SIMULATION OF THE S-2 STATE MULTILINE ELECTRON-PARAMAGNETIC-RESONANCE SIGNAL OF PHOTOSYSTEM-II - A MULTIFREQUENCY APPROACH

The S-2 state electron paramagnetic resonance (EPR) multiline signal of Photosystem II has been simulated at Q-band (35 Ghz), X-band (9 GHz) and S-band (4 GHz) frequencies. The model used for the simulation assumes that the signal arises from an essentially magnetically isolated Mn-III-Mn-IV dimer, with a ground state electronic spin S-T = 1/2. The spectra are generated from exact numerical solution of a general spin Hamiltonian containing anisotropic hyperfine and quadrupolar interactions at both Mn nuclei. The features that distinguish the multiline from the EPR spectra of model manganese dimer complexes (additional width of the spectrum (195 mT), additional peaks (22), internal ''superhyperfine'' structure) are plausibly explained assuming an unusual ligand geometry at both Mn nuclei, giving rise to normally forbidden transitions from quadrupole interactions as well as hyperfine anisotropy. The fitted parameters indicate that the hyperfine and quadrupole interactions arise from Mn ions in low symmetry environments, corresponding approximately to the removal of one ligand from an octahedral geometry in both cases. For a quadrupole interaction of the magnitude indicated here to be present, the Mn-III ion must be 5-coordinate and the Mn-IV 5-coordinate or possibly have a sixth, weakly bound ligand. The hyperfine parameters indicate a quasi-axial anisotropy at Mn-III, which while consistent with Jahn-Teller distortion as expected for a d(4) ion, corresponds here to the unpaired spin being in the ligand deficient, z direction of the molecular reference axis. The fitted parameters for Mn-IV are very unusual, showing a high degree of anisotropy not expected in a d(3) ion. This degree of anisotropy could be qualitatively accounted for by a histidine ligand providing pi backbonding into the metal d(xy) orbital, together with a weakly bound or absent ligand in the x direction.