Is Deprotonation of the Oxygen-Evolving Complex of Photosystem II during the S 1 → S 2 Transition Suppressed by Proton Quantum Delocalization?

Yang, Ke R.; Lakshmi, K. V.; Brudvig, Gary W.; Batista, Victor S.

doi:10.1021/jacs.1c00633

Title: Is Deprotonation of the Oxygen-Evolving Complex of Photosystem II during the S ₁ → S ₂ Transition Suppressed by Proton Quantum Delocalization?

Journal Article · Mon May 24 00:00:00 EDT 2021 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.1c00633· OSTI ID:1784465

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Department of Chemistry, Yale University, New Haven, Connecticut 06520-8107, United States
Department of Chemistry and Chemical Biology and The Baruch ’60 Center for Biochemical Solar Energy, Rensselaer Polytechnic Institute, Troy, New York 12180, United States

We address the protonation state of the water-derived ligands in the oxygen-evolving complex (OEC) of photosystem II (PSII), prepared in the S₂ state of the Kok cycle. We perform quantum mechanics/molecular mechanics calculations of isotropic proton hyperfine coupling constants, with direct comparisons to experimental data from two-dimensional hyperfine sublevel correlation (HYSCORE) spectroscopy and extended X-ray absorption fine structure (EXAFS). We find a low-barrier hydrogen bond with significant delocalization of the proton shared by the water-derived ligand, W1, and the aspartic acid residue D1–D61 of the D1 polypeptide. The lowering of the zero-point energy of a shared proton due to quantum delocalization precludes its release to the lumen during the S₁→ S₂ transition. Retention of the proton facilitates the shuttling of a proton during the isomerization of the tetranuclear manganese–calcium–oxo (Mn₄Ca–oxo) cluster, from the “open” to “closed” conformation, a step suggested to be necessary for oxygen evolution from previous studies. Our findings suggest that quantum-delocalized protons, stabilized by low-barrier hydrogen bonds in model catalytic systems, can facilitate the accumulation of multiple oxidizing equivalents at low overpotentials.

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Research Organization:: Yale Univ., New Haven, CT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-05ER15646; FG02-07ER15903; DESC0001423; SC0001423

OSTI ID:: 1784465

Alternate ID(s):: OSTI ID: 1787806; OSTI ID: 1812295

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Vol. 143 Journal Issue: 22; ISSN 0002-7863

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Reaction mechanisms
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Chemical structure
Extended X-ray absorption fine structure

Title: Is Deprotonation of the Oxygen-Evolving Complex of Photosystem II during the S 1 → S 2 Transition Suppressed by Proton Quantum Delocalization?

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Title: Is Deprotonation of the Oxygen-Evolving Complex of Photosystem II during the S ₁ → S ₂ Transition Suppressed by Proton Quantum Delocalization?