The Mn K-edge x-ray absorption spectra for the pure S states of the tetranuclear Mn cluster of the oxygen-evolving complex of photosystem II during flashinduced S-state cycling have been determined. The relative S-state populations in samples given 0, 1, 2, 3, 4, or 5 flashes were determined from fitting the flash-induced electron paramagnetic resonance (EPR)

The oxygen-evolving complex of Photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S 0 -S 4 ) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the Photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S 1 and S 2 states. The proposed model consists of two di-μ-oxo-bridged binuclear Mn units with Mn-Mn distances of ~2.7 Å that are linked to each other by a mono-μ-oxo bridge with a Mn-Mn separation of ~3.3 Å. The Mn-Mn distances are invariant in the native S 1 and S 2 states. This report describes the application of X-ray absorption spectroscopy to S 3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S 3 state compared to the S 1 and the S 2 states. The two 2.7 Å Mn-Mn distances that characterize the di-μ-oxo centers in the S 1 and S 2 states are lengthened to ~2.8 and 3.0 Å in the S 3 state, respectively. The 3.3 Å Mn-Mn and Mn-Ca distances also increase by 0.04-0.2 Å. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S 3 state. Mn-centered oxidation is evident during the S 0 →S 1 and S 1 →S 2 transitions. We propose that the changes in Mn-Mn distances during the S 2 →S 3 transition are the result of ligand or water oxidation, leading to the Supporting Information Available: E-space S 3 state EXAFS spectrum; the data in k-space and the background that was removed to reduce the low-frequency contributions that show up as peaks at <1 Å in the Fourier transform; and the Fourier isolate of the k-space S 3 spectrum, shown overplotted on the S 3 EXAFS spectrum (PDF). This material is available free of charge via the Internet at http:// pubs.acs.org. NIH Public Access

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, which 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 (EXAFS) of the complex modified by NH3 binding in the S2-state is suggestive of an increase in the Mn-Mn distance of one of these units from 2.72 +/- 0.02 to 2.87 +/- 0.02 A, whereas the Mn-Mn distance of the second unit seems to be unaffected by NH3 treatment. The elongation of one binuclear center could result from the replacement of one bridging 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 A Mn-Mn EXAFS interaction is removed. Consequently, the orientation of individual binuclear units with respect to the membrane normal becomes resolvable by EXAFS spectroscopy of partially oriented PS II membrane particles. The angle between the normal of the PS II-containing membrane and the Mn-Mn vector is determined to be 67 degrees +/- 3 degrees for the 2.87 A distance and 55 degrees +/- 4 degrees for the 2.72 A distance. Only small effects on position, shape, and orientation 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 unaffected in the annealed NH3 S2-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 structure of the manganese complex and its orientation in the membrane are discussed.

The structure of the manganese cluster in the S2 state with the g approximately 4 EPR signal (S2-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 S2-g4 state not only show a shift of the inflection point to higher energy from the S1 state but also reveal a different edge shape from that of the S2 state with the multiline signal (S2-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 S2-g4 state is distinctly different from those in the S2-MLS or S1 states. In the S2-g4 state, the second shell of back-scatters from the Mn absorber is found to contain two Mn-Mn distances of 2.73 and 2.85 A. We interpret this to indicate the presence of two nonequivalent di-mu-oxo-bridged Mn binuclear structures in the Mn cluster of the S2-g4 state. The third shell of the S2-g4 state at about 3.3 A also contains increased heterogeneity. By contrast, very little distance disorder was found to exist in the second shell of the S1 or S2-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 S2 state.

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