcriptional regulator Zhu, Rongfeng; Hao, Ziyang; Lou, Hubing JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 5 https://doi.org/10.1007/s00775-017-1442-7	journal	January 2017
Identification and expression of the BAHD family during development, ripening, and stress response in banana Xu, Yun; Tie, Weiwei; Yan, Yan Molecular Biology Reports, Vol. 48, Issue 2 https://doi.org/10.1007/s11033-020-06132-9	journal	January 2021
Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli Amann, Egon; Ochs, Birgit; Abel, Karl-Josef Gene, Vol. 69, Issue 2, p. 301-315 https://doi.org/10.1016/0378-1119(88)90440-4	journal	September 1988
Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli No authors listed Gene, Vol. 100 https://doi.org/10.1016/0378-1119(91)90366-J	journal	April 1991
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
[26] Raster3D: Photorealistic molecular graphics Merritt, Ethan A.; Bacon, David J. Methods in Enzymology https://doi.org/10.1016/S0076-6879(97)77028-9	book	January 1997
Mg2+ as an Extracellular Signal: Environmental Regulation of Salmonella Virulence Véscovi, Eleonora García; Soncini, Fernando C.; Groisman, Eduardo A. Cell, Vol. 84, Issue 1 https://doi.org/10.1016/S0092-8674(00)81003-X	journal	January 1996
A set of temperature sensitive-replication/-segregation and temperature resistant plasmid vectors with different copy numbers and in an isogenic background (chloramphenicol, kanamycin, lacZ, repA, par, polA) Hashimoto-Gotoh, Tamotsu; Yamaguchi, Miki; Yasojima, Koji Gene, Vol. 241, Issue 1 https://doi.org/10.1016/S0378-1119(99)00434-5	journal	January 2000
The mar regulon: multiple resistance to antibiotics and other toxic chemicals Alekshun, Michael N.; Levy, Stuart B. Trends in Microbiology, Vol. 7, Issue 10 https://doi.org/10.1016/S0966-842X(99)01589-9	journal	October 1999
Gene duplications in H. influenzae Brenner, Steven E.; Hubbard, Tim; Murzin, Alexey Nature, Vol. 378, Issue 6553 https://doi.org/10.1038/378140a0	journal	November 1995
Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases Nagata, Takuya; Shinya, Shoko; Ohnuma, Takayuki Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-81903-3	journal	January 2021
A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence: Y. enterocolitica regulator of inv and virulence Revell, Paula A.; Miller, Virginia L. Molecular Microbiology, Vol. 35, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.01740.x	journal	February 2000
Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis Chain, P. S. G.; Carniel, E.; Larimer, F. W. Proceedings of the National Academy of Sciences, Vol. 101, Issue 38 https://doi.org/10.1073/pnas.0404012101	journal	September 2004
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Datsenko, K. A.; Wanner, B. L. Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645 https://doi.org/10.1073/pnas.120163297	journal	May 2000
Crystal Structures of SlyA Protein, a Master Virulence Regulator of Salmonella , in Free and DNA-bound States Dolan, Kyle T.; Duguid, Erica M.; He, Chuan Journal of Biological Chemistry, Vol. 286, Issue 25 https://doi.org/10.1074/jbc.M111.245258	journal	May 2011
SlyA Protein Activates fimB Gene Expression and Type 1 Fimbriation in Escherichia coli K-12 McVicker, Gareth; Sun, Lei; Sohanpal, Baljinder K. Journal of Biological Chemistry, Vol. 286, Issue 37 https://doi.org/10.1074/jbc.M111.266619	journal	July 2011
Structural Basis for Intrinsic Thermosensing by the Master Virulence Regulator RovA of Yersinia Quade, Nick; Mendonca, Chriselle; Herbst, Katharina Journal of Biological Chemistry, Vol. 287, Issue 43 https://doi.org/10.1074/jbc.M112.379156	journal	August 2012
Analysis of RovA, a Transcriptional Regulator of Yersinia pseudotuberculosis Virulence That Acts through Antirepression and Direct Transcriptional Activation Tran, Hien J.; Heroven, Ann Kathrin; Winkler, Lars Journal of Biological Chemistry, Vol. 280, Issue 51 https://doi.org/10.1074/jbc.M504464200	journal	October 2005
