Evidence for the Proximity of Calcium to the Manganese Cluster of Photosystem II: Determination by X-ray Absorption Spectroscopy

The photosynthetic oxygen-evolving complex contains a cluster of four manganese atoms and requires both Ca and Cl for activity. The question of Ca proximity to the Mn cluster has been investigated by performing Mn X-ray absorption experiments on native samples of photosystem II (PS II) and on samples depleted of Ca and reconstituted by either Ca or Sr. Analysis of X-ray K-edge spectra demonstrates no significant differences in oxidation state or symmetry between Ca- and Sr-reactivated preparations. Differences are observed in the extended X-ray absorption fine structure (EXAFS). The amplitude of a Fourier transform peak due to scatters at distances greater than 3 A is larger for samples reactivated with strontium than for calcium-reactivated samples. Taking into account the stoichiometry of Mn and Ca atoms in PS II, and considering physically reasonable structures, curve-fitting analyses of the EXAFS data using FEFF5-calculated parameters favor a model where both manganese and calcium (or strontium) scatterers contribute to the Fourier peak at approximately 3 A. Other models for the approximately 3 A peak with multiple Mn-Mn interactions or multiple Mn-Ca(Sr) interactions can also be fit to the data, but are considered less likely. This result provides confirmation for the structural proximity of Ca to the Mn cluster suggested previously [Yachandra, V. K., et al. (1993) Science 260, 675-679]. Possible structural arrangements for a calcium-binding site are discussed.