STRUCTURAL CONSEQUENCES OF AMMONIA BINDING TO THE MANGANESE CENTER OFTHE PHOTOSYNTHETIC OXYGEN-EVOLVING COMPLEX - AN X-RAY-ABSORPTION SPECTROSCOPY STUDY OF ISOTROPIC AND ORIENTED PHOTOSYSTEM-II PARTICLES

The structure and orientation of the manganese complex in NH3-treated photosystem II (PS II) membrane particles of spinach are being studied by X-ray absorption spectroscopy. On the basis of earlier work by our group, a structure for the tetranuclear manganese complex of PS II, w hich consists of two di-mu-oxo-bridged binuclear Mn units linked by a mono-mu-oxo group, has been proposed [Yachandra, V. K., et al. (1993) Science 260, 675-679]. The extended X-ray absorption fine structure (E XAFS) of the complex modified by NH3 binding in the S-2-state is sugge stive of an increase in the Mn-Mn distance of one of these units from 2.72 +/- 0.02 to 2.87 +/- 0.02 Angstrom, whereas the Mn-Mn distance of the second unit seems to be unaffected by NH3 treatment. The elongati on of one binuclear center could result from the replacement of one br idging mu-oxo by an amido group. The lengthening of one Mn-Mn distance means that, by NH3 treatment, the distance degeneracy of the 2.7 Angs trom Mn-Mn EXAFS interaction is removed. Consequently, the orientation of individual binuclear units with respect to the membrane normal bec omes resolvable by EXAFS spectroscopy of partially oriented PS II memb rane particles. The angle between the normal of the PS II-containing m embrane and the Mn-Mn vector is determined to be 67 degrees +/- 3 degr ees for the 2.87 Angstrom distance and 55 degrees +/- 4 degrees for th e 2.72 Angstrom distance. Only small effects on position, shape, and o rientation dependence of Mn K-edge spectra result from NH3 treatment, indicating that the Mn oxidation state, the symmetry of the Mn ligand environment, and the orientation of the complex remain essentially una ffected in the annealed NH3 S-2-state. Therefore, it seems likely that the angles determined for the ammonia-modified manganese complex are similar to the respective angles of the untreated complex. The structu re of the manganese complex and its orientation in the membrane are di scussed.