The Tetranuclear Manganese Cluster in Photosystem II: Location and Magnetic Properties of the S2 State As Determined by Saturation−Recovery EPR Spectroscopy

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Abstract
The spin−lattice relaxation enhancement of the dark-stable tyrosine radical, YD•, by the S2 state of the O2-evolving complex (OEC) of photosystem II (PSII) has been measured by using saturation−recovery EPR spectroscopy. Two forms of the S2 state have been compared: the multiline EPR signal species in untreated PSII and the altered multiline EPR signal species in NH3-treated PSII. Previous work has shown that the non-single-exponential spin−lattice relaxation kinetics of YD• in S2-state PSII result from a dipole−dipole interaction with the Mn4 cluster of the OEC. By taking into account the temperature variation of the effective magnetic moment of the S2-state multiline EPR signal form of the OEC, we provide a quantitative analysis of its temperature-dependent enhancement of the spin−lattice relaxation of YD•. Different spin states of the Mn4 cluster in the S2 state are responsible for the effect at different temperature regimes: for T ≤ 10 K, it is the ground spin state (S = 1/2); for T ≥ 30 K, it is the first excited spin state; and at intermediate temperatures, the contributions of the two spin states are comparable. The relaxation enhancement of YD• is equivalent for both forms of the S2-state multiline EPR signal examined, indicating that the magnetic properties of the Mn4 cluster are very similar in the S2 state for both untreated and NH3-treated PSII. EPR progressive microwave-power saturation has also been used to assess the spin−lattice relaxation properties of the Mn4 cluster giving the altered S2-state multiline EPR signal in the NH3 derivative of PSII. The Orbach mechanism is shown to provide the dominant relaxation pathway; the energy difference between the ground and first excited spin states is estimated to be 30 ± 2 cm-1, which is very similar to the value found for the S2-state multiline EPR signal species in untreated PSII. Below 4 K, the effectiveness of the S2-state multiline EPR signal species as a spin relaxation enhancer of YD• drops dramatically. This is interpreted to occur because of temperature-dependent 55Mn nuclear spin−lattice relaxation which causes averaging of the effective Larmor frequency of the S2-state multiline EPR signal species during the time scale for spin−lattice relaxation of YD•; because the line shape of the S2-state multiline EPR signal is dominated by isotropic 55Mn nuclear hyperfine splittings, such nuclear relaxation processes allow frequencies in near resonance with that of YD• to be accessed, thereby producing a greater relaxation enhancement. By using a dipolar model that includes the line shapes of both the YD• and S2-state multiline EPR signals, the spin−lattice relaxation enhancement of YD• is analyzed to obtain a lower limit of 22 Å for the distance between YD• and the OEC. Together with recent studies showing a close proximity of the Mn4 cluster to YZ•, these results provide further support for an asymmetric location of the Mn4 cluster with respect to the two redox-active tyrosines in PSII.

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