Charge Recombination in SnTyrZ•QA–• Radical Pairs in D1 Protein Variants of Photosystem II: Long Range Electron Transfer in the Marcus Inverted Region

Charge recombination in the light-induced radical pair SnTyrZ(•)QA(-•) 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 D1 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 Å without any repopulation through Boltzmann equilibration of intermediates lying higher in energy. In PsbA1-PSII, the charge recombinations in the radical pairs SnTyrZ(•)QA(-•) (ket = 3.4 × 10(-3) s(-1) for S1) were slower than in PsbA3-PSII despite an expected lower driving force owing to a downshifted Em(QA/QA(-•)) in PsbA1-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 Em(TyrZ(•)/TyrZ) in S2. These observations indicate that the charge recombination occurs in the Marcus inverted region. Assuming that the driving force of the reaction (-ΔG(0) ≈ 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 -ΔG(0) = 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 TyrZ(•) and QA(-•) by aromatic cofactors located in between. Observed similar S1TyrZ(•)QA(-•) charge recombinations in PsbA2-PSII and PsbA3-PSII predict that Em(QA/QA(-•)) in PsbA2-PSII is similar to that in PsbA3-PSII.