Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in photosystem II as revealed by Fourier transform infrared spectroscopy

The flash-induced Fourier transform infrared (FTIR) difference spectrum of the oxygen-evolving Mn cluster upon S-1-to-S-2 transition (S-2/S-1 spectrum) was measured using photosystem II (PS II) core complexes of Synechocystis 6803 in which tyrosine residues were specifically labeled with C-13 at the ring-4 position. The double-difference spectrum between the unlabeled and labeled S-2/S-1 spectra showed that the bands at 1254 and 1521 cm(-1) downshifted by 25 and 15 cm(-1), respectively, upon ring-4-C-13-Tyr labeling. This observation indicates that there is a tyrosine residue coupled to the Mn cluster, and the vibrational modes of this tyrosine are affected upon St formation. From a comparison of the above band positions and isotopic shifts in the S-2/S-1 spectrum with those of the FTIR spectra of tyrosine in aqueous solution at pH 0.6 (Tyr-OH) and pH 13.4 (Tyr-O-) and of the Y-D(.)/Y-D FTIR difference spectrum, the 1254 and 1521 cm(-1) bands were assigned to the CO stretching and ring CC stretching modes of tyrosine, respectively, and this tyrosine was suggested to be protonated in PS II. The observation that the effect of the S-2 formation on the tyrosine bands appeared as a decrease in intensity with little frequency change could not be explained by a simple electrostatic effect by Mn oxidation, suggesting that the Mn cluster and a tyrosine are linked via chemical and/or hydrogen bonds and the structural changes of the Mn cluster are transmitted to the tyrosine through these bonds, On the basis of previous EPR studies that showed close proximity of Y-Z to the Mn cluster, Y-Z was proposed as the most probable candidate for the above tyrosine, This is the first demonstration of the structural coupling between Y-Z and the Mn cluster in an intact oxygen-evolving complex, This structural coupling may facilitate electron transfer from the Mn cluster to Yz. Our observation also provides an experimental support in favor of the proton or hydrogen atom abstraction model for the Y-Z function.