Novel mechanism of Cl-dependent proton dislocation in photosystem II (PSII): Hybrid Ab initio Quantum Mechanics=Molecular Mechanics Molecular Dynamics Simulation

The photosynthetic water oxidation reaction in photosystem II (PSII) causes the ejection of four protons (H⁺) and electrons from the substrate water bound to the Mn₄CaO₅ cluster, denoting the catalytic center of the system. Two Cl− ions, Cl1 and Cl2 sites, were found in the vicinity of the Mn₄CaO₅ moiety. Herein, a novel H⁺ transfer mechanism (amide H⁺ exchange-driven scheme) was identified to operate in the Cl2 pathway based on the hybrid ab initio quantum mechanics (QM) molecular dynamics (MD) simulations of PSII. The analysis revealed that H⁺ can be displaced across the peptide bond of the D1-His337 and D1-Asn338 backbones, interrupting the hydrogen bond network spanning to the lumenal side in the crystal structure. The estimated energy barrier was consistent with the previous kinetic data. This is the first report to address unidirectional H⁺ transfer through a peptide bond based on the theoretical analysis involving the environmental protein structure.