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Light-induced protein structural dynamics in bacteriophytochrome revealed by time-resolved x-ray solution scattering

Journal Article · · Science Advances
 [1];  [2];  [1];  [1];  [1];  [1];  [3];  [3];  [4];  [4];  [3];  [1]
  1. Korea Advanced Inst. Science and Technology (KAIST), Daejeon (Korea, Republic of); Institute for Basic Science (IBS) (Korea, Republic of)
  2. Mokpo National University (Korea, Republic of)
  3. Univ. of Illinois, Chicago, IL (United States)
  4. Univ. of Chicago, IL (United States)

Bacteriophytochromes (BphPs) are photoreceptors that regulate a wide range of biological mechanisms via red light–absorbing (Pr)–to–far-red light–absorbing (Pfr) reversible photoconversion. The structural dynamics underlying Pfr-to-Pr photoconversion in a liquid solution phase are not well understood. We used time-resolved x-ray solution scattering (TRXSS) to capture light-induced structural transitions in the bathy BphP photosensory module of Pseudomonas aeruginosa. Kinetic analysis of the TRXSS data identifies three distinct structural species, which are attributed to lumi-F, meta-F, and Pr, connected by time constants of 95 μs and 21 ms. Structural analysis based on molecular dynamics simulations shows that the light activation of PaBphP accompanies quaternary structural rearrangements from an “II”-framed close form of the Pfr state to an “O”-framed open form of the Pr state in terms of the helical backbones. This study provides mechanistic insights into how modular signaling proteins such as BphPs transmit structural signals over long distances and regulate their downstream biological responses.

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); National Institutes of Health (NIH)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1877219
Journal Information:
Science Advances, Journal Name: Science Advances Journal Issue: 21 Vol. 8; ISSN 2375-2548
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
ENGLISH

References (60)

