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Title: Cell fate regulation governed by a repurposed bacterial histidine kinase

Abstract

One of the simplest organisms to divide asymmetrically is the bacterium Caulobacter crescentus. The DivL pseudo-histidine kinase, positioned at one cell pole, regulates cell-fate by controlling the activation of the global transcription factor CtrA via an interaction with the response regulator (RR) DivK. DivL uniquely contains a tyrosine at the histidine phosphorylation site, and can achieve these regulatory functions in vivo without kinase activity. Determination of the DivL crystal structure and biochemical analysis of wild-type and site-specific DivL mutants revealed that the DivL PAS domains regulate binding specificity for DivK~P over DivK, which is modulated by an allosteric intramolecular interaction between adjacent domains. We discovered that DivL's catalytic domains have been repurposed as a phosphospecific RR input sensor, thereby reversing the flow of information observed in conventional histidine kinase (HK)-RR systems and coupling a complex network of signaling proteins for cell-fate regulation.

Authors:
 [1];  [2];  [1];  [2];  [1];  [2];  [1];  [3]
  1. Stanford Univ. School of Medicine, Stanford, CA (United States)
  2. SLAC National Accelerator Laboratory, Menlo Park, CA (United States)
  3. Rutgers Univ., New Brunswick, NJ (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1213908
Grant/Contract Number:  
AC03-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online); Journal Volume: 12; Journal Issue: 10; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; phosphorylation; xylose; binding analysis; cell cycle and cell division; point mutation; crystal structure; caulobacter; histidine

Citation Formats

Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, and Stock, Ann M. Cell fate regulation governed by a repurposed bacterial histidine kinase. United States: N. p., 2014. Web. doi:10.1371/journal.pbio.1001979.
Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, & Stock, Ann M. Cell fate regulation governed by a repurposed bacterial histidine kinase. United States. https://doi.org/10.1371/journal.pbio.1001979
Childers, W. Seth, Xu, Qingping, Mann, Thomas H., Mathews, Irimpan I., Blair, Jimmy A., Deacon, Ashley M., Shapiro, Lucy, and Stock, Ann M. Tue . "Cell fate regulation governed by a repurposed bacterial histidine kinase". United States. https://doi.org/10.1371/journal.pbio.1001979. https://www.osti.gov/servlets/purl/1213908.
@article{osti_1213908,
title = {Cell fate regulation governed by a repurposed bacterial histidine kinase},
author = {Childers, W. Seth and Xu, Qingping and Mann, Thomas H. and Mathews, Irimpan I. and Blair, Jimmy A. and Deacon, Ashley M. and Shapiro, Lucy and Stock, Ann M.},
abstractNote = {One of the simplest organisms to divide asymmetrically is the bacterium Caulobacter crescentus. The DivL pseudo-histidine kinase, positioned at one cell pole, regulates cell-fate by controlling the activation of the global transcription factor CtrA via an interaction with the response regulator (RR) DivK. DivL uniquely contains a tyrosine at the histidine phosphorylation site, and can achieve these regulatory functions in vivo without kinase activity. Determination of the DivL crystal structure and biochemical analysis of wild-type and site-specific DivL mutants revealed that the DivL PAS domains regulate binding specificity for DivK~P over DivK, which is modulated by an allosteric intramolecular interaction between adjacent domains. We discovered that DivL's catalytic domains have been repurposed as a phosphospecific RR input sensor, thereby reversing the flow of information observed in conventional histidine kinase (HK)-RR systems and coupling a complex network of signaling proteins for cell-fate regulation.},
doi = {10.1371/journal.pbio.1001979},
journal = {PLoS Biology (Online)},
number = 10,
volume = 12,
place = {United States},
year = {Tue Oct 28 00:00:00 EDT 2014},
month = {Tue Oct 28 00:00:00 EDT 2014}
}

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Works referenced in this record:

Assembly of the Caulobacter cell division machine: Divisome assembly in Caulobacter
journal, May 2011


Distinct Constrictive Processes, Separated in Time and Space, Divide Caulobacter Inner and Outer Membranes
journal, October 2005


Fluorescence bleaching reveals asymmetric compartment formation prior to cell division in Caulobacter
journal, June 2003

  • Judd, Ellen M.; Ryan, Kathleen R.; Moerner, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 14
  • DOI: 10.1073/pnas.1433105100

