Thermodynamics of the S2-to-S3 State Transition of the Oxygen-Evolving Complex of Photosystem II

TL;DR

This study models the thermodynamics and structural changes during the S2-to-S3 transition of the oxygen-evolving complex in Photosystem II, revealing the sequence of water/hydroxide binding and protonation events at room temperature.

Contribution

It introduces a thermodynamic model for the S2-to-S3 transition, clarifying water insertion and structural rearrangements in the oxygen-evolving complex.

Findings

Water/hydroxide addition is thermodynamically unfavorable in S2 g=2 but favorable in S2 g=4.1.

The S3 state forms via a transition from S2 g=2 to S2 g=4.1.

Protonation and deprotonation events support the transition and structural rearrangements.

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 {\AA} from the Oe2 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 S2 g = 2 state, but it is in the S2 g = 4.1 redox isomer. Thus, formation of the S3 state starts by a transition from the S2 g = 2 to the S2 g = 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 moving with its oxidation to Mn(IV) in the S3 state. In addition, binding additional hydroxide to Mn1 leads to a conformational change of D1-E189 in the S2 g = 4.1 and S3 structures. In the S3 state in the population of protonated D1-E189 increases.