Charge Recombination in S_nTyr_z·Q_A~(-·) Radical Pairs in D1 Protein Variants of Photosystem II: Long Range Electron Transfer in the Marcus Inverted Region

摘要

Charge recombination in the light-induced radical pair S_nTyr_z·Q_A~(-·) in Photosystem II (PSII) from Thermosynechococcus elongatus has been studied at cryogenic temperatures by time-resolved EPR for different configurations of PSII that are expected to affect the driving force of the reaction (oxidation states S0, S1, or S2 of the Mn4CaO5 cluster; PsbA1, PsbA2, or PsbA3 as Dl protein). The kinetics were independent of temperature in the studied range from 4.2 to 50 K, and were not affected by exchange of H2O for D2O, consistent with single-step electron tunneling over the distance of ～32 A without any repopulation through Boltzmann equilibration of intermediates lying higher in energy. In PsbAl-PSII, the charge recombinations in the radical pairs S_nTyr_z·Q_A~(-·) (k_(et)= 3-4 X 10~(-3) s~(-1) for S_L) were slower than in PsbA3-PSII despite an expected lower, driving force owing to a downshifted E_m(Q_A/Q_A~(-·)) in PsbAl-PSII. Conversely, the reaction was slower in the presence of S2 than in the presence of S1, despite an expected larger driving force due to an upshifted E_m(Tyr_z·/Tyr_z) in S2. These Observations indicate that the charge recombination occurs in the Marcus inverted region. Assuming that the driving force of the reaction (—ΔG0≈ 1.2 eV at room temperature for S1) does not vary strongly with temperature, the data indicate an optimal electron transfer rate (for a hypothetical —ΔG0 = λ) substantially faster than would be predicted from extrapolation of room temperature intraprotein ET rates over shorter distances. Possible origins of this deviation are discussed, including a possible enhancement of the electronic coupling of Tyr_z· and Q_a~(-·) by aromatic cofactors located in between. Observed similar S_nTyr_z·Q_A~(-·) charge recombinations in PsbA2-PSlI and PsbA3-PSII predict that E_m(Q_A/Q_A~(-·)) in PsbA2-PSII is similar to that in PsbA3-PSIL.