Differential Localization of Two Histidine Kinases Controlling Bacterial Cell Differentiation
journal, November 1999


Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis
journal, April 2004

  • Ryan, K. R.; Huntwork, S.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 19
  • DOI: 10.1073/pnas.0402153101

Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle
journal, April 2002

  • Laub, M. T.; Chen, S. L.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 7
  • DOI: 10.1073/pnas.062065699

Interplay between the Localization and Kinetics of Phosphorylation in Flagellar Pole Development of the Bacterium Caulobacter crescentus
journal, August 2012


Allosteric Regulation of Histidine Kinases by Their Cognate Response Regulator Determines Cell Fate
journal, May 2008


The Asymmetric Spatial Distribution of Bacterial Signal Transduction Proteins Coordinates Cell Cycle Events
journal, July 2003


Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle
journal, March 2001

  • Jacobs, C.; Hung, D.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 7
  • DOI: 10.1073/pnas.051609998

DivL Performs Critical Cell Cycle Functions in Caulobacter crescentus Independent of Kinase Activity
journal, September 2007

  • Reisinger, Sarah J.; Huntwork, Sarah; Viollier, Patrick H.
  • Journal of Bacteriology, Vol. 189, Issue 22
  • DOI: 10.1128/JB.00868-07

A Dynamic Complex of Signaling Proteins Uses Polar Localization to Regulate Cell-Fate Asymmetry in Caulobacter crescentus
journal, March 2011


A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade
journal, October 2008

  • Iniesta, A. A.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 43
  • DOI: 10.1073/pnas.0808807105

Cell pole-specific activation of a critical bacterial cell cycle kinase
journal, March 2010

  • Iniesta, A. A.; Hillson, N. J.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 15
  • DOI: 10.1073/pnas.1001767107

A novel bacterial tyrosine kinase essential for cell division and differentiation
journal, November 1999

  • Wu, J.; Ohta, N.; Zhao, J. -L.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 23
  • DOI: 10.1073/pnas.96.23.13068

The essential genome of a bacterium
journal, January 2011

  • Christen, Beat; Abeliuk, Eduardo; Collier, John M.
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.58

The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis
journal, January 2010


MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Structural Insight into Partner Specificity and Phosphoryl Transfer in Two-Component Signal Transduction
journal, October 2009


Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein
journal, December 2005

  • Marina, Alberto; Waldburger, Carey D.; Hendrickson, Wayne A.
  • The EMBO Journal, Vol. 24, Issue 24
  • DOI: 10.1038/sj.emboj.7600886

Structure of PAS-Linked Histidine Kinase and the Response Regulator Complex
journal, October 2009


Mechanistic Insights Revealed by the Crystal Structure of a Histidine Kinase with Signal Transducer and Sensor Domains
journal, February 2013


Visualizing autophosphorylation in histidine kinases
journal, February 2014

  • Casino, Patricia; Miguel-Romero, Laura; Marina, Alberto
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4258

Full-Length Structure of a Sensor Histidine Kinase Pinpoints Coaxial Coiled Coils as Signal Transducers and Modulators
journal, July 2013


Ligand-Induced Asymmetry in Histidine Sensor Kinase Complex Regulates Quorum Sensing
journal, September 2006


How to Switch Off a Histidine Kinase: Crystal Structure of Geobacillus stearothermophilus KinB with the inhibitor Sda
journal, February 2009

  • Bick, Matthew J.; Lamour, Valerie; Rajashankar, Kanagalaghatta R.
  • Journal of Molecular Biology, Vol. 386, Issue 1
  • DOI: 10.1016/j.jmb.2008.12.006

Segmental Helical Motions and Dynamical Asymmetry Modulate Histidine Kinase Autophosphorylation
journal, January 2014


Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis
journal, June 2012

  • Dago, A. E.; Schug, A.; Procaccini, A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 26
  • DOI: 10.1073/pnas.1201301109

TNP-ATP and TNP-ADP as Probes of the Nucleotide Binding Site of CheA, the Histidine Protein Kinase in the Chemotaxis Signal Transduction Pathway of Escherichia coli
journal, September 1998

  • Stewart, Richard C.; VanBruggen, Ricaele; Ellefson, Dolph D.
  • Biochemistry, Vol. 37, Issue 35
  • DOI: 10.1021/bi980970n

