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 (A(X), A(Y), A(Z)) 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, Mn(A), Mn(B), and Mn(C) form a strongly exchange coupled core (J(AB) and J(BC) < -100 cm^-1) while Mn(D) is weakly exchange coupled (J(CD)) to one end of the trinuclear core. For untreated and MeOH-treated PS II centers, the Mn(III) ion is either Mn(A) or Mn(C), 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 Mn(D), 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.