Photosystem II (PSII) catalyzes light-driven water oxidation that releases dioxygen into our atmosphere and provides the electrons needed for the synthesis of biomass. The catalysis occurs in the oxygen-evolving oxo-manganese-calcium (Mn₄O₅Ca) cluster that drives the oxidation and deprotonation of substrate water molecules leading to the O₂ formation. However, despite recent advances, the mechanism of these reactions remains unclear and much debated. Here, we show that the light-driven Tyr161_D1 (Y_z) oxidation adjacent to the Mn₄O₅Ca cluster, decreases the barrier for proton transfer from the putative substrate water molecule (W3/W_x) to Glu310_D2, accessible to the luminal bulk. By combining hybrid quantum/classical (QM/MM) free energy calculations with atomistic molecular dynamics simulations, we probe the energetics of the proton transfer along the Cl1 pathway. We demonstrate that the proton transfer occurs via water molecules and a cluster of conserved carboxylates, driven by redox-triggered electric fields directed along the pathway. Glu65_D1 establishes a local molecular gate that controls the proton transfer to the luminal bulk, while Glu312_D2 acts as a local proton storage site. The identified gating region could be important in preventing backflow of protons to the Mn₄O₅Ca cluster. The structural changes, derived here based on the dark-state PSII structure, strongly support recent time-resolved X-ray free electron laser data of the S₃ → S₄ transition (Bhowmick et al. Nature 617, 2023) and reveal the mechanistic basis underlying deprotonation of the substrate water molecules. Our findings provide insight into the water oxidation mechanism of PSII and show how the interplay between redox-triggered electric fields, ion-pairs, and hydration effects control proton transport reactions.