Water-modulated conformational heterogeneity underlies multiple timescales of primary charge separation in...

The kinetics of charge separation in Photosystem II, initiated within the reaction center, remain debated due to spectral congestion and overlapping timescales with energy transfer. Here, by means of atomistic molecular dynamics and quantum dynamics simulations, we present a kinetic model that attributes the observed multi-exponential behavior of the primary charge separation step to water-modulated conformational heterogeneity rather than to parallel pathways involving chemically distinct intermediate radical pairs. We propose that charge separation proceeds predominantly via the ${\mathrm{Chl}}_{\mathrm{D1}}^{+}{\mathrm{Pheo}}_{\mathrm{D1}}^{-}$ intermediate radical pair, with structural fluctuations of protein and solvent, specifically dynamic water channels near the oxygen-evolving complex, governing the multi-exponential kinetics. Analytical resolution of a kinetic scheme, which also incorporates pre-equilibration within the excited-state manifold of the reaction center, yields apparent lifetimes ( < 250 fs, 386 fs, 2.7 ps) comparable with experimental data. This model reconciles previous conflicting assignments and emphasizes the role of protein-solvent dynamics in shaping ultrafast charge separation.