Abstract
The catalytic cycle of photosynthetic water oxidation occurs at the Mn4CaO5 oxygen-evolving complex (OEC) of photosystem II. Extensive spectroscopic data have been collected on the intermediates, especially the S2 (Kok) state, although the proton and electron inventories (Mn oxidation states) are still uncertain. The "high oxidation" paradigm assigns S2 Mn oxidation level (III, IV, IV, IV) or (IV, IV, IV, III), whereas a "low oxidation" paradigm posits two additional electrons. Here, we investigate the geometric (X-ray diffraction, extended X-ray absorption fine structure) and spectroscopic (electron paramagnetic resonance (EPR), electron nuclear double resonance (ENDOR)) properties of the S2 state using quantum chemical density functional theory calculations, focusing on the neglected low paradigm. Two interconvertible electronic spin configurations are predicted as ground states, producing multiline (S = 1/2) and broad (S = 5/2) EPR signals in the low paradigm oxidation state (III, IV, III, III) and with W2 as OH- and O5 as OH-. They have "open" (S = 5/2) and "closed" (S = 1/2) Mn3CaO4-cubane geometries. Other energetically accessible isomers with ground spin states 1/2, 7/2, 9/2, or 11/2 can be obtained through perturbations of hydrogen-bonding networks (e.g., H+ from His337 to O3 or W2), consistent with experimental observations. Conformers with the low oxidation state configuration (III, IV, IV, II) also become energetically accessible when the protonation states are O5 (OH-), W2 (H2O), and neutral His337. The configuration with (III, IV, III, III) agrees well with earlier low-temperature EPR and ENDOR interpretations, whereas the MnII-containing configuration agrees partially with recent ENDOR data. However, the low oxidation paradigm does not yield isotropic ligand hyperfine interactions in good agreement with observed values. We conclude that the low Mn oxidation state proposal for the OEC can closely fit most of the available structural and electronic data for S2 at accessible energies.
| Original language | English |
|---|---|
| Pages (from-to) | 11868-11882 |
| Number of pages | 15 |
| Journal | Journal of Physical Chemistry B |
| Volume | 122 |
| Issue number | 50 |
| DOIs | |
| Publication status | Published - Dec 20 2018 |
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ASJC Scopus subject areas
- Physical and Theoretical Chemistry
- Surfaces, Coatings and Films
- Materials Chemistry
Cite this
Reconciling Structural and Spectroscopic Fingerprints of the Oxygen-Evolving Complex of Photosystem II : A Computational Study of the S2 State. / Chen, He; Case, David A.; Dismukes, G Charles.
In: Journal of Physical Chemistry B, Vol. 122, No. 50, 20.12.2018, p. 11868-11882.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Reconciling Structural and Spectroscopic Fingerprints of the Oxygen-Evolving Complex of Photosystem II
T2 - A Computational Study of the S2 State
AU - Chen, He
AU - Case, David A.
AU - Dismukes, G Charles
PY - 2018/12/20
Y1 - 2018/12/20
N2 - The catalytic cycle of photosynthetic water oxidation occurs at the Mn4CaO5 oxygen-evolving complex (OEC) of photosystem II. Extensive spectroscopic data have been collected on the intermediates, especially the S2 (Kok) state, although the proton and electron inventories (Mn oxidation states) are still uncertain. The "high oxidation" paradigm assigns S2 Mn oxidation level (III, IV, IV, IV) or (IV, IV, IV, III), whereas a "low oxidation" paradigm posits two additional electrons. Here, we investigate the geometric (X-ray diffraction, extended X-ray absorption fine structure) and spectroscopic (electron paramagnetic resonance (EPR), electron nuclear double resonance (ENDOR)) properties of the S2 state using quantum chemical density functional theory calculations, focusing on the neglected low paradigm. Two interconvertible electronic spin configurations are predicted as ground states, producing multiline (S = 1/2) and broad (S = 5/2) EPR signals in the low paradigm oxidation state (III, IV, III, III) and with W2 as OH- and O5 as OH-. They have "open" (S = 5/2) and "closed" (S = 1/2) Mn3CaO4-cubane geometries. Other energetically accessible isomers with ground spin states 1/2, 7/2, 9/2, or 11/2 can be obtained through perturbations of hydrogen-bonding networks (e.g., H+ from His337 to O3 or W2), consistent with experimental observations. Conformers with the low oxidation state configuration (III, IV, IV, II) also become energetically accessible when the protonation states are O5 (OH-), W2 (H2O), and neutral His337. The configuration with (III, IV, III, III) agrees well with earlier low-temperature EPR and ENDOR interpretations, whereas the MnII-containing configuration agrees partially with recent ENDOR data. However, the low oxidation paradigm does not yield isotropic ligand hyperfine interactions in good agreement with observed values. We conclude that the low Mn oxidation state proposal for the OEC can closely fit most of the available structural and electronic data for S2 at accessible energies.
AB - The catalytic cycle of photosynthetic water oxidation occurs at the Mn4CaO5 oxygen-evolving complex (OEC) of photosystem II. Extensive spectroscopic data have been collected on the intermediates, especially the S2 (Kok) state, although the proton and electron inventories (Mn oxidation states) are still uncertain. The "high oxidation" paradigm assigns S2 Mn oxidation level (III, IV, IV, IV) or (IV, IV, IV, III), whereas a "low oxidation" paradigm posits two additional electrons. Here, we investigate the geometric (X-ray diffraction, extended X-ray absorption fine structure) and spectroscopic (electron paramagnetic resonance (EPR), electron nuclear double resonance (ENDOR)) properties of the S2 state using quantum chemical density functional theory calculations, focusing on the neglected low paradigm. Two interconvertible electronic spin configurations are predicted as ground states, producing multiline (S = 1/2) and broad (S = 5/2) EPR signals in the low paradigm oxidation state (III, IV, III, III) and with W2 as OH- and O5 as OH-. They have "open" (S = 5/2) and "closed" (S = 1/2) Mn3CaO4-cubane geometries. Other energetically accessible isomers with ground spin states 1/2, 7/2, 9/2, or 11/2 can be obtained through perturbations of hydrogen-bonding networks (e.g., H+ from His337 to O3 or W2), consistent with experimental observations. Conformers with the low oxidation state configuration (III, IV, IV, II) also become energetically accessible when the protonation states are O5 (OH-), W2 (H2O), and neutral His337. The configuration with (III, IV, III, III) agrees well with earlier low-temperature EPR and ENDOR interpretations, whereas the MnII-containing configuration agrees partially with recent ENDOR data. However, the low oxidation paradigm does not yield isotropic ligand hyperfine interactions in good agreement with observed values. We conclude that the low Mn oxidation state proposal for the OEC can closely fit most of the available structural and electronic data for S2 at accessible energies.
UR - http://www.scopus.com/inward/record.url?scp=85058133681&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85058133681&partnerID=8YFLogxK
U2 - 10.1021/acs.jpcb.8b08147
DO - 10.1021/acs.jpcb.8b08147
M3 - Article
C2 - 30444623
AN - SCOPUS:85058133681
VL - 122
SP - 11868
EP - 11882
JO - Journal of Physical Chemistry B Materials
JF - Journal of Physical Chemistry B Materials
SN - 1520-6106
IS - 50
ER -