55Mn ENDOR of the S2-State Multiline EPR Signal of Photosystem II:  Implications on the Structure of the Tetranuclear Mn Cluster

We have performed continuous-wave electron paramagnetic resonance (CW-EPR) and electron spin echo electron nuclear double resonance (ESE-ENDOR) experiments on the multiline form of the S2-state of untreated, MeOH-treated, and ammonia-treated spinach photosystem II (PS II) centers. Through simultaneously constrained simulations of the CW-EPR and ESE-ENDOR data, we conclude that four effective 55Mn hyperfine tensors (AX, AY, AZ) are required to properly simulate the experimental data untreated and MeOH-treated PS II centers (MHz): −232, −232, −270; 200, 200, 250; −311, −311, −270; 180, 180, 240; ammonia-treated PS II centers (MHz): 208, 208, 158; −150, −150, −112; 222, 222, 172; −295, −315, −390. We further show that these effective hyperfine tensors are best supported by a trimer/monomer arrangement of three Mn(IV) ions and one Mn(III) ion. In this topology, MnA, MnB, and MnC form a strongly exchange coupled core (JAB and JBC < −100 cm-1) while MnD is weakly exchange coupled (JCD) to one end of the trinuclear core. For untreated and MeOH-treated PS II centers, the Mn(III) ion is either MnA or MnC, with a zero-field-splitting of D = −1.25 to −2.25 cm-1. For ammonia-treated PS II centers, the Mn(III) ion is MnD, with a zero-field-splitting of D = +0.75 to +1.75 cm-1. The binding of the ammonia ligand results in a shift of the Mn(III) ion from the trinuclear core to the monomer Mn ion. This structural model can also account for the higher spin of the g = 4.1 signal and the magnetic properties of the S0-state.