Structure of the oxygen-evolving complex of photosystem II: information on the S2 state through quantum chemical calculation of its magnetic properties

Abstract

Twelve structural models for the S(2) state of the oxygen-evolving complex (OEC) of photosystem II are evaluated in terms of their magnetic properties. The set includes ten models based on the 'fused twist' core topology derived by polarized EXAFS spectra and two related models proposed in recent mechanistic investigations. Optimized geometries and spin population analyses suggest that Mn(iii), which is most often identified with the manganese ion at site D, is always associated with a penta-coordinate environment, unless a chloride is directly ligated to the metal. Exchange coupling constants were determined by broken-symmetry density functional theory calculations and the complete spectrum of magnetic sublevels was obtained by direct diagonalization of the Heisenberg Hamiltonian. Seven models display a doublet ground state and are considered spectroscopic models for the ground state corresponding to the multiline signal (MLS) of the S(2) state of the OEC, whereas the remaining five models display a sextet ground state and could be related to the g = 4.1 signal of the S(2) state. It is found that the sign of the exchange coupling constant between the Mn centres at positions A and B of the cluster is directly related to the ground state multiplicity, implying that interconversion between the doublet and sextet can be induced by only small structural perturbations. The recently proposed quantum chemical method for the calculation of (55)Mn hyperfine coupling constants is subsequently applied to the S(2) MLS state models and the quantities that enter into the individual steps of the procedure (site-spin expectation values, intrinsic site isotropic hyperfine parameters and projected (55)Mn isotropic hyperfine constants) are analyzed and discussed in detail with respect to the structural and electronic features of each model. The current approach performs promisingly. It reacts sensitively to structural distortions and hence may be able to distinguish between different structural proposals. Thus it emerges as a useful contributor to the ongoing efforts that aim at establishing correlations between the body of spectroscopic data available for the various S(i) states of the OEC and their actual geometric features.

Structural Analysis of High-Spin States of S0-S4 at OEC Complex: A Theoretical Approach of Small Models

“…5,6,36 It is mainly explained by the μ-oxobridge MnD1---O5---MnA4 that is high sensitive to oxidation and spin state of manganese atoms as reported in literature. 13,14,[36][37][38]40,41 The standard structural deviations (σ) observed between HS regarding experimental structure is around 10.0% (see Table S2, Supplementary Information section).…”

“…This spin scheme was considered in this work once HS OEC structures are well described in literature as the main spin scheme found in natural OEC. 5,6,26 We considered initially S0 with zero charge and the following states given in Table 1, according to Kok Cycle scheme, where we can check the different spin/charge arrangements considered in our calculations. For these structures all calculations were performed using the software package Gaussian 09.…”

“…The most part of oxygen gas available on nature comes from the photooxidative process of water molecules developed by green plants, algae and cyanobacteria. [1][2][3][4][5][6][7][8][9][10][11] (1) As a result of this photochemical process (reaction 1), based on the oxidation of water molecules, we have the evolving process of oxygen gas and the energy supply to the maintenance of organisms that carry the Photosystem II (PSII) into their cells. 12 The reaction 1 is developed in several steps which are catalyzed by PSII-a protein complex found, mainly, in thylakoid membrane from plant chloroplasts or in inner cyanobacteria membrane.…”

“…The most part of oxygen gas available on nature comes from the photooxidative process of water molecules developed by green plants, algae and cyanobacteria. [1][2][3][4][5][6][7][8][9][10][11] (1)…”

“…Within this protein system we can find an oxygen evolving complex (OEC- Figure 1b) composed of 4 manganese atoms, 4 oxygen atoms and 1 calcium atom (Mn 4 CaO 5 ). [1][2][3][4][5][6][7][8][9][10][11][13][14][15][16][17] This complex constitutes the Vol. 28, No.…”