SlyA and H-NS Regulate Transcription of the Escherichia coli K5 Capsule Gene Cluster, and Expression of slyA in Escherichia coli Is Temperature-dependent, Positively Autoregulated, and Independent of H-NS Corbett, David; Bennett, Hayley J.; Askar, Hamdia Journal of Biological Chemistry, Vol. 282, Issue 46 https://doi.org/10.1074/jbc.M703465200	journal	September 2007
Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica Perez, J. Christian; Latifi, Tammy; Groisman, Eduardo A. Journal of Biological Chemistry, Vol. 283, Issue 16 https://doi.org/10.1074/jbc.M709843200	journal	February 2008
Molecular Mechanisms of Ligand-Mediated Attenuation of DNA Binding by MarR Family Transcriptional Regulators Perera, I. C.; Grove, A. Journal of Molecular Cell Biology, Vol. 2, Issue 5 https://doi.org/10.1093/jmcb/mjq021	journal	August 2010
An Improved General Amino Acid Replacement Matrix Le, S. Q.; Gascuel, O. Molecular Biology and Evolution, Vol. 25, Issue 7 https://doi.org/10.1093/molbev/msn067	journal	April 2008
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
SWISS-MODEL: an automated protein homology-modeling server Schwede, T. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg520	journal	July 2003
RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more Salgado, Heladia; Peralta-Gil, Martin; Gama-Castro, Socorro Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1201	journal	November 2012
Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans Dale, Colin; Maudlin, Ian International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 1 https://doi.org/10.1099/00207713-49-1-267	journal	January 1999
Identification of new members of the Escherichia coli K-12 MG1655 SlyA regulon Curran, Thomas D.; Abacha, Fatima; Hibberd, Stephen P. Microbiology, Vol. 163, Issue 3 https://doi.org/10.1099/mic.0.000423	journal	March 2017
MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures Kraulis, P. J. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S0021889891004399	journal	October 1991
MOLREP an Automated Program for Molecular Replacement Vagin, A.; Teplyakov, A. Journal of Applied Crystallography, Vol. 30, Issue 6, p. 1022-1025 https://doi.org/10.1107/S0021889897006766	journal	December 1997
Improved Fourier coefficients for maps using phases from partial structures with errors Read, R. J. Acta Crystallographica Section A Foundations of Crystallography, Vol. 42, Issue 3 https://doi.org/10.1107/S0108767386099622	journal	May 1986
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Assessment of phase accuracy by cross validation: the free R value. Methods and applications Brünger, A. T. Acta Crystallographica Section D Biological Crystallography, Vol. 49, Issue 1 https://doi.org/10.1107/S0907444992007352	journal	January 1993
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist: Truncated H-NS protein from EPEC Williamson, Helen S.; Free, Andrew Molecular Microbiology, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-2958.2004.04421.x	journal	December 2004
Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ: Co-regulation by SlyA and PhoP/PhoQ in S. Typhimurium Navarre, William Wiley; Halsey, Thomas A.; Walthers, Don Molecular Microbiology, Vol. 56, Issue 2 https://doi.org/10.1111/j.1365-2958.2005.04553.x	journal	February 2005
A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist: Truncated H-NS protein from EPEC Williamson, Helen S.; Free, Andrew Molecular Microbiology, Vol. 56, Issue 2 https://doi.org/10.1111/j.1365-2958.2005.04569.x	journal	February 2005
Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12 Lithgow, James K.; Haider, Fouzia; Roberts, Ian S. Molecular Microbiology, Vol. 66, Issue 3 https://doi.org/10.1111/j.1365-2958.2007.05950.x	journal	November 2007
