Hydrogen bonding of redox-active tyrosine Z of photosystem II probed by FTIR difference spectroscopy

The Tyr(Z)(.)/Tyr(Z) FTIR difference spectrum is reported for the first time in Mn-depleted photosystem II (PS LT)-enriched membranes of spinach, in PS II core complexes of Synechocystis sp. PCC 6803 WT, and in the mutant lacking Tyr(D) (D2-Tyr160Phe). In Synechocystis, the nu(7'a)(CO) and delta(COH) infrared modes of Tyr(Z) are proposed to account at 1279 and 1255 cm(-1). The frequency of these modes indicate that Tyr(Z) is protonated at pH 6 and involved in a strong hydrogen bond to the side chain of a histidine, probably D1-His190. A positive signal at 1512 cm(-1) is assigned to the nu(CO) mode of Tyr(Z)(.) on the basis of the 27 cm(-1) downshift observed upon C-13-Tyr labeling at the Tyr ring C4 carbon. A second TR signal, at 1532 cm(-1), is tentatively assigned to the nu(8a)(CC) mode of Tyr(Z)(.). The frequency of the nu(CO) mode of Tyr(Z)(.) at 1512 cm(-1) is comparable to that observed at 1513 cm(-1) for the Tyr(.) obtained by UV photochemistry of tyrosinate in solution, while it is higher than that of Tyr(D)(.) in WT PS II at 1503 cm(-1) and that of non-hydrogen-bonded Tyr(D)(.) in the D2-His189Gln mutant at 1497 cm(-1) [Hienerwadel, R., Boussac, A., Breton, J., Diner, B. A., and Berthomieu, C. (1997) Biochemistry 36, 14712-14723]. This latter work and the present FTIR study suggest that hydrogen bonding induces an upshift of the nu(CO) IR mode of tyrosyl radicals and that Tyr(Z)(.) forms (a) stronger hydrogen bond(s) than Tyr(D)(.) in WT PS II. Alternatively, the frequency difference between Tyr(D)(.) and Tyr(D)(.) nu(CO) modes could be explained by a more localized positive charge near the tyrosyl radical oxygen of Tyr(D)(.) than Tyr(Z)(.). The Tyr(Z)(.)/Tyr(Z) spectrum obtained in Mn-depleted PS II membranes of spinach shows large similarities with the S-3'/S-2' spectrum characteristic of radical formation in Mn-containing but Ca2+-depleted PS II, in support of the assignment using ESEEM of Tyr(Z)(.) as being responsible for the split EPR signal observed upon illumination in these conditions [Tang, X.-S., Randall, D. W., Force, D. A., Diner, B. A., and Britt, R. D. (1996) J. Am. Chem. Sec. 118, 7638-7639]. The peak at 1514 cm(-1) is assigned to the nu(CO) mode of Tyr(Z)(.) in these preparations, which indicates that Mn depletion only very slightly perturbs the immediate environment of Tyr(Z)(.) phenoxyl.