The Semiquinone-Iron Complex of Photosystem II: Structural Insights from ESR and Theoretical Simulation; Evidence that the Native Ligand to the Non-Heme Iron Is Carbonate

The semiquinone-iron complex of photosystem II was studied using electron spin resonance (ESR) spectroscopy and density functional theory calculations. Two forms of the signal were investigated: 1), the native g similar to 1.9 form; and 2), the g similar to 1.84 form, which is well known in purple bacterial reaction centers and occurs in photosystem 11 when treated with formate. The g similar to 1.9 form shows low- and high-field edges at g similar to 3.5 and g < 0.8, respectively, and resembles the g similar to 1.84 form in terms of shape and width. Both types of ESR signal were simulated using the theoretical approach used previously for the BRC complex, a spin Hamiltonian formalism in which the semiquinone radical magnetically interacts (J similar to 1 cm(-1)) with the nearby high-spin Fe2+. The two forms of ESR signal differ mainly by an axis rotation of the exchange coupling tensor (J) relative to the zero-field tensor (D) and a small increase in the zero-field parameter D (similar to 6 cm(-1)). Density functional theory calculations were conducted on model semiquinone-iron systems to identify the physical nature of these changes. The replacement of formate (or glutamate in the bacterial reaction centers) by bicarbonate did not result in changes in the coupling environment. However, when carbonate (CO32-) was used instead of bicarbonate, the exchange and zero-field tensors did show changes that matched those obtained from the spectral simulations. This indicates that 1), the doubly charged carbonate ion is responsible for the g similar to 1.9 form of the semiquinone-iron signal; and 2), carbonate, rather than bicarbonate, is the ligand to the iron.