Oxygen Blocks the Reaction of the FixL−FixJ Complex with ATP but Does Not Influence Binding of FixJ or ATP to FixL
journal, November 2005

  • Sousa, Eduardo Henrique Silva; Gonzalez, Gonzalo; Gilles-Gonzalez, Marie-Alda
  • Biochemistry, Vol. 44, Issue 46
  • DOI: 10.1021/bi051661h

Probing the Nucleotide Binding Domain of the Osmoregulator EnvZ Using Fluorescent Nucleotide Derivatives
journal, November 2002

  • Plesniak, Leigh; Horiuchi, Yuki; Sem, Daniel
  • Biochemistry, Vol. 41, Issue 47
  • DOI: 10.1021/bi020331j

A High-Throughput TNP-ATP Displacement Assay for Screening Inhibitors of ATP-Binding in Bacterial Histidine Kinases
journal, April 2011

  • Guarnieri, Michael T.; Blagg, Brian S. J.; Zhao, Rui
  • ASSAY and Drug Development Technologies, Vol. 9, Issue 2
  • DOI: 10.1089/adt.2010.0289

A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus
journal, November 2007

  • Thanbichler, M.; Iniesta, A. A.; Shapiro, L.
  • Nucleic Acids Research, Vol. 35, Issue 20
  • DOI: 10.1093/nar/gkm818

Identification of direct residue contacts in protein-protein interaction by message passing
journal, December 2008

  • Weigt, M.; White, R. A.; Szurmant, H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 1
  • DOI: 10.1073/pnas.0805923106

Features of Protein–Protein Interactions in Two‐Component Signaling Deduced from Genomic Libraries
book, January 2007


Systematic Dissection and Trajectory-Scanning Mutagenesis of the Molecular Interface That Ensures Specificity of Two-Component Signaling Pathways
journal, November 2010


Rewiring the Specificity of Two-Component Signal Transduction Systems
journal, June 2008


Branched Signal Wiring of an Essential Bacterial Cell-Cycle Phosphotransfer Protein
journal, September 2013


Activation and Inhibition of the Receptor Histidine Kinase AgrC Occurs through Opposite Helical Transduction Motions
journal, March 2014


Structural plasticity and catalysis regulation of a thermosensor histidine kinase
journal, September 2009

  • Albanesi, D.; Martin, M.; Trajtenberg, F.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0906699106

The Two Active Sites of Thermotoga maritima CheA Dimers Bind ATP with Dramatically Different Affinities
journal, July 2009

  • Eaton, Anna K.; Stewart, Richard C.
  • Biochemistry, Vol. 48, Issue 27
  • DOI: 10.1021/bi900474g

Regulation of the bacterial cell cycle by an integrated genetic circuit
journal, November 2006

  • Biondi, Emanuele G.; Reisinger, Sarah J.; Skerker, Jeffrey M.
  • Nature, Vol. 444, Issue 7121
  • DOI: 10.1038/nature05321

The HHpred interactive server for protein homology detection and structure prediction
journal, July 2005

  • Soding, J.; Biegert, A.; Lupas, A. N.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki408

XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

A short history of SHELX
journal, December 2007

  • Sheldrick, George M.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122
  • DOI: 10.1107/S0108767307043930

The Buccaneer software for automated model building. 1. Tracing protein chains
journal, August 2006


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

The CCP4 suite programs for protein crystallography
journal, September 1994


An SMC ATPase mutant disrupts chromosome segregation in Caulobacter: Role of the SMC ATPase in chromosome segregation
journal, September 2011


NADH-coupled microplate photometric assay for kinetic studies of ATP-hydrolyzing enzymes with low and high specific activities
journal, October 2003


Binding of guanosine 5'-triphosphate by soluble factors required for polypeptide synthesis.
journal, March 1968

  • Ertel, R.; Brot, N.; Redfield, B.
  • Proceedings of the National Academy of Sciences, Vol. 59, Issue 3
  • DOI: 10.1073/pnas.59.3.861

[22] Elongation factor Tu and the aminoacyl-tRNA · EFTu · GTP complex
book, January 1974


Communication Modules in Bacterial Signaling Proteins
journal, December 1992


Ligand-Induced Asymmetry in Histidine Sensor Kinase Complex Regulates Quorum Sensing
journal, September 2006


Allosteric Regulation of Histidine Kinases by Their Cognate Response Regulator Determines Cell Fate
journal, May 2008


