Modeling of the P700 + Charge Recombination Kinetics with Phylloquinone and Plastoquinone-9 in the A 1 Site of Photosystem I

Abstract

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 0 (a monomeric chlorophyll a) and A 1 (phylloquinone). PS I complexes isolated from menA and menB mutants contain plastoquinone-9 rather than phylloquinone in the A 1 site and show altered rates of forward electron transfer from A 1 − 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 A 1 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–A 1 cores shows that the replacement of phylloquinone by plastoquinone-9 induces a decrease in the free energy gap between A 1 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 A 1 explains the acceleration in the rate of P700 + dark reduction in menA PS I, and the resulting uphill electron transfer from A 1 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.