Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation

Cecilia Tommos, L. Sun, Petra Fromme, L. Hammarström, C. Zhang, S. Styring, A. W. Rutherford

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O2-based chemistry in biological systems. Light-driven water oxidation is catalysed by photosystem II, the active site of which contains a redox-active tyrosine denoted YZ, a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co-workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo-radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re-reduced by abstracting hydrogen atoms from substrate water or hydroxide-ligated to the manganese cluster. The proposed function of YZ requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of YZ in an inhibited and O2-evolving photosystem II is discussed. Domino-deprotonation from YZ to the bulk solution is shown to be consistent with a variety of data obtained on metal-depleted samples. Experimental data that suggest that the oxidation of YZ in O2-evolving samples is coupled to proton transfer in a hydrogen-bonding network are described. Finally, a dielectric-dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.

Original languageEnglish (US)
Pages (from-to)1383-1394
Number of pages12
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume357
Issue number1426
DOIs
StatePublished - Oct 29 2002
Externally publishedYes

Fingerprint

protons
hydrogen
Photosystem II Protein Complex
Protons
Hydrogen
electrons
Electrons
oxidation
electron
Atoms
Oxidation
Water
photosystem II
tyrosine
Proton transfer
Tyrosine
algae
water
Calcium Chloride
Hydrogen Bonding

Keywords

  • Oxygen-evolving complex
  • Photosynthetic water oxidation
  • Photosystem II
  • Redox-active tyrosine
  • Tyrosine radical

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation. / Tommos, Cecilia; Sun, L.; Fromme, Petra; Hammarström, L.; Zhang, C.; Styring, S.; Rutherford, A. W.

In: Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 357, No. 1426, 29.10.2002, p. 1383-1394.

Research output: Contribution to journalArticle

Tommos, Cecilia ; Sun, L. ; Fromme, Petra ; Hammarström, L. ; Zhang, C. ; Styring, S. ; Rutherford, A. W. / Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation. In: Philosophical Transactions of the Royal Society B: Biological Sciences. 2002 ; Vol. 357, No. 1426. pp. 1383-1394.
@article{52b7c8d0985740699edb425aca0cae34,
title = "Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation",
abstract = "When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O2-based chemistry in biological systems. Light-driven water oxidation is catalysed by photosystem II, the active site of which contains a redox-active tyrosine denoted YZ, a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co-workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo-radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re-reduced by abstracting hydrogen atoms from substrate water or hydroxide-ligated to the manganese cluster. The proposed function of YZ requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of YZ in an inhibited and O2-evolving photosystem II is discussed. Domino-deprotonation from YZ to the bulk solution is shown to be consistent with a variety of data obtained on metal-depleted samples. Experimental data that suggest that the oxidation of YZ in O2-evolving samples is coupled to proton transfer in a hydrogen-bonding network are described. Finally, a dielectric-dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.",
keywords = "Oxygen-evolving complex, Photosynthetic water oxidation, Photosystem II, Redox-active tyrosine, Tyrosine radical",
author = "Cecilia Tommos and L. Sun and Petra Fromme and L. Hammarstr{\"o}m and C. Zhang and S. Styring and Rutherford, {A. W.}",
year = "2002",
month = "10",
day = "29",
doi = "10.1098/rstb.2002.1135",
language = "English (US)",
volume = "357",
pages = "1383--1394",
journal = "Philosophical Transactions of the Royal Society B: Biological Sciences",
issn = "0800-4622",
publisher = "Royal Society of London",
number = "1426",

}

TY - JOUR

T1 - Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation

AU - Tommos, Cecilia

AU - Sun, L.

AU - Fromme, Petra

AU - Hammarström, L.

AU - Zhang, C.

AU - Styring, S.

AU - Rutherford, A. W.

PY - 2002/10/29

Y1 - 2002/10/29

N2 - When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O2-based chemistry in biological systems. Light-driven water oxidation is catalysed by photosystem II, the active site of which contains a redox-active tyrosine denoted YZ, a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co-workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo-radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re-reduced by abstracting hydrogen atoms from substrate water or hydroxide-ligated to the manganese cluster. The proposed function of YZ requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of YZ in an inhibited and O2-evolving photosystem II is discussed. Domino-deprotonation from YZ to the bulk solution is shown to be consistent with a variety of data obtained on metal-depleted samples. Experimental data that suggest that the oxidation of YZ in O2-evolving samples is coupled to proton transfer in a hydrogen-bonding network are described. Finally, a dielectric-dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.

AB - When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O2-based chemistry in biological systems. Light-driven water oxidation is catalysed by photosystem II, the active site of which contains a redox-active tyrosine denoted YZ, a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co-workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo-radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re-reduced by abstracting hydrogen atoms from substrate water or hydroxide-ligated to the manganese cluster. The proposed function of YZ requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of YZ in an inhibited and O2-evolving photosystem II is discussed. Domino-deprotonation from YZ to the bulk solution is shown to be consistent with a variety of data obtained on metal-depleted samples. Experimental data that suggest that the oxidation of YZ in O2-evolving samples is coupled to proton transfer in a hydrogen-bonding network are described. Finally, a dielectric-dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.

KW - Oxygen-evolving complex

KW - Photosynthetic water oxidation

KW - Photosystem II

KW - Redox-active tyrosine

KW - Tyrosine radical

UR - http://www.scopus.com/inward/record.url?scp=0037195341&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037195341&partnerID=8YFLogxK

U2 - 10.1098/rstb.2002.1135

DO - 10.1098/rstb.2002.1135

M3 - Article

C2 - 12437877

AN - SCOPUS:0037195341

VL - 357

SP - 1383

EP - 1394

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0800-4622

IS - 1426

ER -