Structural Coupling of a Tyrosine Side Chain with the Non-Heme Iron Center in Photosystem II As Revealed by Light-Induced Fourier Transform Infrared Difference Spectroscopy

The non-heme iron is located between the quinone electron acceptors, QA and QB, in photosystem II (PSII), and together with its bicarbonate ligand, it regulates the electron and proton transfer reactions of quinone acceptors. In this study, we have investigated the structural coupling of a nearby Tyr residue with the non-heme iron center using Fourier transform infrared (FTIR) spectroscopy. Light-induced Fe2+/Fe3+ FTIR difference spectra of PSII core complexes from unlabeled and [4-13C]Tyr-labeled Thermosynechococcus elongatus revealed that the CO stretching (νCO) bands of a Tyr side chain are located at 1253 and 1241 cm−1 in the Fe2+ and Fe3+ states, respectively. Upon deuteration, both νCO bands were upshifted by 11−12 cm−1. Taking into account the criteria for determining the hydrogen bond structure of a Tyr side chain from infrared bands reported previously [Takahashi, R., and Noguchi, T. (2007) J. Phys. Chem. B 111, 13833−13844] and the results of DFT calculations of model complexes of p-cresol hydrogen-bonded with bicarbonate, we interpreted the observed νCO bands and their deuteration effects as indicating that one Tyr side chain with a hydrogen bond donor−acceptor form is strongly coupled to the non-heme iron. From the X-ray structures of PSII core complexes, it is proposed that either D1-Y246 or D2-Y244 provides a hydrogen bond to the oxygen of the bicarbonate ligand but the other Tyr does not directly interact with bicarbonate. The Tyr residue coupled to the non-heme iron may play a key role in the regulatory function of the iron−bicarbonate center by stabilizing the bicarbonate ligand and forming a rigid hydrogen bond network around the non-heme ion.