Chloride Maintains a Protonated Internal Water Network in the Photosynthetic Oxygen Evolving Complex

In photosystem II (PSII), water oxidation occurs at a Mn₄CaO₅ cluster and results in production of molecular oxygen. The Mn₄CaO₅ cluster cycles among five oxidation states, called S_n states. As a result, protons are released at the metal cluster and transferred through a 35 Å hydrogen-bonding network to the lumen. At 283 K, an infrared band at 2830 cm^-1 is assigned to an internal solvated hydronium ion via H₂¹⁸O solvent exchange. This result is similar to a previous report at 263 K. Computations on an oxygen evolving complex model predict that chloride can stabilize a hydronium ion on a network of nine water molecules. In this model, a H₃O⁺ stretching mode at 2738 cm^-1 is predicted to shift to higher frequency with bromide and to lower frequency with nitrate substitution. The calculated frequencies were compared to S₂-minus-S₁ reaction-induced Fourier transform infrared spectra acquired from chloride-, bromide-, or nitrate-containing PSII samples, which were active in oxygen evolution. As predicted, the frequency of the 2830 cm^-1 band shifted to higher energy with bromide and to lower energy with nitrate substitution. These results support the conclusion that an internal hydronium ion and chloride play a direct role in an internal proton transfer event during the S₁-to-S₂ transition.