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

• Published in: Biochemistry (Easton) 1997-08, Vol.36 (32), p.9735-9746
• Main Authors: Koulougliotis, Dionysios, Schweitzer, Robert H, Brudvig, Gary W
• Format: Article
• Language: English
• Subjects: Ammonia - pharmacology; Electron Spin Resonance Spectroscopy - methods; Manganese - chemistry; Manganese - metabolism; Oxidation-Reduction - drug effects; Photosynthetic Reaction Center Complex Proteins - chemistry; Photosynthetic Reaction Center Complex Proteins - drug effects; Photosynthetic Reaction Center Complex Proteins - metabolism; Photosystem II Protein Complex; plant biochemistry; Plant Leaves; plant physiology; Spinacia oleracea
• ISSN: 0006-2960; 1520-4995
• DOI: 10.1021/bi970326t

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, ther