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Title: Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II

Abstract

The room temperature pump–probe X-ray free electron laser (XFEL) measurements used for serial femtosecond crystallography provide remarkable information about the structures of the catalytic (S-state) intermediates of the oxygen-evolution reaction of photosystem II. However, mixed populations of these intermediates and moderate resolution limit the interpretation of the data from current experiments. The S3 XFEL structures show extra density near the OEC that may correspond to a water/hydroxide molecule. However, in the latest structure, this additional oxygen is 2.08 Å from the Oε2 of D1–E189, which is closer than the sum of the van der Waals radii of the two oxygens. In this work, we use Boltzmann statistics and Monte Carlo sampling to provide a model for the S2-to-S3 state transition, allowing structural changes and the insertion of an additional water/hydroxide. Based on our model, water/hydroxide addition to the oxygen-evolving complex (OEC) is not thermodynamically favorable in the S2 g = 2 state, but it is in the S2 g = 4.1 redox isomer. Thus, formation of the S3 state starts by a transition from the S2 g = 2 to the S2 g = 4.1 structure. Then, electrostatic interactions support protonation of D1–H190 and deprotonation of the Ca2+-ligated water (W3)more » with proton loss to the lumen. The W3 hydroxide moves toward Mn4, completing the coordination shell of Mn4 and favoring its oxidation to Mn(IV) in the S3 state. In addition, binding an additional hydroxide to Mn1 leads to a conformational change of D1–E189 in the S2 g = 4.1 and S3 structures. In the S3 state a fraction of D1–E189 release from Mn1 and bind a proton.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [4]; ORCiD logo [3];  [2];  [3]
+ Show Author Affiliations
  1. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Univ. of Groningen (The Netherlands); The British Univ. in Egypt, Cairo (Egypt)
  2. City College of New York, NY (United States); The Graduate Center of the City Univ. of New York, NY (United States)
  3. Yale Univ., New Haven, CT (United States)
  4. Zewail City of Science and Technology, Giza (Egypt)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Yale Univ., New Haven, CT (United States); City Univ. of New York (CUNY), NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; European Research Council (ERC)
OSTI Identifier:
1577781
Alternate Identifier(s):
OSTI ID: 1562140
Grant/Contract Number:  
FG02-05ER15646; SC0001423; ERC-Kupper-614507
Resource Type:
Accepted Manuscript
Journal Name:
Physical Chemistry Chemical Physics. PCCP
Additional Journal Information:
Journal Volume: 21; Journal Issue: 37; Journal ID: ISSN 1463-9076
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Chemistry; Physics

Citation Formats

Amin, Muhamed, Kaur, Divya, Yang, Ke R., Wang, Jimin, Mohamed, Zainab, Brudvig, Gary W., Gunner, M. R., and Batista, Victor. Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II. United States: N. p., 2019. Web. doi:10.1039/c9cp02308a.
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Amin, Muhamed, Kaur, Divya, Yang, Ke R., Wang, Jimin, Mohamed, Zainab, Brudvig, Gary W., Gunner, M. R., & Batista, Victor. Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II. United States. https://doi.org/10.1039/c9cp02308a
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Amin, Muhamed, Kaur, Divya, Yang, Ke R., Wang, Jimin, Mohamed, Zainab, Brudvig, Gary W., Gunner, M. R., and Batista, Victor. Mon . "Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II". United States. https://doi.org/10.1039/c9cp02308a. https://www.osti.gov/servlets/purl/1577781.
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@article{osti_1577781,
title = {Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II},
author = {Amin, Muhamed and Kaur, Divya and Yang, Ke R. and Wang, Jimin and Mohamed, Zainab and Brudvig, Gary W. and Gunner, M. R. and Batista, Victor},
abstractNote = {The room temperature pump–probe X-ray free electron laser (XFEL) measurements used for serial femtosecond crystallography provide remarkable information about the structures of the catalytic (S-state) intermediates of the oxygen-evolution reaction of photosystem II. However, mixed populations of these intermediates and moderate resolution limit the interpretation of the data from current experiments. The S3 XFEL structures show extra density near the OEC that may correspond to a water/hydroxide molecule. However, in the latest structure, this additional oxygen is 2.08 Å from the Oε2 of D1–E189, which is closer than the sum of the van der Waals radii of the two oxygens. In this work, we use Boltzmann statistics and Monte Carlo sampling to provide a model for the S2-to-S3 state transition, allowing structural changes and the insertion of an additional water/hydroxide. Based on our model, water/hydroxide addition to the oxygen-evolving complex (OEC) is not thermodynamically favorable in the S2 g = 2 state, but it is in the S2 g = 4.1 redox isomer. Thus, formation of the S3 state starts by a transition from the S2 g = 2 to the S2 g = 4.1 structure. Then, electrostatic interactions support protonation of D1–H190 and deprotonation of the Ca2+-ligated water (W3) with proton loss to the lumen. The W3 hydroxide moves toward Mn4, completing the coordination shell of Mn4 and favoring its oxidation to Mn(IV) in the S3 state. In addition, binding an additional hydroxide to Mn1 leads to a conformational change of D1–E189 in the S2 g = 4.1 and S3 structures. In the S3 state a fraction of D1–E189 release from Mn1 and bind a proton.},
doi = {10.1039/c9cp02308a},
journal = {Physical Chemistry Chemical Physics. PCCP},
number = 37,
volume = 21,
place = {United States},
year = {Mon Sep 02 00:00:00 EDT 2019},
month = {Mon Sep 02 00:00:00 EDT 2019}
}
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https://doi.org/10.1039/c9cp02308a
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