Photosynthetic Oxygen Evolution: Changes in Magnetism of the Water-Oxidizing Enzyme

M. Sivaraja, Gerard Dismukes, J. S. Philo, J. Lary

Research output: Contribution to journalArticle

39 Citations (Scopus)

Abstract

Changes in magnetic susceptibility produced by single-turnover flashes of light have been measured for the first time for four of the oxidation states, so-called S states, produced during oxygen evolution in Photosystem II (PSII) complexes of spinach. The data reveal new insights into the structure and bonding of the manganese cluster responsible for catalysis of water oxidation. In samples that have been dark adapted for 15 min or longer to favor population of the “resting” S1 state, a train of six flashes increases the paramagnetism on flashes 1, 3, and 5, while no or small increases are observed on flashes 2, 4, and 6. Advancement to the S1 state does not restore the dark level of S1 magnetism. This is due to two effects: formation of net paramagnetism from 02 release on the S4→ S0 reaction (scavengeable by glucose oxidase) and a large increase in magnetism for the S^resting) → S2reaction, which is not restored without dark readaptation. Comparison of these data with models proposed for the structure of the manganese site reveals that models in which oxidation of substrate water occurs prior to S4or oxidation of magnetically isolated Mn ions cannot account for the susceptibility changes observed. The large increase of 17 μB 2/PSII observed for the S1(resting)→S2oxidation is opposite in sign to the decrease in paramagnetism reported for oxidation of synthetic Mn dimers containing the μ2-OXO-di-μ2-Carboxylato and di-μ2-OXO-μ2-carboxylato bridges undergoing the oxidation Mn2(III,III) → Mn2(III,IV). Consequently, these complexes must not provide complete structural representations of the bridging geometry or ligand types in the enzyme. The increase in susceptibility can be understood in terms of reduced antiferromagnetic coupling within a higher nuclearity cluster of three or four magnetically interacting Mn ions. This nuclearity is consistent with earlier EPR data.

Original languageEnglish (US)
Pages (from-to)3221-3225
Number of pages5
JournalJournal of the American Chemical Society
Volume111
Issue number9
DOIs
StatePublished - Jan 1 1989
Externally publishedYes

Fingerprint

Photosystem II Protein Complex
Magnetism
Manganese
Enzymes
Ions
Oxygen
Paramagnetism
Oxidation
Glucose Oxidase
Spinacia oleracea
Water
Catalysis
Ligands
Light
Population
Glucose oxidase
Magnetic susceptibility
Dimers
Paramagnetic resonance
Geometry

All Science Journal Classification (ASJC) codes

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

@article{403ee1b1859849b086c2920d4ce56644,
title = "Photosynthetic Oxygen Evolution: Changes in Magnetism of the Water-Oxidizing Enzyme",
abstract = "Changes in magnetic susceptibility produced by single-turnover flashes of light have been measured for the first time for four of the oxidation states, so-called S states, produced during oxygen evolution in Photosystem II (PSII) complexes of spinach. The data reveal new insights into the structure and bonding of the manganese cluster responsible for catalysis of water oxidation. In samples that have been dark adapted for 15 min or longer to favor population of the “resting” S1 state, a train of six flashes increases the paramagnetism on flashes 1, 3, and 5, while no or small increases are observed on flashes 2, 4, and 6. Advancement to the S1 state does not restore the dark level of S1 magnetism. This is due to two effects: formation of net paramagnetism from 02 release on the S4→ S0 reaction (scavengeable by glucose oxidase) and a large increase in magnetism for the S^resting) → S2reaction, which is not restored without dark readaptation. Comparison of these data with models proposed for the structure of the manganese site reveals that models in which oxidation of substrate water occurs prior to S4or oxidation of magnetically isolated Mn ions cannot account for the susceptibility changes observed. The large increase of 17 μB 2/PSII observed for the S1(resting)→S2oxidation is opposite in sign to the decrease in paramagnetism reported for oxidation of synthetic Mn dimers containing the μ2-OXO-di-μ2-Carboxylato and di-μ2-OXO-μ2-carboxylato bridges undergoing the oxidation Mn2(III,III) → Mn2(III,IV). Consequently, these complexes must not provide complete structural representations of the bridging geometry or ligand types in the enzyme. The increase in susceptibility can be understood in terms of reduced antiferromagnetic coupling within a higher nuclearity cluster of three or four magnetically interacting Mn ions. This nuclearity is consistent with earlier EPR data.",
author = "M. Sivaraja and Gerard Dismukes and Philo, {J. S.} and J. Lary",
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Photosynthetic Oxygen Evolution : Changes in Magnetism of the Water-Oxidizing Enzyme. / Sivaraja, M.; Dismukes, Gerard; Philo, J. S.; Lary, J.

In: Journal of the American Chemical Society, Vol. 111, No. 9, 01.01.1989, p. 3221-3225.

Research output: Contribution to journalArticle

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T1 - Photosynthetic Oxygen Evolution

T2 - Changes in Magnetism of the Water-Oxidizing Enzyme

AU - Sivaraja, M.

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AU - Lary, J.

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AB - Changes in magnetic susceptibility produced by single-turnover flashes of light have been measured for the first time for four of the oxidation states, so-called S states, produced during oxygen evolution in Photosystem II (PSII) complexes of spinach. The data reveal new insights into the structure and bonding of the manganese cluster responsible for catalysis of water oxidation. In samples that have been dark adapted for 15 min or longer to favor population of the “resting” S1 state, a train of six flashes increases the paramagnetism on flashes 1, 3, and 5, while no or small increases are observed on flashes 2, 4, and 6. Advancement to the S1 state does not restore the dark level of S1 magnetism. This is due to two effects: formation of net paramagnetism from 02 release on the S4→ S0 reaction (scavengeable by glucose oxidase) and a large increase in magnetism for the S^resting) → S2reaction, which is not restored without dark readaptation. Comparison of these data with models proposed for the structure of the manganese site reveals that models in which oxidation of substrate water occurs prior to S4or oxidation of magnetically isolated Mn ions cannot account for the susceptibility changes observed. The large increase of 17 μB 2/PSII observed for the S1(resting)→S2oxidation is opposite in sign to the decrease in paramagnetism reported for oxidation of synthetic Mn dimers containing the μ2-OXO-di-μ2-Carboxylato and di-μ2-OXO-μ2-carboxylato bridges undergoing the oxidation Mn2(III,III) → Mn2(III,IV). Consequently, these complexes must not provide complete structural representations of the bridging geometry or ligand types in the enzyme. The increase in susceptibility can be understood in terms of reduced antiferromagnetic coupling within a higher nuclearity cluster of three or four magnetically interacting Mn ions. This nuclearity is consistent with earlier EPR data.

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