Comparison of the structure of the manganese complex in the S1 and S2 states of the photosynthetic oxygen-evolving complex: an x-ray absorption spectroscopy study

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Abstract
A Mn-containing enzyme complex is involved in the oxidation of H2O to O2 in algae and higher plants. X-ray absorption spectroscopy is well suited for studying the structure and function of Mn in this enzyme complex. Results of X-ray K-edge and extended X-ray absorption fine structure (EXAFS) studies of Mn in the S1 and S2 states of the photosynthetic O2-evolving complex in photosystem II preparations from spinach are presented in this paper. The S2 state was prepared by illumination at 190 K or by illumination at 277 K in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU);these are protocols that limit the photosystem II reaction center to one turnover. Both methods produce an S2 state characterized by a multiline electron paramagnetic resonance (EPR) signal. An additional protocol, illumination at 140 K, produces a state characterized by the g = 4.1 EPR signal. We have previously observed a shift to higher energy in the X-ray absorption K-edge energy of Mn upon advancement from the dark-adapted S1 state to the S2 state produced by illumination at 190 K [Goodin, D.B., Yachandra, V.K., Britt, R.D., Sauer, K., and Klein, M.P. (1984) Biochem. Biophys. Acta 767, 209-216]. The Mn K-edge spectrum of the 277 K illuminated sample is similar to that produced at 190 K, indicating that the S2 state is similar when produced at 190 or 277 K. A similar edge shape and an edge shift of the same magnitude are seen for the 140 K illuminated sample, establishing that the S2 sate can be generated at temperatures as low as 140 K in the absence of the multiline signal. These results indicate that the g = 4.1 signal arises from oxidation of the Mn complex and that the structural differences between the species responsible for the g = 4.1 signal and the multiline EPR signal are subtle. The salient features of the Mn EXAFS results from the spinach S1 state and for the S2 state generated at 190 K are a Mn neighbor at .apprx.2.70 .ANG. and two shells of N or O at .apprx.1.75 and 2.00 .ANG., indicative of the .mu.-oxo-bridged Mn complex. These features are invariant not only for the dark S1 and 190 K illuminated S2 states but also for the S2 state prepared at 277 K, where ligand exchange is considered to be facile. We conclude from the edge and EXAFS studies that the light-induced S1 to S2 transition at 190 K or at 277 K involves a change in the oxidation state of Mn with no EXAFS-detectable change in the coordination of Mn in the O2-evolving complex.

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