Monitoring the Reaction Process During the S 2 → S 3 Transition in Photosynthetic Water Oxidation Using Time-Resolved Infrared Spectroscopy.

Photosynthetic water oxidation performed at the Mn4 CaO5 cluster in photosystem II plays a crucial role in energy production as electron and proton sources necessary for CO2 fixation. Molecular oxygen, a byproduct, is a source of the oxygenic atmosphere that sustains life on earth. However, the molecular mechanism of water oxidation is not yet well-understood. In the reaction cycle of intermediates called S states, the S2 → S3 transition is particularly important; it consists of multiple processes of electron transfer, proton release, and water insertion, and generates an intermediate leading to O-O bond formation. In this study, we monitored the reaction process during the S2 → S3 transition using time-resolved infrared spectroscopy to clarify its molecular mechanism. A change in the hydrogen-bond interaction of the oxidized YZ • radical, an immediate electron acceptor of the Mn4 CaO5 cluster, was clearly observed as a ∼100 μs phase before the electron-transfer phase with a time constant of ∼350 μs. This observation provides strong experimental evidence that rearrangement of the hydrogen-bond network around YZ • , possibly due to the movement of a water molecule located near YZ • to the Mn site, takes place before the electron transfer. The electron transfer was coupled with proton release, as revealed by a relatively high deuterium kinetic isotope effect of 1.9. This proton release, which decreases the redox potential of the Mn4 CaO5 cluster to facilitate electron transfer to YZ • , was proposed to determine, as a rate-limiting step, the relatively slow electron-transfer rate of the S2 → S3 transition.