HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

Light-driven water oxidation in algae, cyanobacteria, and higher plants generates dioxygen that supports life on Earth. The water-oxidation reaction is catalyzed by the oxygen-evolving complex (OEC) in photosystem II (PSII) that is comprised of the tetranuclear manganese calcium-oxo (Mn₄CaO₅) cluster, with participation of the redox-active tyrosine residue (Y_Z) and a hydrogen-bonded network of amino acids and water molecules. Y_Z mediates successive proton-coupled electron transfer (PCET) reactions that are essential for the oxidation of water to dioxygen at the Mn₄CaO₅ cluster. It has been proposed that the strong hydrogen bond between Y_Z and and its conjugate base, D1-His190, likely renders Y_Z kinetically and thermodynamically competent leading to highly efficient water oxidation.¹ However, a detailed understanding of PCET at Y_Z remains elusive due to the transient nature of its intermediate states. In this study, we utilize a combination of high-resolution two-dimensional (2D) ¹⁴N hyperfine sublevel correlation (HYSCORE) spectroscopy and density functional theory (DFT) methods to investigate the electronic structure of a bioinspired artificial photosynthetic reaction center, benzimidazole-phenol porphyrin (BiP–PF₁₀), that mimics the PCET process at the Y_Z residue of PSII. The results of these studies underscore the importance of proximal water molecules and charge delocalization on the electronic structure of the artificial reaction center.