Is Deprotonation of the Oxygen-Evolving Complex of Photosystem II during the S1 → S2 Transition Suppressed by Proton Quantum Delocalization?

• Published in: Journal of the American Chemical Society Vol. 143; no. 22; pp. 8324 - 8332
• Main Authors: Yang, Ke R, Lakshmi, K. V, Brudvig, Gary W, Batista, Victor S
• Format: Journal Article
• Language: English
• Published: American Chemical Society 09.06.2021
• ISSN: 0002-7863; 1520-5126
• DOI: 10.1021/jacs.1c00633

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.