Nanosecond Structure of Radical Pair Intermediates from High-Frequency Quantum Oscillations: Insight into the Q_A^•- to...

We demonstrate the validity of our approach to deduce, from the anisotropy of quantum oscillations, the geometry of short-lived radical pair intermediates in photosynthesis. A global fit of a two-dimensional W-band (94 GHz) electron paramagnetic resonance (EPR) experiment provides the same global minimum values for the geometry of the A-side radical pair P₇₀₀^•+A_1A^•- in photosystem I (PSI) as observed in a previous Q-band (34 GHz) EPR study, yet with a significantly increased convergence rate of 62%. This demonstrates that the global fit yields the correct radical pair geometry even at Q-band frequencies. With this information, we revisit our previous Q-band study of the cofactor arrangement of P₈₆₅^•+Q_A^•-, the stabilized charge-separated state in purple bacterial reaction centers (RCs). Analysis of calculated two-dimensional data sets of P₈₆₅^•+Q_A^•- reveals that the quantum oscillation technique is unaffected by a mirror ambiguity in disordered solids and thus can provide unambiguous solutions for all five Euler angles of the radical pair geometry. This enables us to elucidate the Q_A^•- to Q_B electron transfer step in purple bacterial photosynthesis, the subject of controversial discussions for more than 25 years. Our results show that this electron transfer step involves a gating mechanism requiring a 60° rotation of the headgroup of Q_A^•- in its binding pocket.