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Title: Structural Basis for DNA Recognition by the Two-Component Response Regulator RcsB

Journal Article · · mBio
 [1];  [2];  [3];  [2];  [1];
  1. Center for Structural Genomics of Infectious Diseases, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA, Department of Biochemistry and Molecular Genetics, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
  2. Department of Microbiology and Immunology, Loyola University Chicago, Health Sciences Division, Stritch School of Medicine, Maywood, Illinois, USA
  3. Keck Biophysics Facility, Northwestern University, Evanston, Illinois, USA
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RcsB is a highly conserved transcription regulator of the Rcs phosphorelay system, a complex two-component signal transduction system (N. Majdalani and S. Gottesman, Annu Rev Microbiol 59:379–405, 2005; A. J. Wolfe, Curr Opin Microbiol 13:204–209, 2010,https://doi.org/10.1016/j.mib.2010.01.002; D. J. Clarke, Future Microbiol 5:1173–1184, 2010,https://doi.org/10.2217/fmb.10.83). RcsB plays an important role in virulence and pathogenicity in human hosts by regulating biofilm formation. RcsB can regulate transcription alone or together with its auxiliary transcription regulators by forming heterodimers. This complexity allows RcsB to regulate transcription of more than 600 bacterial genes in response to different stresses (D. Wang et al., Mol Plant Microbe Interact 25:6–17, 2012,https://doi.org/10.1094/MPMI-08-11-0207). Despite increasing knowledge of RcsB importance, molecular mechanisms that drive the ability of RcsB to control transcription of a large number of genes remain unclear. Here, we present crystal structures of unphosphorylated RcsB in complex with the consensus DNA-binding sequence of 22-mer (DNA22) and 18-mer (DNA18) of the flhDC operon from Escherichia coli determined at 3.15- and 3.37-Å resolution, respectively. The results of our structural analysis combined with the results of in vitro binding assays provide valuable insights to the protein regulatory mechanism, demonstrate how RcsB recognizes target DNA sequences, and reveal a unique oligomeric state that allows RcsB to form homo- and heterodimers. This information will help us understand the complex mechanisms of transcriptional regulation by RcsB in bacteria.

Research Organization:
Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Illinois at Urbana-Champaign, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); NIAID; National Institutes of Health (NIH); HHS
Grant/Contract Number:
SC0012443; NIH R01AI083640; NIH 2R01AI083640-06A1; R01AI083640; 2R01AI083640-06A1; AC02-06CH11357
OSTI ID:
1493948
Alternate ID(s):
OSTI ID: 1499720
Journal Information:
mBio, Journal Name: mBio Vol. 9 Journal Issue: 1; ISSN 2161-2129
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

References (29)

Salmonella Biofilm Development Depends on the Phosphorylation Status of RcsB journal May 2012
Crystal structure of nonphosphorylated receiver domain of the stress response regulator RcsB from Escherichia coli : X-Ray Structure of the RcsB Receiver Domain journal October 2016
Regulation and mode of action of the second small RNA activator of RpoS translation, RprA: RprA regulation and mode of action journal October 2002
Structure of the response regulator ChrA in the haem-sensing two-component system of Corynebacterium diphtheriae journal July 2015
The RcsAB Box: CHARACTERIZATION OF A NEW OPERATOR ESSENTIAL FOR THE REGULATION OF EXOPOLYSACCHARIDE BIOSYNTHESIS IN ENTERIC BACTERIA journal March 2000
RflM mediates target specificity of the RcsCDB phosphorelay system for transcriptional repression of flagellar synthesis in Salmonella enterica : Repression of journal June 2016
RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli: Regulation of flhDC by RcsB journal August 2003
Nε−Lysine Acetylation of a Bacterial Transcription Factor Inhibits Its DNA-Binding Activity journal December 2010
Dali server: conservation mapping in 3D journal May 2010
Transcriptional regulation by BglJ–RcsB, a pleiotropic heteromeric activator in Escherichia coli journal December 2013
DNA-binding proteins journal September 1983
Structure of the Escherichia coli Response Regulator NarL † , ‡ journal January 1996
An asymmetric heterodomain interface stabilizes a response regulator–DNA complex journal February 2014
Phosphorylation-dependent conformational changes and domain rearrangements in Staphylococcus aureus VraR activation journal May 2013
Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay journal August 2006
Fine-structure mapping and identification of two regulators of capsule synthesis in Escherichia coli K-12. journal June 1988
The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae journal April 2008
Genome Expression Analyses Revealing the Modulation of the Salmonella Rcs Regulon by the Attenuator IgaA journal January 2009
Signal transduction in bacteria: molecular mechanisms of stimulus—response coupling journal April 1998
Detecting Envelope Stress by Monitoring β-Barrel Assembly journal December 2014
Dimerization allows DNA target site recognition by the NarL response regulator journal September 2002
Acid stress response in Escherichia coli: mechanism of regulation of gadA transcription by RcsB and GadE journal February 2010
Non-canonical activation of OmpR drives acid and osmotic stress responses in single bacterial cells journal November 2017
Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA journal June 2002
Structural basis of DNA sequence recognition by the response regulator PhoP in Mycobacterium tuberculosis journal April 2016
Interaction of the RcsB Response Regulator with Auxiliary Transcription Regulators in Escherichia coli journal December 2015
Structural Analysis of the DNA-binding Domain of the Erwinia amylovora RcsB Protein and Its Interaction with the RcsAB Box journal March 2003
Acetylation of the Response Regulator RcsB Controls Transcription from a Small RNA Promoter journal July 2013
Identification of an RcsA/RcsB Recognition Motif in the Promoters of Exopolysaccharide Biosynthetic Operons from Erwinia amylovora and Pantoea stewartii Subspecies stewartii journal February 1999

Figures / Tables (2)

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