Histidine 332 of the D1 polypeptide modulates the magnetic and redox properties of the manganese cluster and tyrosine Y-Z in photosystem II

An electron spin-echo envelope modulation study [Tang, X.-S., Diner, B. A., Larsen, B. S., Gilchrist, M. L., Jr., Lorigan, G. A., and Britt, R. D. (19 94) Proc. Natl. Acad. Sci. U.S.A. 91, 704-708] and a recent Fourier transfo rm infrared study [Noguchi, T., Inoue, Y., and Tang, X.-S. (1999) Biochemis try 38, 10187-10195], both conducted with [N-15]histidine-labeled photosyst em II particles, show that at least one histidine residue coordinates the O -2-evolving Mn cluster in photosystem Il. Evidence obtained from site-direc ted mutagenesis studies suggests that one of these residues may be His332 o f the D1 polypeptide. The mutation D1-H332E is of particular interest becau se cells of the cyanobacterium Synechocystis sp. PCC 6803 that contain this mutation evolve no O-2 but appear to assemble Mn clusters in nearly all ph otosystem II reaction centers [Chu, H.-A., Nguyen, A. P., and Debus, R. J. (1995) Biochemistry 34, 5859-5882]. Photosystem II particles isolated from the Synechocystis D1-H332E mutant are characterized in this study. Intact D 1-H332E photosystem II particles exhibit an altered S-2 state multiline EPR signal that has more hyperfine lines and narrower splittings than the S-2 State multiline EPR signal observed in wild-type* PSII particles. However, the quantum yield for oxidizing the S-1 state Mn cluster is very low, corre sponding to an 8000-fold slowing of the rate of Mn oxidation by Y-Z(.), and the temperature threshold for forming the S-2 State is approximately 100 K higher than in wild-type PSII preparations. Furthermore. the D1-H332E PSII particles are unable to advance beyond the (YZS2)-S-. state, as shown by t he accumulation of a narrow "split" EPR signal under multiple turnover cond itions. In Mn-depleted photosystem II particles, charge recombination betwe en Q(A)(.-) and Y-Z(.) in D1-H332E is accelerated in comparison to wild-typ e*, showing that the mutation alters the redox properties of Y-Z in additio n to those of the Mn cluster. These results are consistent with D1-His332 b eing located near the Mn-Y-Z complex and perhaps ligating Mn.