Light-Induced Conformational Changes of the Chromophore and the Protein in Phytochromes: Bacterial Phytochromes as Model Systems journal April 2010
SwissParam: A fast force field generation tool for small organic molecules journal May 2011
Spectroscopy and a High-Resolution Crystal Structure of Tyr263 Mutants of Cyanobacterial Phytochrome Cph1 journal October 2011
Structure of the Full-Length Bacteriophytochrome from the Plant Pathogen Xanthomonas campestris Provides Clues to its Long-Range Signaling Mechanism journal September 2016
Transient electronic and vibrational signatures during reversible photoswitching of a cyanobacteriochrome photoreceptor journal April 2021
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers journal September 2015
Structure of a Bacteriophytochrome and Light-Stimulated Protomer Swapping with a Gene Repressor journal August 2012
Light Signaling Mechanism of Two Tandem Bacteriophytochromes journal July 2015
Crystal Structure of Deinococcus Phytochrome in the Photoactivated State Reveals a Cascade of Structural Rearrangements during Photoconversion journal March 2016
Signaling Mechanism of Phytochromes in Solution journal February 2021
Light helps bacteria make important lifestyle decisions journal September 2011
Reversible molecular motional switch based on circular photoactive protein oligomers exhibits unexpected photo-induced contraction journal August 2021
Protein Structural Dynamics Revealed by Time-Resolved X-ray Solution Scattering journal July 2015
Characterizing Enzyme Reactions in Microcrystals for Effective Mix-and-Inject Experiments using X-ray Free-Electron Lasers journal September 2020
The Origin of Ultrafast Multiphasic Dynamics in Photoisomerization of Bacteriophytochrome journal July 2020
Direct Observation of Insulin Association Dynamics with Time-Resolved X-ray Scattering journal September 2017
Elucidating the Molecular Mechanism of Ultrafast Pfr-State Photoisomerization in Bathy Bacteriophytochrome PaBphP journal October 2019
Visualizing Solution-Phase Reaction Dynamics with Time-Resolved X-ray Liquidography journal February 2009
Red/Green Cyanobacteriochromes: Sensors of Color and Power journal November 2012
Direct Observation of Cooperative Protein Structural Dynamics of Homodimeric Hemoglobin from 100 ps to 10 ms with Pump–Probe X-ray Solution Scattering journal April 2012
Pump–Dump–Probe and Pump–Repump–Probe Ultrafast Spectroscopy Resolves Cross Section of an Early Ground State Intermediate and Stimulated Emission in the Photoreactions of the Pr Ground State of the Cyanobacterial Phytochrome Cph1 journal January 2012
Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome journal October 2011
Signal amplification and transduction in phytochrome photosensors journal April 2014
Direct observation of bond formation in solution with femtosecond X-ray scattering journal February 2015
Atomistic characterization of the active-site solvation dynamics of a model photocatalyst journal November 2016
Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering journal September 2008
Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser journal August 2014
CHARMM36m: an improved force field for folded and intrinsically disordered proteins journal November 2016
Structural snapshot of a bacterial phytochrome in its functional intermediate state journal November 2018
Vibrational wavepacket dynamics in Fe carbene photosensitizer determined with femtosecond X-ray emission and scattering journal January 2020
Ultrafast coherent motion and helix rearrangement of homodimeric hemoglobin visualized with femtosecond X-ray solution scattering journal June 2021
Mapping the emergence of molecular vibrations mediating bond formation journal June 2020
Light-induced structural changes in a full-length cyanobacterial phytochrome probed by time-resolved X-ray scattering journal January 2019
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein journal December 2005
Combined probes of X-ray scattering and optical spectroscopy reveal how global conformational change is temporally and spatially linked to local structural perturbation in photoactive yellow protein journal January 2016
Finding intersections between electronic excited state potential energy surfaces with simultaneous ultrafast X-ray scattering and spectroscopy journal January 2019
Dynamics and efficiency of photoswitching in biliverdin-binding phytochromes journal January 2019
X-ray snapshots reveal conformational influence on active site ligation during metalloprotein folding journal January 2019
The structural changes in the signaling mechanism of bacteriophytochromes in solution revealed by a multiscale computational investigation journal January 2021
The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties journal February 2003
Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion journal July 2007
The structure of a complete phytochrome sensory module in the Pr ground state journal September 2008
Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: Photoconversion and signal transduction journal September 2008
Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome journal August 2009
Protein structural dynamics in solution unveiled via 100-ps time-resolved x-ray scattering journal April 2010
Protein folding from heterogeneous unfolded state revealed by time-resolved X-ray solution scattering journal June 2020
A New Type of Bacteriophytochrome Acts in Tandem with a Classical Bacteriophytochrome to Control the Antennae Synthesis in Rhodopseudomonas palustris journal July 2005
Ultrafast X-Ray Scattering Measurements of Coherent Structural Dynamics on the Ground-State Potential Energy Surface of a Diplatinum Molecule journal February 2019
Visualizing Photochemical Dynamics in Solution through Picosecond X-Ray Scattering journal October 2001
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates journal December 1995
Pr‐favoured variants of the bacteriophytochrome from the plant pathogen Xanthomonas campestris hint on light regulation of virulence‐associated mechanisms journal May 2021
Biochemical and spectroscopic characterization of the bacterial phytochrome of Pseudomonas aeruginosa: Pseudomonas phytochrome journal March 2005
Structural photoactivation of a full-length bacterial phytochrome journal August 2016
Long-range allosteric signaling in red light–regulated diguanylyl cyclases journal March 2017
Tracking Ca 2+ ATPase intermediates in real time by x-ray solution scattering journal March 2020
Ultrafast X-ray Diffraction of Transient Molecular Structures in Solution journal August 2005
Phytochrome Structure and Signaling Mechanisms journal June 2006
Chromophore Structure in the Photocycle of the Cyanobacterial Phytochrome Cph1 journal September 2006
Phytochromes in Agrobacterium fabrum journal April 2021
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser journal March 2020

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