Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Dimer Asymmetry and Light Activation Mechanism in Brucella Blue-Light Sensor Histidine Kinase

Journal Article · · mBio (Online)
The ability to sense and respond to environmental cues is essential for adaptation and survival in living organisms. In bacteria, this process is accomplished by multidomain sensor histidine kinases that undergo autophosphorylation in response to specific stimuli, thereby triggering downstream signaling cascades. However, the molecular mechanism of allosteric activation is not fully understood in these important sensor proteins. Here, we report the full-length crystal structure of a blue light photoreceptor LOV histidine kinase (LOV-HK) involved in light-dependent virulence modulation in the pathogenic bacterium Brucella abortus. Joint analyses of dark and light structures determined in different signaling states have shown that LOV-HK transitions from a symmetric dark structure to a highly asymmetric light state. The initial local and subtle structural signal originated in the chromophore-binding LOV domain alters the dimer asymmetry via a coiled-coil rotary switch and helical bending in the helical spine. These amplified structural changes result in enhanced conformational flexibility and large-scale rearrangements that facilitate the phosphoryl transfer reaction in the HK domain.
Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1783844
Journal Information:
mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 12; ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)Copyright Statement
Country of Publication:
United States
Language:
ENGLISH

References (61)

Signal transduction in photoreceptor histidine kinases journal August 2019
VMD: Visual molecular dynamics journal February 1996
[20] Processing of X-ray diffraction data collected in oscillation mode book January 1997
Crystallization and initial X-ray diffraction analysis of the multi-domain Brucella blue light-activated histidine kinase LOV-HK in its illuminated state journal December 2018
HullRad: Fast Calculations of Folded and Disordered Protein and Nucleic Acid Hydrodynamic Properties journal February 2018
Inference of Macromolecular Assemblies from Crystalline State journal September 2007
How to Switch Off a Histidine Kinase: Crystal Structure of Geobacillus stearothermophilus KinB with the inhibitor Sda journal February 2009
Structural Basis for the Slow Dark Recovery of a Full-Length LOV Protein from Pseudomonas putida journal April 2012
The β-Scaffold of the LOV Domain of the Brucella Light-Activated Histidine Kinase Is a Key Element for Signal Transduction journal June 2012
Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain journal March 2016
Structure of the Full-Length Bacteriophytochrome from the Plant Pathogen Xanthomonas campestris Provides Clues to its Long-Range Signaling Mechanism journal September 2016
Signaling States of a Short Blue-Light Photoreceptor Protein PpSB1-LOV Revealed from Crystal Structures and Solution NMR Spectroscopy journal September 2016
Applications of the Restriction Free (RF) cloning procedure for molecular manipulations and protein expression journal October 2010
Structure and function of HWE/HisKA2-family sensor histidine kinases journal April 2017
Protein production by auto-induction in high-density shaking cultures journal May 2005
Full-Length Structure of a Sensor Histidine Kinase Pinpoints Coaxial Coiled Coils as Signal Transducers and Modulators journal July 2013
Time-Resolved X-Ray Solution Scattering Reveals the Structural Photoactivation of a Light-Oxygen-Voltage Photoreceptor journal June 2017
Structural Coupling between Autokinase and Phosphotransferase Reactions in a Bacterial Histidine Kinase journal June 2017
Electronic and Protein Structural Dynamics of a Photosensory Histidine Kinase journal May 2010
An Analysis of the Solution Structure and Signaling Mechanism of LovK, a Sensor Histidine Kinase Integrating Light and Redox Signals journal August 2010
Blue Light Regulated Two-Component Systems: Enzymatic and Functional Analyses of Light-Oxygen-Voltage (LOV)-Histidine Kinases and Downstream Response Regulators journal June 2013
Asymmetry in the Autophosphorylation of the Two-Component Regulatory System Transmitter Protein Nitrogen Regulator II of Escherichia coli journal April 2000
Visualizing autophosphorylation in histidine kinases journal February 2014
Enzymatic assembly of DNA molecules up to several hundred kilobases journal April 2009
Function, structure and mechanism of bacterial photosensory LOV proteins journal August 2011