Rewiring Bacteria, Two Components at a Time
journal, June 2008


A Dynamic Complex of Signaling Proteins Uses Polar Localization to Regulate Cell-Fate Asymmetry in Caulobacter crescentus
journal, March 2011


Structure of PAS-Linked Histidine Kinase and the Response Regulator Complex
journal, October 2009


Full-Length Structure of a Sensor Histidine Kinase Pinpoints Coaxial Coiled Coils as Signal Transducers and Modulators
journal, July 2013


Branched Signal Wiring of an Essential Bacterial Cell-Cycle Phosphotransfer Protein
journal, September 2013


Probing the Nucleotide Binding Domain of the Osmoregulator EnvZ Using Fluorescent Nucleotide Derivatives
journal, November 2002

  • Plesniak, Leigh; Horiuchi, Yuki; Sem, Daniel
  • Biochemistry, Vol. 41, Issue 47
  • DOI: 10.1021/bi020331j

Oxygen Blocks the Reaction of the FixL−FixJ Complex with ATP but Does Not Influence Binding of FixJ or ATP to FixL
journal, November 2005

  • Sousa, Eduardo Henrique Silva; Gonzalez, Gonzalo; Gilles-Gonzalez, Marie-Alda
  • Biochemistry, Vol. 44, Issue 46
  • DOI: 10.1021/bi051661h

The Two Active Sites of Thermotoga maritima CheA Dimers Bind ATP with Dramatically Different Affinities
journal, July 2009

  • Eaton, Anna K.; Stewart, Richard C.
  • Biochemistry, Vol. 48, Issue 27
  • DOI: 10.1021/bi900474g

Regulation of the bacterial cell cycle by an integrated genetic circuit
journal, November 2006

  • Biondi, Emanuele G.; Reisinger, Sarah J.; Skerker, Jeffrey M.
  • Nature, Vol. 444, Issue 7121
  • DOI: 10.1038/nature05321

Visualizing autophosphorylation in histidine kinases
journal, February 2014

  • Casino, Patricia; Miguel-Romero, Laura; Marina, Alberto
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4258

Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein
journal, December 2005

  • Marina, Alberto; Waldburger, Carey D.; Hendrickson, Wayne A.
  • The EMBO Journal, Vol. 24, Issue 24
  • DOI: 10.1038/sj.emboj.7600886

Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis
journal, April 2004

  • Ryan, K. R.; Huntwork, S.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 19
  • DOI: 10.1073/pnas.0402153101

Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle
journal, March 2001

  • Jacobs, C.; Hung, D.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 7
  • DOI: 10.1073/pnas.051609998

A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade
journal, October 2008

  • Iniesta, A. A.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 43
  • DOI: 10.1073/pnas.0808807105

Structural plasticity and catalysis regulation of a thermosensor histidine kinase
journal, September 2009

  • Albanesi, D.; Martin, M.; Trajtenberg, F.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0906699106

Cell pole-specific activation of a critical bacterial cell cycle kinase
journal, March 2010

  • Iniesta, A. A.; Hillson, N. J.; Shapiro, L.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 15
  • DOI: 10.1073/pnas.1001767107

Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis
journal, June 2012

  • Dago, A. E.; Schug, A.; Procaccini, A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 26
  • DOI: 10.1073/pnas.1201301109

Binding of guanosine 5'-triphosphate by soluble factors required for polypeptide synthesis.
journal, March 1968

  • Ertel, R.; Brot, N.; Redfield, B.
  • Proceedings of the National Academy of Sciences, Vol. 59, Issue 3
  • DOI: 10.1073/pnas.59.3.861

A novel bacterial tyrosine kinase essential for cell division and differentiation
journal, November 1999

  • Wu, J.; Ohta, N.; Zhao, J. -L.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 23
  • DOI: 10.1073/pnas.96.23.13068

Phosphorylation Alters the Interaction of the Response Regulator OmpR with Its Sensor Kinase EnvZ
journal, January 2002

  • Mattison, Kirsten; Kenney, Linda J.
  • Journal of Biological Chemistry, Vol. 277, Issue 13
  • DOI: 10.1074/jbc.m111128200

A High-Throughput TNP-ATP Displacement Assay for Screening Inhibitors of ATP-Binding in Bacterial Histidine Kinases
journal, April 2011

