One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR

EPR spectroscopy is an important spectroscopic method for identification and characterization of radical species involved in many biological reactions. The tyrosyl radical is one of the most studied amino acid radical intermediates in biology. Often in conjunction with histidine residues, it is involved in many fundamental biological electron and proton transfer processes, such as in the water oxidation in photosystem II. As biological processes are typically extremely complicated and hard to control, molecular bio-mimetic model complexes are often used to clarify the mechanisms of the biological reactions. Here, we present theoretical calculations to investigate the sensitivity of magnetic resonance parameters to proton-coupled electron transfer events, as well as conformational substates of the molecular constructs which mimic the tyrosine–histidine (Tyr–His) pairs found in a large variety of proteins. Upon oxidation of the phenol, the Tyr analog, these complexes can perform not only one-electron one-proton transfer (EPT), but also one-electron two-proton transfers (E2PT). It is shown that in aprotic environment the g_X-components of the electronic g-tensor are extremely sensitive to the first proton transfer from the phenoxyl oxygen to the imidazole nitrogen (EPT product), leading to a significant increase of the g_X-value of up to 0.003, but are not sensitive to the second proton transfer (E2PT). In the latter case, the change of the g_X-value is much smaller (ca. 0.0001), which is too small to be distinguished even by high-frequency EPR. The ¹⁴N hyperfine values are also too similar to allow differentiation between the different protonation states in EPT and E2PT. The magnetic resonance parameters were also calculated as a function of the rotation angles around single bonds. It was demonstrated that rotation of the phenoxyl group results in large positive changes (> 0.001) in the g_X-values. Analysis of the data reveals that the main source of these changes is related to the strength of the H-bond between phenoxyl oxygen and the proton(s) on N₁ and N₂ positions of the imidazole.