Multiple pathways of charge recombination revealed by the temperature dependence of electron transfer kinetics in cyanobacterial photosystem I

The kinetics of charge recombination in Photosystem I P-700-F-A/F-B complexes and P-700-F-x cores lacking the terminal iron-sulfur clusters were studied over a temperatures range of 310 K to 4.2 K. Analysis of the charge recombination kinetics in this temperature range allowed the assignment of backward electron transfer from the different electron acceptors to P-700(+). The kinetic and thermodynamic parameters of these recombination reactions were determined. The kinetics of all electron transfer reactions were activation-less below 170 K, the glass transition temperature of the water-glycerol solution. Above this temperature, recombination from [F-A/F-B](-) in P-7 00-F-A/F-B complexes was found to proceed along two pathways with different activation energies (E-a). The charge recombination via A(1A) has an E-a of similar to 290 meV and is dominant at temperatures above similar to 280 K, whereas the direct recombination from F-x(-) has an E-a of 22 meV and is prevalent in the 200 K to 270 K temperature range. Charge recombination from the F-x cluster becomes highly heterogeneous at temperatures below 200 K. The conformational mobility of Photosystem I was studied by molecular dynamics simulations. The F-x cluster was found to 'swing' by similar to 30 degrees along the axis between the two sulfur atoms proximal to F-A/F-B. The partial rotation of F-x is accompanied by significant changes of electric potential within the iron-sulfur cluster, which may induce preferential electron localization at different atoms of the F-x cluster. These effects may account for the partial arrest of forward electron transfer and for the heterogeneity of charge recombination observed at the glass transition temperature.