Rapid Evolution of the Photosystem II Electronic Structure during Water Splitting

TL;DR

This study uses time-resolved X-ray emission spectroscopy to observe rapid changes in the Photosystem II Mn4Ca cluster during water splitting, proposing a new mechanism involving MnIV=O formation that clarifies the O-O bond formation process.

Contribution

It introduces a novel spectroscopic approach and proposes a new mechanism for oxygen evolution involving MnIV=O formation in the S3 state, advancing understanding of water oxidation.

Findings

Rapid (within 50 μs) changes in Mn Kβ XES spectrum during oxygen evolution.

No oxidation of Mn4Ca core above MnIV state before O-O bond formation.

Proposed mechanism where O-O bond formation occurs before the final electron transfer.

Abstract

Photosynthetic water oxidation is a fundamental process that sustains the biosphere. A Mn$_{4}$Ca cluster embedded in the photosystem II protein environment is responsible for the production of atmospheric oxygen. Here, time-resolved x-ray emission spectroscopy (XES) was used to observe the process of oxygen formation in real time. These experiments reveal that the oxygen evolution step, initiated by three sequential laser flashes, is accompanied by rapid (within 50 $\mu$s) changes to the Mn K$\beta$ XES spectrum. However, no oxidation of the Mn$_{4}$Ca core above the all Mn$^{\text{IV}}$ state was detected to precede O-O bond formation. A new mechanism featuring Mn$^{\text{IV}}$=O formation in the S$_{3}$ state is proposed to explain the spectroscopic results. This chemical formulation is consistent with the unique reactivity of the S$_{3}$ state and explains facilitation of the following S$_{3}$ to S$_{0}$ transition, resolving in part the kinetic limitations associated with O-O bond formation. In the proposed mechanism, O-O bond formation precedes transfer of the final (4$^{\text{th}}$) electron from the Mn$_{4}$Ca cluster, in agreement with experiment.