Protonation Structure of a Key Histidine in the Water Oxidizing Center

Abstract

Photosynthetic water oxidation is performed at the Mn cluster in photosystem II (PSII). During this process, the protonation states of water molecules and amino acid residues around the Mn cluster are crucial. In this chapter, we investigated the protonation structure of a key His residue in water oxidation, D1-H337, which forms a hydrogen bond with the Mn cluster. To determine its protonation state, we used polarized attenuated total reflectance Fourier-transform infrared (ATR-FTIR) spectroscopy accompanied with quantum mechanics/molecular mechanics (QM/MM) calculations. Light-induced polarized ATR-FTIR difference spectra upon the S1 → S2 transition showed broad positive and negative features at ~2900 and ~2600 cm−1, respectively. Large dichroic ratios with several minor Fermi resonance peaks of NH vibration of a His residue were also observed. QM/MM calculations well reproduced the spectral features as the NτH vibrations of protonated cationic D1-H337. These spectral features were reversed on the S0 formation, which indicated that this His retains the protonated cation state during the water oxidation process. In addition, QM/MM calculations showed that the redox potential (Em) of the Mn cluster in the S1 → S2 transition is comparable to that of water oxidation when D1-H337 is a protonated cation. From these results, we concluded that the protonated cationic D1-H337 plays a key role to maintain the high Em value of the Mn cluster during the S-state cycle to perform water oxidation.