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Title: X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II

Abstract

The oxygen-evolving complex (OEC) catalyzes water-splitting through a reaction mechanism that cycles the OEC through the “S-state” intermediates. Understanding structure/function relationsships of the S-states is crucial for elucidating the water-oxidation mechanism. Serial femtosecond X-ray crystallography has been used to obtain radiation damage-free structures. However, it remains to be established whether “diffraction-before-destruction” is actually accomplished or if significant changes are produced by the high-intensity X-ray pulses during the femtosecond scattering measurement. Here, we use ab initio molecular dynamics simulations to estimate the extent of structural changes induced on the femtosecond time scale. We found that the radiation damage is dependent on the bonding and charge of each atom in the OEC, in a manner that may provide lessons for XFEL studies of other metalloproteins. The maximum displacement of Mn and oxygen centers is 0.25 and 0.39 Å, respectively, during the 50 fs pulse, which is significantly smaller than the uncertainty given the 1.9 Å resolution of the current PSII crystal structures. However, these structural changes might be detectable when comparing isomorphous Fourier differences of electron density maps of the different S-states. Lastly, one conclusion is that pulses shorter than 15 fs should be used to avoid significant radiation damage.

Authors:
ORCiD logo [1];  [2]; ORCiD logo [2]; ORCiD logo [2];  [3]
+ Show Author Affiliations
  1. Zewail City of Science and Technology, Giza (Egypt). Center for Photonics and Smart Materials; Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Center for Free-Electron Laser Science
  2. Yale Univ., New Haven, CT (United States). Dept. of Chemistry
  3. City College of New York, NY (United States). Dept. of Physics
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1480308
Grant/Contract Number:  
FG02-05ER15646; SC0001423
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
Additional Journal Information:
Journal Volume: 121; Journal Issue: 40; Journal ID: ISSN 1520-6106
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Amin, Muhamed, Askerka, Mikhail, Batista, Victor S., Brudvig, Gary W., and Gunner, M. R. X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II. United States: N. p., 2017. Web. doi:10.1021/acs.jpcb.7b08371.
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Amin, Muhamed, Askerka, Mikhail, Batista, Victor S., Brudvig, Gary W., & Gunner, M. R. X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II. United States. https://doi.org/10.1021/acs.jpcb.7b08371
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Amin, Muhamed, Askerka, Mikhail, Batista, Victor S., Brudvig, Gary W., and Gunner, M. R. Fri . "X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II". United States. https://doi.org/10.1021/acs.jpcb.7b08371. https://www.osti.gov/servlets/purl/1480308.
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@article{osti_1480308,
title = {X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II},
author = {Amin, Muhamed and Askerka, Mikhail and Batista, Victor S. and Brudvig, Gary W. and Gunner, M. R.},
abstractNote = {The oxygen-evolving complex (OEC) catalyzes water-splitting through a reaction mechanism that cycles the OEC through the “S-state” intermediates. Understanding structure/function relationsships of the S-states is crucial for elucidating the water-oxidation mechanism. Serial femtosecond X-ray crystallography has been used to obtain radiation damage-free structures. However, it remains to be established whether “diffraction-before-destruction” is actually accomplished or if significant changes are produced by the high-intensity X-ray pulses during the femtosecond scattering measurement. Here, we use ab initio molecular dynamics simulations to estimate the extent of structural changes induced on the femtosecond time scale. We found that the radiation damage is dependent on the bonding and charge of each atom in the OEC, in a manner that may provide lessons for XFEL studies of other metalloproteins. The maximum displacement of Mn and oxygen centers is 0.25 and 0.39 Å, respectively, during the 50 fs pulse, which is significantly smaller than the uncertainty given the 1.9 Å resolution of the current PSII crystal structures. However, these structural changes might be detectable when comparing isomorphous Fourier differences of electron density maps of the different S-states. Lastly, one conclusion is that pulses shorter than 15 fs should be used to avoid significant radiation damage.},
doi = {10.1021/acs.jpcb.7b08371},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 40,
volume = 121,
place = {United States},
year = {Fri Sep 15 00:00:00 EDT 2017},
month = {Fri Sep 15 00:00:00 EDT 2017}
}
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https://doi.org/10.1021/acs.jpcb.7b08371
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