Rapid Evolution of the Photosystem II Electronic Structure during Water\n Splitting

Abstract

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