Orientation of the Tetranuclear Manganese Cluster and Tyrosine Z in the O2-Evolving Complex of Photosystem II: An EPR Study of the S2YZ• State in Oriented Acetate-Inhibited Photosystem II Membranes

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Abstract
Inhibitory treatment by acetate, followed by illumination and rapid freezing, is known to trap the S2YZ• state of the O2-evolving complex (OEC) in photosystem II (PS II). An EPR spectrum of this state exhibits broad split signals due to the interaction of the tyrosyl radical, YZ•, with the S = 1/2 S2 state of the Mn4 cluster. We present a novel approach to analyze S2YZ• spectra of one-dimensionally (1-D) oriented acetate-inhibited PS II membranes to determine the magnitude and relative orientation of the S2YZ• dipolar vector within the membrane. Although there exists a vast body of EPR data on isolated spins in oriented membrane sheets, the present study is the first of its kind on dipolar-coupled electron spin pairs in such systems. We demonstrate the feasibility of the technique and establish a rigorous treatment to account for the disorder present in partially oriented 1-D membrane preparations. We find that (i) the point-dipole distance between YZ• and the Mn4 cluster is 7.9 ± 0.2 Å, (ii) the angle between the interspin vector and the thylakoid membrane normal is 75°, (iii) the gz-axis of the Mn4 cluster is 70° away from the membrane normal and 35° away from the interspin vector, and (iv) the exchange interaction between the two spins is −275 × 10-4 cm-1, which is antiferromagnetic. Due to the sensitivity of EPR line shapes of oriented spin-coupled pairs to the interspin distance, the present study imposes a tighter constraint on the YZ-Mn4 point−dipole distance than obtained from randomly oriented samples. The geometric constraints obtained from the 1-D oriented sample are combined with published models of the structure of Mn-depleted PS II to propose a location of the Mn4 cluster. A structure in which YZ is hydrogen bonded to a manganese-bound hydroxide ligand is consistent with available data and favors maximal orbital overlap between the two redox center that would facilitate direct electron- and proton-transfer steps.

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