Temperature Dependence of and Ligation Effects on Long-Range Electron Transfer in Complementary [Zn,Fe^III]Hemoglobin Hybrids

This report presents the first full temperature response of long-range electron transfer within a protein electron-transfer complex of known architecture, the [2n,Fe^III]hemoglobin hybrids. For both hybrids k₁ exhibits a thermally activated regime in which nonadiabatic electron transfer is coupled to thermal vibrations and/or fluctuations within the α₁–β₂ electron-transfer complex and its environment. Below ca. 160 K, k₁is independent of temperature and the transfer process occurs by nonadiabatic electron tunneling in which the accompanying nuclear rearrangement proceeds by nuclear tunneling. The transition between these two regimes differs in the two hybrids because of different responses of the ferriheme (Fe^IIIP) coordination state to cooling. Variable-temperature optical measurements and EPR spectroscopy show that the H₂0 heme ligand of the [α(Fe^IIIH₂O),β(Zn)] species is replaced by the imidazole of the distal histidine upon cooling, but the heme ligation of the [α(Zn),β(Fe^IIIH₂O)] hybrid remains invariant. Analysis of the data in terms of the quantum-mechanical theory of vibronically coupled electron tunneling permits us to make comparisons with results for electron transfer in ruthenium-modified proteins, as well as with electron transfer from the cytochrome-to-bacteriochlorophyll special pair in the photosynthetic reaction center of C. vinosum.