  • Guarnieri, Michael T.; Blagg, Brian S. J.; Zhao, Rui
  • ASSAY and Drug Development Technologies, Vol. 9, Issue 2
  • DOI: 10.1089/adt.2010.0289

The HHpred interactive server for protein homology detection and structure prediction
journal, July 2005

  • Soding, J.; Biegert, A.; Lupas, A. N.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki408

A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus
journal, November 2007

  • Thanbichler, M.; Iniesta, A. A.; Shapiro, L.
  • Nucleic Acids Research, Vol. 35, Issue 20
  • DOI: 10.1093/nar/gkm818

Integration of Rotation and Piston Motions in Coiled-Coil Signal Transduction
journal, June 2007

  • Gao, Rong; Lynn, David G.
  • Journal of Bacteriology, Vol. 189, Issue 16
  • DOI: 10.1128/jb.00459-07

Polar Remodeling and Histidine Kinase Activation, Which Is Essential for Caulobacter Cell Cycle Progression, Are Dependent on DNA Replication Initiation
journal, June 2010

  • Iniesta, Antonio A.; Hillson, Nathan J.; Shapiro, Lucy
  • Journal of Bacteriology, Vol. 192, Issue 15
  • DOI: 10.1128/jb.00468-10

The Core Dimerization Domains of Histidine Kinases Contain Recognition Specificity for the Cognate Response Regulator
journal, August 2003


High-Resolution Anatomy of a Progressively Pinching Cell Division
journal, October 2005


Mutations in DivL and CckA Rescue a divJ Null Mutant of Caulobacter crescentus by Reducing the Activity of CtrA
journal, April 2006


Specificity Residues Determine Binding Affinity for Two-Component Signal Transduction Systems
journal, November 2013

  • Willett, Jonathan W.; Tiwari, Nitija; Müller, Susanne
  • mBio, Vol. 4, Issue 6
  • DOI: 10.1128/mbio.00420-13

Communication Modules in Bacterial Signaling Proteins
journal, December 1992


The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis
journal, January 2010


Segmental Helical Motions and Dynamical Asymmetry Modulate Histidine Kinase Autophosphorylation
journal, January 2014


Interplay between the Localization and Kinetics of Phosphorylation in Flagellar Pole Development of the Bacterium Caulobacter crescentus
journal, August 2012


Role of the VirA histidine autokinase of Agrobacterium tumefaciens in the initial steps of pathogenesis
journal, May 2014


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Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication
journal, May 2015


miRNA863-3p sequentially targets negative immune regulator ARLPKs and positive regulator SERRATE upon bacterial infection
journal, April 2016

  • Niu, Dongdong; Lii, Yifan E.; Chellappan, Padmanabhan
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11324

Multiple communication mechanisms between sensor kinases are crucial for virulence in Pseudomonas aeruginosa
journal, June 2018

  • Francis, Vanessa I.; Waters, Elaine M.; Finton-James, Sutharsan E.
  • Nature Communications, Vol. 9, Issue 1
  • DOI: 10.1038/s41467-018-04640-8

Multicopy plasmids allow bacteria to escape from fitness trade-offs during evolutionary innovation
journal, April 2018

  • Rodriguez-Beltran, Jeronimo; Hernandez-Beltran, J. Carlos R.; DelaFuente, Javier
  • Nature Ecology & Evolution, Vol. 2, Issue 5
  • DOI: 10.1038/s41559-018-0529-z

Selective sequestration of signalling proteins in a membraneless organelle reinforces the spatial regulation of asymmetry in Caulobacter crescentus
journal, January 2020


Dynamic translation regulation in Caulobacter cell cycle control
journal, October 2016

  • Schrader, Jared M.; Li, Gene-Wei; Childers, W. Seth
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 44
  • DOI: 10.1073/pnas.1614795113

Integration of cell cycle signals by multi-PAS domain kinases
journal, May 2018

  • Mann, Thomas H.; Shapiro, Lucy
  • Proceedings of the National Academy of Sciences
  • DOI: 10.1101/323444

Absolute measurements of mRNA translation in C. crescentus reveal important fitness costs of vitamin B 12 scavenging
journal, February 2019

  • Aretakis, James R.; Gega, Alisa; Schrader, Jared M.
  • mSystems
  • DOI: 10.1101/552000

Regulation of bacterial surface attachment by a network of sensory transduction proteins
journal, February 2019