Sequential conformational transitions and α-helical supercoiling regulate a sensor histidine kinase journal August 2017
A pH-gated conformational switch regulates the phosphatase activity of bifunctional HisKA-family histidine kinases journal December 2017
Structural insights into the signalling mechanisms of two-component systems journal July 2018
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein journal December 2005
Structural plasticity and catalysis regulation of a thermosensor histidine kinase journal September 2009
Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX journal November 2010
Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein journal May 2011
Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor journal July 2012
Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation journal December 2014
Insights into histidine kinase activation mechanisms from the monomeric blue light sensor EL346 journal February 2019
Structural basis of molecular logic OR in a dual-sensor histidine kinase journal September 2019
Structural and Enzymatic Insights into the ATP Binding and Autophosphorylation Mechanism of a Sensor Histidine Kinase journal August 2010
Structural asymmetry does not indicate hemiphosphorylation in the bacterial histidine kinase CpxA journal June 2020
MolProbity : all-atom structure validation for macromolecular crystallography journal December 2009
Features and development of Coot journal March 2010
Towards automated crystallographic structure refinement with phenix.refine journal March 2012
Resolution of structural heterogeneity in dynamic crystallography journal May 2013
S-SAD phasing of monoclinic histidine kinase from Brucella abortus combining data from multiple crystals and orientations: an example of data-collection strategy and a posteriori analysis of different data combinations journal June 2015
Conformational dynamics of the essential sensor histidine kinase WalK journal September 2017
Decreased in vivo virulence and altered gene expression by a Brucella melitensis light-sensing histidine kinase mutant journal September 2014
The B rucella abortus virulence regulator, LovhK, is a sensor kinase in the general stress response signalling pathway : The LovhK stress sensor kinase of journal October 2014
A coiled coil switch mediates cold sensing by the thermosensory protein DesK: Signal sensing and transduction by DesK journal August 2015
Regulation of the Erythrobacter litoralis DSM 8509 general stress response by visible light journal June 2019
Long-range allosteric signaling in red light–regulated diguanylyl cyclases journal March 2017
Structural Basis of a Phototropin Light Switch journal September 2003
Blue-Light-Activated Histidine Kinases: Two-Component Sensors in Bacteria journal August 2007
Light Regulation of Swarming Motility in Pseudomonas syringae Integrates Signaling Pathways Mediated by a Bacteriophytochrome and a LOV Protein journal June 2013
General Stress Signaling in the Alphaproteobacteria journal November 2015
Two-Component Sensing and Regulation: How Do Histidine Kinases Talk with Response Regulators at the Molecular Level? journal September 2019
Mechanistic Insights Revealed by the Crystal Structure of a Histidine Kinase with Signal Transducer and Sensor Domains journal February 2013
Segmental Helical Motions and Dynamical Asymmetry Modulate Histidine Kinase Autophosphorylation journal January 2014
Genetic and Biochemical Dissection of a HisKA Domain Identifies Residues Required Exclusively for Kinase and Phosphatase Activities journal November 2012
A LOV Protein Modulates the Physiological Attributes of Xanthomonas axonopodis pv. citri Relevant for Host Plant Colonization journal June 2012
LOV Histidine Kinase Modulates the General Stress Response System and Affects the virB Operon Expression in Brucella abortus journal May 2015
A Blue Light Inducible Two-Component Signal Transduction System in the Plant Pathogen Pseudomonas syringae pv. tomato journal February 2008
Asymmetric activation mechanism of a homodimeric red light-regulated photoreceptor journal June 2018

Similar Records

Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation
Journal Article · Mon Dec 01 19:00:00 EST 2014 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1214045

An Analysis of the Solution Structure and Signaling Mechanism of LovK, a Sensor Histidine Kinase Integrating Light and Redox Signals
Journal Article · Mon Dec 06 23:00:00 EST 2010 · Biochemistry-US · OSTI ID:1002929

Structure of the Entire Cytoplasmic Portion of a Sensor Histidine-kinase Protein
Journal Article · Fri Dec 31 23:00:00 EST 2004 · EMBO J. · OSTI ID:913703