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Stepwise Disintegration of the Photosynthetic Oxygen-Evolving Complex

Tommos, Cecilia; McCracken, John; Styring, Stenbjörn LU and Babcock, Gerald T (1998) In Journal of the American Chemical Society 120(40). p.10441-10452
Abstract
Photosynthetic water oxidation catalyzed by Photosystem II takes place at a site that comprises a redox-active tyrosine, YZ, a tetramanganese cluster, and, in addition to its redox components, two inorganic cofactors, calcium and chloride. Recent work suggests that YZ and the metal site are intimately linked in the oxidation and deprotonation reactions of substrate water. The metal cluster stores oxidizing equivalents and provides binding sites for the substrate from which YZ is proposed to abstract hydrogen atoms during the catalytic cycle of photosystem II. Intrinsic to this hydrogen-abstraction mechanism for water oxidation is an intimate structural and functional relationship between the metal site and YZ, which predicts that the local... (More)
Photosynthetic water oxidation catalyzed by Photosystem II takes place at a site that comprises a redox-active tyrosine, YZ, a tetramanganese cluster, and, in addition to its redox components, two inorganic cofactors, calcium and chloride. Recent work suggests that YZ and the metal site are intimately linked in the oxidation and deprotonation reactions of substrate water. The metal cluster stores oxidizing equivalents and provides binding sites for the substrate from which YZ is proposed to abstract hydrogen atoms during the catalytic cycle of photosystem II. Intrinsic to this hydrogen-abstraction mechanism for water oxidation is an intimate structural and functional relationship between the metal site and YZ, which predicts that the local YZ environment will be sensitive to the composition and integrity of the metal cluster. To test this postulate, we have examined the YZ site and its status with respect to solvent exposure under varying degrees of disassembly of the oxygen-evolving complex. 1H2H-isotope exchange was carried out for various times in samples devoid of Mn, Ca2+, and Cl-, and in samples depleted exclusively of Ca2+. The YZ and S2YZ species were cryotrapped to high yield in these two preparations, respectively, and the radical site was characterized by using electron spin-echo envelope modulation spectroscopy. The isotope exchange at the YZ site was completed with an upper limit on the minutes time scale in both the (Mn)4-depleted and the Ca-depleted samples. The number of isotope-exchangeable protons in the site and their distances to YZ were found to be different in the two systems, indicating that YZ is shielded from the solvent in the Ca-depleted system and, upon removal of the (Mn)4 cluster, becomes accessible to bulk water. The results from an electron spin-echo analysis of S2YZ, in the weak-coupling limit, suggest that YZ in samples that retain the (Mn)4 cluster, but lack Ca2+, is involved in a bifurcated hydrogen bond. The data for both classes of samples are consistent with a hydrogen-abstraction function for YZ in water oxidation and provide insight into the light-driven assembly of the (Mn)4 cluster. (Less)
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organization
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type
Contribution to journal
publication status
published
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in
Journal of the American Chemical Society
volume
120
issue
40
pages
10441 - 10452
publisher
The American Chemical Society
external identifiers
  • scopus:0032517368
ISSN
1520-5126
DOI
10.1021/ja980281z
language
English
LU publication?
yes
id
3cec180e-eee6-4b7c-9753-dfdd6ca60015 (old id 125619)
date added to LUP
2007-07-06 17:23:53
date last changed
2017-01-01 07:05:43
@article{3cec180e-eee6-4b7c-9753-dfdd6ca60015,
  abstract     = {Photosynthetic water oxidation catalyzed by Photosystem II takes place at a site that comprises a redox-active tyrosine, YZ, a tetramanganese cluster, and, in addition to its redox components, two inorganic cofactors, calcium and chloride. Recent work suggests that YZ and the metal site are intimately linked in the oxidation and deprotonation reactions of substrate water. The metal cluster stores oxidizing equivalents and provides binding sites for the substrate from which YZ is proposed to abstract hydrogen atoms during the catalytic cycle of photosystem II. Intrinsic to this hydrogen-abstraction mechanism for water oxidation is an intimate structural and functional relationship between the metal site and YZ, which predicts that the local YZ environment will be sensitive to the composition and integrity of the metal cluster. To test this postulate, we have examined the YZ site and its status with respect to solvent exposure under varying degrees of disassembly of the oxygen-evolving complex. 1H2H-isotope exchange was carried out for various times in samples devoid of Mn, Ca2+, and Cl-, and in samples depleted exclusively of Ca2+. The YZ and S2YZ species were cryotrapped to high yield in these two preparations, respectively, and the radical site was characterized by using electron spin-echo envelope modulation spectroscopy. The isotope exchange at the YZ site was completed with an upper limit on the minutes time scale in both the (Mn)4-depleted and the Ca-depleted samples. The number of isotope-exchangeable protons in the site and their distances to YZ were found to be different in the two systems, indicating that YZ is shielded from the solvent in the Ca-depleted system and, upon removal of the (Mn)4 cluster, becomes accessible to bulk water. The results from an electron spin-echo analysis of S2YZ, in the weak-coupling limit, suggest that YZ in samples that retain the (Mn)4 cluster, but lack Ca2+, is involved in a bifurcated hydrogen bond. The data for both classes of samples are consistent with a hydrogen-abstraction function for YZ in water oxidation and provide insight into the light-driven assembly of the (Mn)4 cluster.},
  author       = {Tommos, Cecilia and McCracken, John and Styring, Stenbjörn and Babcock, Gerald T},
  issn         = {1520-5126},
  language     = {eng},
  number       = {40},
  pages        = {10441--10452},
  publisher    = {The American Chemical Society},
  series       = {Journal of the American Chemical Society},
  title        = {Stepwise Disintegration of the Photosynthetic Oxygen-Evolving Complex},
  url          = {http://dx.doi.org/10.1021/ja980281z},
  volume       = {120},
  year         = {1998},
}