  • Reyes Ruiz, Leila M.; Fiebig, Aretha; Crosson, Sean
  • PLOS Genetics
  • DOI: 10.1101/554154

Reversed Signaling Flow of a Bacterial Pseudokinase
posted_content, October 2019

  • Kowallis, Kimberly A.; Silfani, Elayna M.; Kasumu, Amanda P.
  • BioRxiv
  • DOI: 10.1101/812529

Classification of ab initio models of proteins restored from small-angle X-ray scattering
journal, August 2018

  • Oide, Mao; Sekiguchi, Yuki; Fukuda, Asahi
  • Journal of Synchrotron Radiation, Vol. 25, Issue 5
  • DOI: 10.1107/s1600577518010342

Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking
journal, September 2016

  • Dubey, Badri N.; Lori, Christian; Ozaki, Shogo
  • Science Advances, Vol. 2, Issue 9
  • DOI: 10.1126/sciadv.1600823

Emerging concepts in pseudoenzyme classification, evolution, and signaling
journal, August 2019


The Protease ClpXP and the PAS Domain Protein DivL Regulate CtrA and Gene Transfer Agent Production in Rhodobacter capsulatus
journal, April 2018

  • Westbye, Alexander B.; Kater, Lukas; Wiesmann, Christina
  • Applied and Environmental Microbiology, Vol. 84, Issue 11
  • DOI: 10.1128/aem.00275-18

Absolute Measurements of mRNA Translation in Caulobacter crescentus Reveal Important Fitness Costs of Vitamin B 12 Scavenging
journal, May 2019


Regulation of bacterial surface attachment by a network of sensory transduction proteins
journal, May 2019


Integration of cell cycle signals by multi-PAS domain kinases
journal, July 2018

  • Mann, Thomas H.; Shapiro, Lucy
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 30
  • DOI: 10.1073/pnas.1808543115

Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication
text, January 2015


Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking
text, January 2016


miRNA863-3p sequentially targets negative immune regulator ARLPKs and positive regulator SERRATE upon bacterial infection
journal, April 2016

  • Niu, Dongdong; Lii, Yifan E.; Chellappan, Padmanabhan
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11324

A cell cycle kinase with tandem sensory PAS domains integrates cell fate cues
journal, April 2016

  • Mann, Thomas H.; Seth Childers, W.; Blair, Jimmy A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11454

Multicopy plasmids allow bacteria to escape from fitness trade-offs during evolutionary innovation
journal, April 2018

  • Rodriguez-Beltran, Jeronimo; Hernandez-Beltran, J. Carlos R.; DelaFuente, Javier
  • Nature Ecology & Evolution, Vol. 2, Issue 5
  • DOI: 10.1038/s41559-018-0529-z

Reciprocal control of motility and biofilm formation by the PdhS2 two-component sensor kinase of Agrobacterium tumefaciens
journal, February 2019

  • Heindl, Jason E.; Crosby, Daniel; Brar, Sukhdev
  • Microbiology, Vol. 165, Issue 2
  • DOI: 10.1099/mic.0.000758

Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking
journal, September 2016

  • Dubey, Badri N.; Lori, Christian; Ozaki, Shogo
  • Science Advances, Vol. 2, Issue 9
  • DOI: 10.1126/sciadv.1600823

Polar Organizing Protein PopZ Is Required for Chromosome Segregation in Agrobacterium tumefaciens
journal, September 2017

  • Ehrle, Haley M.; Guidry, Jacob T.; Iacovetto, Rebecca
  • Journal of Bacteriology, Vol. 199, Issue 17
  • DOI: 10.1128/jb.00111-17

Absolute Measurements of mRNA Translation in Caulobacter crescentus Reveal Important Fitness Costs of Vitamin B 12 Scavenging
journal, May 2019


Regulation of bacterial surface attachment by a network of sensory transduction proteins
journal, May 2019


Comparative Analysis ofWolbachiaGenomes Reveals Streamlining and Divergence of Minimalist Two-Component Systems
journal, May 2015

  • Christensen, Steen; Serbus, Laura Renee
  • G3 Genes|Genomes|Genetics, Vol. 5, Issue 5
  • DOI: 10.1534/g3.115.017137

Redefining bacterial origins of replication as centralized information processors
journal, June 2015

  • Marczynski, Gregory T.; Rolain, Thomas; Taylor, James A.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00610