We present a model of photosynthetic water oxidation that utilizes the property of higher-valent Mn ions in two different environments and the characteristic function of redox-active ligands to explain all known aspects of electron transfer from H20 to Z, the electron donor to P680, the photosystem H reaction center chlorophyll a. There are two major features of this model. (i) The four functional Mn atoms are divided into two groups of two Mn each: [Mn] complexes in a hydrophobic cavity in the intrinsic 34-kDa protein; and (Mn) complexes on the hydrophilic surface of the extrinsic 33-kDa protein. The oxidation of H20 is carried out by two [Mn] complexes, and the protons are transferred from a [Mn] complex to a (Mn) complex along the hydrogen bond between their respective ligand H20 molecules. (it) Each of the two [Mn] ions binds one redox-active ligand (RAL), such as a quinone (alternatively, an aromatic amino acid residue). Electron transfer occurs from the reduced RAL to the oxidized Z. When the experimental data concerning atomic structure of the water-oxidizing center (WOC), electron transfer between the WOC and Z, the electronic structure of the WOC, the proton-release pattern, and the effect of Cl-are compared with the predictions of the model, satisfactory qualitative and, in many instances, quantitative agreements are obtained. In particular, this model clarifies the origin of the observed absorption-difference spectra, which have the same pattern in all S-state transitions, and of the effect of Cl1-depletion on the S states.Oxidation of water to molecular oxygen is carried out in plants through a four-step univalent redox sequence promoted by photo-induced oxidation of the photosystem II (PS11) reaction center P680 (for reviews, see refs. 1 and 2). An electron carrier Z, which exists between the water oxidation center (WOC) and P680, is suggested to be a bound plastoquinol PQH2 (3); Mn ions are included in the WOC and play an essential role in the H20 oxidation process (for review, see ref. 4); cooperation of several intrinsic and extrinsic polypeptides is required for the functioning of Mn (1); and chloride ions are also essential (5). However, the mechanism of H20 oxidation is not understood in its details and further studies are required. Various models have been proposed (6-11) that suggest how the state of the WOC, described in terms of the redox state of Mn ions and the chemical forms of the intermediates of H20 oxidation, are changed during the four-step univalent redox sequence according to Kok's four-photon scheme (2). However, none of the earlier models explains all of the existing data, and no laboratory has yet succeeded in revealing unequivocally the microscopic structure of the WOC. We present here a model for the mechanism of H20 oxidation in photosynthetic systems. It utilizes the chemistry of higher-valency Mn ions in two different environments and the characteristic function of redox-active ligands to explain all known aspects of electron transfer from H20 to Z and to p...