Orientation of the Mn(II)-Mn(III) dimer which results from the reduction of the oxygen-evolving complex of photosystem II by NO: An electron paramagnetic resonance study

The central part of the oxygen-evolving complex of photosystem II is a clus ter of four manganese atoms. The known EPR spectra in the various oxidation states of the cluster are complicated by the magnetic interactions of the four Mn ions and accordingly are difficult to analyze. It has been shown re cently that NO at -30 degreesC slowly reduces the cluster to a Mn(II)-Mn(II I) state [Sarrou, J., Ioannidis, N., Deligiannakis, Y., and Petrouleas, V. (1998) Biochemistry 37, 3581-3587). We study herein the orientation depende nce of the Mn(II)-Mn(III) EPR spectrum with respect to the thylakoid membra ne plane. Both the powder and the oriented spectra are satisfactorily simul ated with the same set of fine and hyperfine parameters assuming axial symm etry and collinear g and A tensors. The axial component of the tensors is f ound to be oriented at an angle of 20 degrees +/- 10 degrees to the membran e plane normal (mosaic spread Omega = 40 degrees). We make the reasonable a ssumption that the Mn(II)-Mn(III) dimer is one of the di-mu -oxo units that has been suggested to comprise the Mn tetramer. On the basis of the sign o f the hyperfine tensor anisotropy, the axial direction is assigned to the d (z)2 orbital of Mn(III), which by comparison with synthetic model complexes is assumed to be oriented perpendicular to the Mn-(mu -oxo)-Mn plane. The present results complement earlier orientation studies by EXAFS and suggest that the Mn-(mu -oxo)-Mn plane makes a small angle (approximately 20 degre es) with the membrane plane and the axis connecting the bridging oxygens is approximately parallel to the plane.