Theoretical study of the multiline EPR signal from the S(2) state of the oxygen evolving complex of photosystem II: Evidence for a magnetic tetramer.

The Oxygen evolving complex of plant photosystem II is made of a manganese cluster that gives rise to a low temperature EPR multiline signal in the S(2) oxidation state. The origin of this EPR signal has been addressed with respect to the question of the magnetic couplings between the electron and nuclear spins of the four possible Mn ions that make up this complex. Considering Mn(III) and Mn(IV) as the only possible oxidation states present in the S(2) state, and no large anisotropy of the magnetic tensors, the breadths of the EPR spectra calculated for dimers and trimers with S = (1/2) have been compared with that of the biological site. It is concluded that neither a dinuclear nor a trinuclear complex made of Mn(III) and Mn(IV) can be responsible for the multiline signal; but that, by contrast, a tetranuclear Mn complex can be the origin of this signal. The general shape of the experimental spectrum, its particular hyperfine pattern, the positions of most of the hyperfine lines and their relative intensities can be fit by a tetramer model described by the following six fitting parameters: g approximately 1.987, A(1) approximately 122.4 10(-4) cm(-1), A(2) approximately 87.2 10(-4) cm(-1), A(3) approximately 81.6 10(-4) cm(-1), A(4) approximately 19.1 10(-4) cm(-1) and deltaH = 24.5 G. A second model described by parameters very close to those given above except for A(4) approximately 77.5 10(-4) cm(-1) gives an equally good fit. However, no other set of parameters gives an EPR spectrum that reproduces the hyperfine pattern of the S(2) multiline signal. This demonstrates that in the S(2) state of the oxygen evolving complex, the four manganese ions are organized in a magnetic tetramer.