Density functional theory (DFT) and time-dependent DFT (TDDFT) calculations are reported on three sets of isomeric models of the {Mn(4)/Ca} water-oxidizing complex of photosystem II (PS II), which share the general formula [CaMn(4)O(4)(N(2)C(3)H(4))(RCOO)(6)](q)⋅(H(2)O)(n) (R=H, CH(3); q=-1, 0, +1, +2; n=3, 4, 5, 6, 7). Comparison with the full range of available data on Mn K-edge X-ray absorption energy values determined for the photosystem allows us to validate the structures that correspond to the particular S states and to determine their Mn oxidation patterns. By using a new TDDFT procedure, it is shown that variations in the absolute K-edge energy values for a particular S state, reported by different research groups, can be quantitatively explained by different geometries adopted by the Mn cluster, which demonstrates flexibility in the position of the fourth 'dangling' Mn atom in relation to a cubane structure created by the Ca atom and the three other Mn atoms. Computational results show that each step of the S cycle occurs by removal of one electron directly from the Mn cluster. This Mn-centered oxidation still agrees with the small difference observed experimentally between the K-edge energy values of the S(2) and S(3) states of the photosystem, thus resolving a controversy as to whether this represents ligand-centered or metal-centered oxidation. The overall oxidation state of Mn atoms in the tetramanganese cluster during functional turnover changes from 2.75 for S(0), 3.00 for S(1), and 3.25 for S(2) up to 3.50 for the S(3) state, which is systematically 0.50 lower than the previously proposed oxidation states of the cluster. The calculations give insight into why these earlier, purely empirical, assignments of the Mn oxidation levels in PS II could be in error.

The semiquinone-iron complex of photosystem II was studied using electron spin resonance (ESR) spectroscopy and density functional theory calculations. Two forms of the signal were investigated: 1), the native g approximately 1.9 form; and 2), the g approximately 1.84 form, which is well known in purple bacterial reaction centers and occurs in photosystem II when treated with formate. The g approximately 1.9 form shows low- and high-field edges at g approximately 3.5 and g < 0.8, respectively, and resembles the g approximately 1.84 form in terms of shape and width. Both types of ESR signal were simulated using the theoretical approach used previously for the BRC complex, a spin Hamiltonian formalism in which the semiquinone radical magnetically interacts (J approximately 1 cm(-1)) with the nearby high-spin Fe(2+). The two forms of ESR signal differ mainly by an axis rotation of the exchange coupling tensor (J) relative to the zero-field tensor (D) and a small increase in the zero-field parameter D ( approximately 6 cm(-1)). Density functional theory calculations were conducted on model semiquinone-iron systems to identify the physical nature of these changes. The replacement of formate (or glutamate in the bacterial reaction centers) by bicarbonate did not result in changes in the coupling environment. However, when carbonate (CO(3)(2-)) was used instead of bicarbonate, the exchange and zero-field tensors did show changes that matched those obtained from the spectral simulations. This indicates that 1), the doubly charged carbonate ion is responsible for the g approximately 1.9 form of the semiquinone-iron signal; and 2), carbonate, rather than bicarbonate, is the ligand to the iron.

Time-dependent density functional theory (TDDFT) has been applied to study core excitations from 1s and 2p Mn orbitals in a series of manganese complexes with oxygen and nitrogen donor ligands. The effect of basis set and functional on the excitation energy was evaluated in detail for one complex, Mn(acac)2 x (H2O)2. The results obtained for a range of compounds, namely, [Mn(Im)6]Cl2, Mn(CH3COO)2 x 4 H2O, Mn(acac)3, Mn(SALADHP)2 and [Mn(SALPN)O]2, show good consistency with the data from X-ray absorption spectroscopy (XAS), confirming the relation between the Mn K-edge energy and the oxidation state of the Mn atom. The energies predicted for 2p core excitations show a dependence on the metal oxidation state very similar to that determined experimentally by 1s2p resonant inelastic X-ray scattering (RIXS) studies for Mn(acac)2 x (H2O)2, Mn(acac)3, and Mn(sal)2(bipy). The reliability of the K-edge energies obtained in the present study indicates that TDDFT can be used in determining the oxidation states of Mn atoms in different computational models of the manganese cluster of photosystem II (PSII).

Time-dependent density functional theory (TDDFT) calculations have been performed on a series of manganese dimers with averaged metal oxidation states of 2.0, 2.5, 3.0, 3.5 and 4.0. The excitation energies and oscillator strengths of transitions within the Mn K-core edges have been determined. The theoretical edge energies reproduce the experimental correlation between the relative position of the Mn K-edge and the averaged Mn oxidation state extremely well. A comparison with the results obtained previously for Mn complexes with different ligand environments shows that TDDFT can be successfully applied to determine the relative edge energy differences between Mn systems, taking into account the various oxidation states of the metal and differences in ligand environment in a self-consistent manner. The accuracy of the calculated edge energies indicates that the methodology employed in the current study can be used to determine the oxidation states of Mn atoms in the Mn4Ca cluster of photosystem II (PSII).

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