SlyA Regulates Type III Secretion System (T3SS) Genes in Parallel with the T3SS Master Regulator HrpL in Dickeya dadantii 3937 Zou, Lifang; Zeng, Quan; Lin, Haiping Applied and Environmental Microbiology, Vol. 78, Issue 8 https://doi.org/10.1128/AEM.07021-11	journal	January 2012
Ferrioxamine-Mediated Iron(III) Utilization by Salmonella enterica Kingsley, Robert A.; Reissbrodt, Rolf; Rabsch, Wolfgang Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1610-1618.1999	journal	April 1999
Characterization of SlyA in Shigella flexneri Identifies a Novel Role in Virulence Weatherspoon-Griffin, Natasha; Wing, Helen J. Infection and Immunity, Vol. 84, Issue 4 https://doi.org/10.1128/IAI.00806-15	journal	February 2016
A Novel Autotransporter Adhesin Is Required for Efficient Colonization during Bubonic Plague Lawrenz, Matthew B.; Lenz, Jonathan D.; Miller, Virginia L. Infection and Immunity, Vol. 77, Issue 1 https://doi.org/10.1128/IAI.01206-08	journal	October 2008
SlyA, a MarR Family Transcriptional Regulator, Is Essential for Virulence in Dickeya dadantii 3937 Haque, M. M.; Kabir, M. S.; Aini, L. Q. Journal of Bacteriology, Vol. 191, Issue 17 https://doi.org/10.1128/JB.00240-09	journal	June 2009
Comparative Analysis of the Regulation of rovA from the Pathogenic Yersiniae Lawrenz, Matthew B.; Miller, Virginia L. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/JB.00528-07	journal	June 2007
H-NS Represses inv Transcription in Yersinia enterocolitica through Competition with RovA and Interaction with YmoA Ellison, Damon W.; Miller, Virginia L. Journal of Bacteriology, Vol. 188, Issue 14 https://doi.org/10.1128/JB.00862-05	journal	July 2006
Global Transcriptional Start Site Mapping Using Differential RNA Sequencing Reveals Novel Antisense RNAs in Escherichia coli Thomason, Maureen K.; Bischler, Thorsten; Eisenbart, Sara K. Journal of Bacteriology, Vol. 197, Issue 1 https://doi.org/10.1128/JB.02096-14	journal	September 2014
Expression during Host Infection and Localization of Yersinia pestis Autotransporter Proteins Lenz, J. D.; Lawrenz, M. B.; Cotter, D. G. Journal of Bacteriology, Vol. 193, Issue 21 https://doi.org/10.1128/JB.05877-11	journal	August 2011
Genome Size Determination and Coding Capacity of Sodalis glossinidius, an Enteric Symbiont of Tsetse Flies, as Revealed by Hybridization to Escherichia coliGene Arrays Akman, Leyla; Rio, Rita V. M.; Beard, Charles B. Journal of Bacteriology, Vol. 183, Issue 15 https://doi.org/10.1128/JB.183.15.4517-4525.2001	journal	August 2001
Regulation of Escherichia coli Hemolysin E Expression by H-NS and Salmonella SlyA Wyborn, Neil R.; Stapleton, Melanie R.; Norte, Valia A. Journal of Bacteriology, Vol. 186, Issue 6 https://doi.org/10.1128/JB.186.6.1620-1628.2004	journal	March 2004
Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Merriam, J. J.; Mathur, R.; Maxfield-Boumil, R. Infection and immunity, Vol. 65, Issue 6 https://doi.org/10.1128/iai.65.6.2497-2501.1997	journal	January 1997
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. Guzman, L. M.; Belin, D.; Carson, M. J. Journal of Bacteriology, Vol. 177, Issue 14, p. 4121-4130 https://doi.org/10.1128/jb.177.14.4121-4130.1995	journal	July 1995
Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of Salmonella by Nitrate Respiration Lopez, Christopher A.; Winter, Sebastian E.; Rivera-Chávez, Fabian mBio, Vol. 3, Issue 3 https://doi.org/10.1128/mBio.00143-12	journal	June 2012
FRUIT, a Scar-Free System for Targeted Chromosomal Mutagenesis, Epitope Tagging, and Promoter Replacement in Escherichia coli and Salmonella enterica Stringer, Anne M.; Singh, Navjot; Yermakova, Anastasiya PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044841	journal	September 2012
Expression during Host Infection and Localization of Yersinia pestis Autotransporter Proteins L., Miller, V.; M., Palacios,; B., Lawrenz, M. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/8kyg-ak46	text	January 2011

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