Visible Light Induction of an Electron Paramagnetic Resonance Split Signal in Photosystem II in the S2 State Reveals the Importance of Charges in the Oxygen-Evolving Center during Catalysis: A Unifying Model

Cryogenic illumination of Photosystem II (PSII) can lead to the trapping of the metastable radical Y-z(center dot), the radical form of the redox-active tyrosine residue D1-Tyr161 (known as Y-z). Magnetic interaction between this radical and the CaMn4 cluster of PSII gives rise to so-called split electron paramagnetic resonance (EPR) signals with characteristics that are dependent on the S state. We report here the observation and characterization of a split EPR signal that can be directly induced from PSII centers in the S-2 state through visible light illumination at 10 K. We further show that the induction of this split signal takes place via a Mn-centered mechanism, in the same way as when using near-infrared light illumination [Koulougliotis, D., et al. (2003) Biochemistry 42, 3045-3053]. On the basis of interpretations of these results, and in combination with literature data for other split signals induced under a variety of conditions (temperature and light quality), we propose a unified model for the mechanisms of split signal induction across the four S states (S-0, S-1, S-2, and S-3). At the heart of this model is the stability or instability of the Y-z(center dot)(D1-His190)(+) pair that would be formed during cryogenic oxidation of Y-Z. Furthermore, the model is closely related to the sequence of transfers of protons and electrons from the CaMn4, cluster during the S cycle and further demonstrates the utility of the split signals in probing the immediate environment of the oxygen-evolving center in PSII.