Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II

Abstract

The room temperature pump–probe X-ray free electron laser (XFEL) measurements used for serial femtosecond crystallography provide remarkable information about the structures of the catalytic (S-state) intermediates of the oxygen-evolution reaction of photosystem II. However, mixed populations of these intermediates and moderate resolution limit the interpretation of the data from current experiments. The S₃ XFEL structures show extra density near the OEC that may correspond to a water/hydroxide molecule. However, in the latest structure, this additional oxygen is 2.08 Å from the Oε2 of D1–E189, which is closer than the sum of the van der Waals radii of the two oxygens. Here, we use Boltzmann statistics and Monte Carlo sampling to provide a model for the S₂-to-S₃ state transition, allowing structural changes and the insertion of an additional water/hydroxide. Based on our model, water/hydroxide addition to the oxygen-evolving complex (OEC) is not thermodynamically favorable in the S₂g = 2 state, but it is in the S₂g = 4.1 redox isomer. Thus, formation of the S₃ state starts by a transition from the S₂g = 2 to the S₂g = 4.1 structure. Then, electrostatic interactions support protonation of D1–H190 and deprotonation of the Ca²⁺-ligated water (W3) with proton loss to the lumen. The W3 hydroxide moves toward Mn4, completing the coordination shell of Mn4 and favoring its oxidation to Mn(IV) in the S₃ state. In addition, binding an additional hydroxide to Mn1 leads to a conformational change of D1–E189 in the S₂g = 4.1 and S₃ structures. In the S₃ state a fraction of D1–E189 release from Mn1 and bind a proton.