Coordination Changes of Carboxyl Ligands at the QAFeQB Triad in Photosynthetic Reaction Centers Studied by Density-Functional Theory

Abstract

The electron exit pathway of photosystem II (PSII) in plants and cyanobacteria comprises two quinone molecules (QA and QB) working in a series and in between a non-heme iron atom with a carboxyl ligand. Currently, the role of the Fe atom and its ligand in the QA-Fe-QB triad is insufficiently understood. We investigated the changes in the oxidation state and the coordination environment of the Fe in PSII upon quinone reduction using density-functional theory calculations (DFT). The electron transfer from QA − to QB in PSII was not accompanied by an oxidation state change of Fe(II), as previously also found for bacterial reaction center. Instead, DFT on large geometry-optimized cluster models of the Fe site and its surrounding environment based on the crystal structure suggested a transition from 6-coordinated Fe(II) to 5-coordinated Fe(II) due to a switch from bidentate to monodentate ligation (carboxylate shift) of bicarbonate at the Fe, which is induced by QA − formation. We propose that the non-heme Fe serves an essential function in the QA − →QB reaction: it steers charge densities and hydrogen-bonding within the iron-bicarbonate-quinone complex, facilitating rapid and high-yield QB reduction.KeywordsNon-heme ironPhotosystem IIElectron transferBicarbonateDensity-functional theory