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

摘要

Cryogenic illumination of Photosystem II (PSII) can lead to the trapping of the metastable radical Y_Z,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(D1- His190)~+ pair that would be formed during cryogenic oxidation of YZ. 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.