Photosystem II: Probing Protons and Breaking Barriers.

Abstract

Photosystem II (PSII) is a multisubunit protein-pigment complex that drives the oxidation of water, producing molecular oxygen essential for life. At the core of PSII, the oxygen-evolving complex (OEC) facilitates sequential four-electron oxidation steps following the Kok cycle. Despite significant progress in structural and spectroscopic studies, fundamental questions remain regarding the precise mechanisms of substrate water incorporation, deprotonation pathways, and oxygen-oxygen bond formation. A key challenge is determining the protonation states of water ligands and oxo bridges in the OEC, as incorrect assignments can eventually lead to misinterpretation of reaction energetics and mechanisms. This Review examines recent structural, spectroscopic, and theoretical studies, with a particular focus on proton transfer pathways and the role of key residues in regulating OEC deprotonation, emphasizing the importance of systematically establishing protonation states at lower S-states before modeling higher oxidation states. By integrating structural data with fundamental chemical principles, we outline essential considerations for constructing a physically meaningful and mechanistically coherent model of water oxidation in PSII.