skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: X-ray spectroscopy of the photosynthetic oxygen-evolving complex

Abstract

Water oxidation to dioxygen in photosynthesis is catalyzed by a Mn4Ca cluster with O bridging in Photosystem II (PS II) of plants, algae and cyanobacteria. A variety of spectroscopic methods have been applied to analyzing the participation of the complex. X-ray spectroscopy is particularly useful because it is element-specific, and because it can reveal important structural features of the complex with high accuracy and identify the participation of Mn in the redox chemistry. Following a brief history of the application of X-ray spectroscopy to PS II, an overview of newer results will be presented and a description of the present state of our knowledge based on this approach.

Authors:
; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
Physical Biosciences Division
OSTI Identifier:
971437
Report Number(s):
LBNL-2318E
Journal ID: 0010-8545
DOE Contract Number:
DE-AC02-05CH11231; GM55302
Resource Type:
Journal Article
Resource Relation:
Journal Name: Coordination Chemistry Reviews
Country of Publication:
United States
Language:
English
Subject:
59; 37; Photosystem II; X-ray spectroscopy; Water oxidation; Manganese enzyme

Citation Formats

Sauer, Ken, Yano, Junko, and Yachandra, Vittal K. X-ray spectroscopy of the photosynthetic oxygen-evolving complex. United States: N. p., 2007. Web.
Sauer, Ken, Yano, Junko, & Yachandra, Vittal K. X-ray spectroscopy of the photosynthetic oxygen-evolving complex. United States.
Sauer, Ken, Yano, Junko, and Yachandra, Vittal K. Thu . "X-ray spectroscopy of the photosynthetic oxygen-evolving complex". United States. doi:. https://www.osti.gov/servlets/purl/971437.
@article{osti_971437,
title = {X-ray spectroscopy of the photosynthetic oxygen-evolving complex},
author = {Sauer, Ken and Yano, Junko and Yachandra, Vittal K},
abstractNote = {Water oxidation to dioxygen in photosynthesis is catalyzed by a Mn4Ca cluster with O bridging in Photosystem II (PS II) of plants, algae and cyanobacteria. A variety of spectroscopic methods have been applied to analyzing the participation of the complex. X-ray spectroscopy is particularly useful because it is element-specific, and because it can reveal important structural features of the complex with high accuracy and identify the participation of Mn in the redox chemistry. Following a brief history of the application of X-ray spectroscopy to PS II, an overview of newer results will be presented and a description of the present state of our knowledge based on this approach.},
doi = {},
journal = {Coordination Chemistry Reviews},
number = ,
volume = ,
place = {United States},
year = {Thu Apr 05 00:00:00 EDT 2007},
month = {Thu Apr 05 00:00:00 EDT 2007}
}
  • Water oxidation to dioxygen in photosynthesis is catalyzed by a Mn{sub 4}Ca cluster with O bridging in Photosystem II (PS II) of plants, algae and cyanobacteria. A variety of spectroscopic methods have been applied to analyzing the participation of the complex. X-ray spectroscopy is particularly useful because it is element-specific, and because it can reveal important structural features of the complex with high accuracy and identify the participation of Mn in the redox chemistry. Following a brief history of the application of X-ray spectroscopy to PS II, an overview of newer results will be presented and a description of themore » present state of our knowledge based on this approach.« less
  • Manganese x-ray absorption spectra (XAS) are reported for the S{sub 1} state of highly purified, highly concentrated preparations of the oxygen-evolving complex (OEC) from photosystem II (PSII). Improvements in concentration (ca. 1.5 mM Mn) and detection efficiency (13-element solid-state detector array) have permitted a substantial improvement in data quality relative to previous solution XAS studies of PSII. Principal findings are that there is no need to include a shell of oxygens at ca. 1.75 {angstrom} in order to account for the Mn EXAFS, that there are 2-3 Mn-Mn distances of ca. 2.7 {angstrom}, and that there are one and possiblymore » two shells of additional scatterers at longer distance (ca. 3.3 and 4.2 {angstrom}) from the Mn. Even with this higher quality data, it is not possible to use EXAFS to determine whether chloride is coordinated to the Mn. The structure consequences of these results are discussed in the context of proposed structural models. It is concluded that neither a cubane nor previously prepared butterfly type clusters can account for the observed features.« less
  • A Mn-containing enzyme complex is involved in the oxidation of H/sub 2/O to O/sub 2/ 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 S/sub 1/ and S/sub 2/ states of the photosynthetic O/sub 2/-evolving complex in photosystem II preparations from spinach are presented in this paper. The S/sub 2/ 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);more » these are protocols that limit the photosystem II reaction center to one turnover. Both methods produce an S/sub 2/ 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. The authors have previously observed a shift to higher energy in the X-ray absorption K-edge energy of Mn upon advancement from the dark-adapted S/sub 1/ state to the S/sub 2/ state produced by illumination at 190 K. The Mn K-edge spectrum of the 277 K illuminated sample is similar to that produced at 190 K, indicating that the S/sub 2/ 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. 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. They conclude from the edge and EXAFS studies that the light-induced S/sub 1/ to S/sub 2/ 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 O/sub 2/-evolving complex.« less
  • X-ray absorption spectroscopy (XAS) has been used to characterize the structural consequences of Ca{sup 2+} replacement in the reaction center complex of the photosynthetic oxygen-evolving complex (OEC). EPR and activity measurements demonstrate that, in the absence of the 17 and 23 kDa extrinsic polypeptides, it is not necessary to use either low pH or Ca chelators to effect complete replacement of the active site Ca{sup 2+} by Sr{sup 2+}, Dy{sup 3+}, or La{sup 3+}. The extended X-ray absorption fine structure (EXAFS) spectra for the OEC show evidence for a Mn...Mn interaction at ca. 3.3 A that could arise either frommore » Mn...Mn scattering within the Mn cluster or Mn...Ca scattering between the Mn cluster and the inorganic Ca{sup 2+} cofactor. There is no significant change in either the amplitude or the phase of this feature when Ca{sup 2+} is replaced by Sr{sup 2+} or Dy{sup 3+}, thus demonstrating that there is no EXAFS-detectable Mn...Ca contribution at ca. 3.3 A in these samples. The only significant consequence of Ca{sup 2+} replacement is a small change in the ca. 2.7 A Mn...Mn distance. The average Mn...Mn distance decreases 0.014 A when Ca{sup 2+} is replaced by Sr{sup 2+} and increases 0.012 A when Ca{sup 2+} is replaced by Dy{sup 3+}. 75 refs., 10 figs., 5 tabs.« less
  • The oxygen-evolving complex of photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S0-S4) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S1 and S2 states. The proposed model consists ofmore » two di-mu-oxo bridged binuclear Mn units with Mn-Mn distances of {approximately}2.7 Angstrom that are linked to each other by a mono-mu-oxo bridge with a Mn-Mn separation of {approximately}3.3 Angstrom. The Mn-Mn distances are invariant in the S1 and S2 states. This report describes the application of X-ray absorption spectroscopy to S3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S3 state compared to the S1 and the S2 states. The two 2.7 Angstrom Mn-Mn distances that characterize the di-mu-oxo centers are both lengthened to {approximately}2.8 and 3.0 Angstrom. The 3.3 Angstrom Mn-Mn and Mn-Ca distance also increases by 0.04-0.2 Angstrom. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate water oxidation in the S3 state. Mn-centered oxidation is evident during the S0 to S1 and S1 to S2 transitions. During the S2 to S3 transition, we propose that the changes in Mn-Mn distances are the consequence of ligand or water oxidation. Models that can account for such changes and the implications for the mechanism of water oxidation are discussed.« less