Modeling of the P700⁺ charge recombination kinetics with phylloquinone and plastoquinone-9 in the A₁ site of photosystem I

Light activation of photosystem I (PS I) induces electron transfer from the excited primary electron donor P700 (a special pair of chlorophyll a/a′ molecules) to three iron-sulfur clusters, F_X, F_A, and F_B via acceptors A_O (a monomeric chlorophyll a) and A₁ (phylloquinone). PS I complexes isolated from menA and menB mutants contain plastoquinone-9 rather than phylloquinone in the A₁ site and show altered rates of forward electron transfer from A₁^- to [F_A/F_B] and altered rates of back electron transfer from [F_A/F_B]^- to P700⁺ (Semenov, A. Y., et al., J. Biol. Chem. 275:23429-23438, 2000). To identify the modified electron transfer steps, we studied the kinetics of flash-induced P700⁺ reduction in PS I that contains either an intact set or a subset of iron-sulfur clusters F_X, F_A, and F_B and with the A₁ binding site occupied by phylloquinone or plastoquinone-9. A modeling of the forward and backward electron transfer kinetics in P700-F_A/F_B complexes, P700-F_X cores, and P700-A₁ cores shows that the replacement of phylloquinone by plastoquinone-9 induces a decrease in the free energy gap between A₁ and F_A/F_B from ∼-205 mV in wild-type PS I to ∼-70 mV in menA PS I. The +135 mV increase in the midpoint potential of A₁ explains the acceleration in the rate of P700⁺ dark reduction in menA PS I, and the resulting uphill electron transfer from A₁ to F_X in menA PS I explains the absence of a contribution from F_X^- to the reduction of P700⁺. This fully quantitative description of PS I relates electron transfer rates, equilibrium constants, and redox potentials, and can be used to predict changes in these parameters upon substitution of electron transfer cofactors.