Structure-Function Correlations in the (A0 → A1 → FX) Electron Transfer Kinetics of the Phylloquinone (A1) Acceptor in Cyanobacterial Photosystem I

Phylloquinone (PhQ) functions as a cofactor with a highly reducing redox potential during light-induced electron transfer (ET) processes in Photosystem I (PS I). The origin of its low redox potential is investigated here by specifically replacing the H-bonded Leu residue (L722PsaA) with a bulky Trp residue. The low temperature transient EPR (TR-EPR) spectrum of the L722WPsaA variant shows that the orientation of PhQ in the chargeseparated state is identical to that in native PS I. A change in the hyperfine couplings, however, indicates a redistribution of the unpaired spin density over the PhQ ring consistent with a considerable reduction in H-bond strength. The observed kinetics in the L722WPsaA variant relative to the wild-type show: (i) a faster rate of forward electron transfer by an order of magnitude from A1A •− to FX, and (ii) only a minor alteration in the spin polarization pattern, indicating an upper limit of about 1 ns for the A0A •− to A1A •− ET time constant. An order of magnitude change in the kinetics from A1A •− to FX is consistent with a more reducing redox potential of PhQ, comparable to that obtained for PS I with anthraquinone (AQ) incorporated into the A1A site. However, the driving energy for the preceding ET step from A0 − to PhQ is altered to a lesser extent in the L722WPsaA variant than for AQ-substituted PS I. Studies of temperature dependence indicate that the electron transfer from A1A •− to FX is thermally activated with properties different from both native and AQ-substituted PS I.