Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0) Characterized by X-ray absorption spectroscopy at 20 K and room temperature

被引:270
作者
Haumann, M
Müller, C
Liebisch, P
Iuzzolino, L
Dittmer, J
Grabolle, M
Neisius, T
Meyer-Klaucke, W
Dau, H [1 ]
机构
[1] Free Univ Berlin, Fachbereich Phys, Arnimallee 14, D-14195 Berlin, Germany
[2] Univ Marburg, D-35032 Marburg, Germany
[3] European Synchrotron Radiat Facil, F-38043 Grenoble, France
[4] EMBL Outstn Hamburg, D-22603 Hamburg, Germany
关键词
D O I
10.1021/bi048697e
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Structural and electronic changes (oxidation states) of the Mn4Ca complex of photosystem 11 (PSII) in the water oxidation cycle are of prime interest. For all four transitions between semistable S-states (S-0 --> S-1, S-1 --> S-2, S-2 --> S-3, and S-3,S-4 --> S-0), oxidation state and structural changes of the Mn complex were investigated by X-ray absorption spectroscopy (XAS) not only at 20 K but also at room temperature (RT) where water oxidation is functional. Three distinct experimental approaches were used: (1) illumination-freeze approach (XAS at 20 K), (2) flash-and-rapid-scan approach (RT), and (3) a novel time scan/sampling-XAS method (RT) facilitating particularly direct monitoring of the spectral changes in the S-state cycle. The rate of X-ray photoreduction was quantitatively assessed, and it was thus verified that the Mn ions remained in their initial oxidation state throughout the data collection period (>90%, at 20 K and at RT, for all S-states). Analysis of the complete XANES and EXAFS data sets (20 K and RT data, S-0-S-3, XANES and EXAFS) obtained by the three approaches leads to the following conclusions. (i) In all S-states, the gross structural and electronic features of the Mn complex are similar at 20 K and room temperature. There are no indications for significant temperature-dependent variations in structure, protonation state, or charge localization. (ii) Mn-centered oxidation likely occurs on each of the three S-state transitions, leading to the S3 state. (iii) Significant structural changes are coupled to the S-0 --> S-1 and the S-2 --> S-3 transitions which are identified as changes in the Mn-Mn bridging mode. We propose that in the S-2 --> S-3 transition a third Mn-(mu-O)(2)-Mn unit is formed, whereas the S-0 --> S-1 transition involves deprotonation of mu-hydroxo bridge. In light of these results, the mechanism of accumulation of four oxidation equivalents by the Mn complex and possible implications for formation of the O-O bond are considered.
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页码:1894 / 1908
页数:15
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