Protonation structure of the photosynthetic water oxidizing complex in the S0 state as revealed by normal mode analysis using quantum mechanics/molecular mechanics calculations

Abstract

Photosynthetic water oxidation takes place through the light-driven cycle of five intermediates (S₀–S₄) of the water oxidizing complex (WOC), which consists of the Mn₄CaO₅ cluster and surrounding amino acid residues in photosystem II. Clarifying the protonation structures of the Mn₄CaO₅ cluster and its water ligands (W1–W4) is essential for understanding the molecular mechanism of water oxidation. Here, we performed normal mode analysis of WOC in the S₀ and S₁ states using quantum mechanics/molecular mechanics calculations and simulated an S₁-minus-S₀ infrared difference spectrum focusing on the symmetric COO⁻ stretching (ν_sCOO⁻) region. The calculated spectrum by an S₀ model, in which O4 of the Mn₄CaO₅ cluster is protonated and W2 is H₂O, and a corresponding S₁ state with deprotonated O4 best reproduced the ν_sCOO⁻ features of the experimental spectrum, whereas models with protonated O5 showed poor agreement. In addition, comparison of the calculated coordination distances of the water ligands with the experimental data by X-ray diffraction analysis indicates that W2 is most probably not OH⁻ but H₂O both in the S₀ and S₁ states. The present calculations thus strongly suggest that the S₀ state has a protonation structure of O4–H and W2 = H₂O. The O4–H structure in the S₀ state supports the view that this proton is released through the O4–water chain immediately after electron transfer during the S₀ → S₁ transition.