CORRELATION BETWEEN STRUCTURE AND MAGNETIC SPIN-STATE OF THE MANGANESE CLUSTER IN THE OXYGEN-EVOLVING COMPLEX OF PHOTOSYSTEM-II IN THE S-2 STATE - DETERMINATION BY X-RAY-ABSORPTION SPECTROSCOPY

The structure of the manganese cluster in the S-2 state with the g approximate to 4 EPR signal (S-2.g4 state) generated by 130 K illumination of photosystem II (PSII) membranes prepared from spinach has been investigated by X-ray absorption spectroscopy. The Mn X-ray absorption K-edge spectra of the S-2-g4 state not only show a shift of the inflection point to higher energy from the S-1 state but also reveal a different edge shape from that of the S-2 state with the multiline signal (S-2-MLS state). Extended X-ray absorption fine structure (EXAFS) studies of the Mn K-edge show that the structure of the Mn cluster in the S-2-g4 state is distinctly different from those in the S-2-MLS or S-1 states. In the S-2-g4 state, the second shell of back-scatterers from the Mn absorber is found to contain two Mn-Mn distances of 2.73 and 2.85 Angstrom. We interpret this to indicate the presence of two nonequivalent di-mu-oxo-bridged Mn binuclear structures in the Mn cluster of the S-2-g4 state. The third shell of the S-2-g4 state at about 3.3 Angstrom also contains increased heterogeneity. By contrast, very little distance disorder was found to exist in the second shell of the S-1 or S-2-MLS states. A mechanism is proposed to explain these results in the context of our model for the Mn cluster and the EPR properties of the Mn complex in the S-2 state.