EPR-ENDOR characterization of ( 17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II

Iain L. McConnell, Vladimir M. Grigoryants, Charles P. Scholes, William K. Myers, Ping Yu Chen, James W. Whittaker, Gary W Brudvig

Research output: Contribution to journalArticle

64 Citations (Scopus)

Abstract

The synthesis of efficient water-oxidation catalysts demands insight into the only known, naturally occurring water-oxidation catalyst, the oxygen-evolving complex (OEC) of photosystem II (PSII). Understanding the water oxidation mechanism requires knowledge of where and when substrate water binds to the OEC. Mn catalase in its Mn(III)-Mn(IV) state is a protein model of the OEC's S 2 state. From 17O-labeled water exchanged into the di-μ-oxo di-Mn(III,IV) coordination sphere of Mn catalase, CW Q-band ENDOR spectroscopy revealed two distinctly different 17O signals incorporated in distinctly different time regimes. First, a signal appearing after 2 h of 17O exchange was detected with a 13.0 MHz hyperfine coupling. From similarity in the time scale of isotope incorporation and in the 17O μ-oxo hyperfine coupling of the di-μ-oxo di-Mn(III,IV) bipyridine model (Usov, O. M.; Grigoryants, V. M.; Tagore, R.; Brudvig, G. W.; Scholes, C. P.J. Am. Chem. Soc. 2007, 129, 11886-11887), this signal was assigned to μ-oxo oxygen. EPR line broadening was obvious from this 17O μ-oxo species. Earlier exchange proceeded on the minute or faster time scale into a non-μ-oxo position, from which 17O ENDOR showed a smaller 3.8 MHz hyperfine coupling and possible quadrupole splittings, indicating a terminal water of Mn(III). Exchangeable proton/deuteron hyperfine couplings, consistent with terminal water ligation to Mn(III), also appeared. Q-band CW ENDOR from the S 2 state of the OEC was obtained following multihour 17O exchange, which showed a 17O hyperfine signal with a 11 MHz hyperfine coupling, tentatively assigned as μ-oxo- 17O by resemblance to the μ-oxo signals from Mn catalase and the di-μ-oxo di-Mn(III,IV) bipyridine model.

Original languageEnglish
Pages (from-to)1504-1512
Number of pages9
JournalJournal of the American Chemical Society
Volume134
Issue number3
DOIs
Publication statusPublished - Jan 25 2012

Fingerprint

Photosystem II Protein Complex
Electron Spin Resonance Spectroscopy
Catalase
Manganese
Paramagnetic resonance
Oxygen
Water
Oxidation
Catalysts
Deuterium
Isotopes
Ligation
Protons
Spectrum Analysis
Spectroscopy
Proteins
Substrates

ASJC Scopus subject areas

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

Cite this

EPR-ENDOR characterization of ( 17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II. / McConnell, Iain L.; Grigoryants, Vladimir M.; Scholes, Charles P.; Myers, William K.; Chen, Ping Yu; Whittaker, James W.; Brudvig, Gary W.

In: Journal of the American Chemical Society, Vol. 134, No. 3, 25.01.2012, p. 1504-1512.

Research output: Contribution to journalArticle

McConnell, Iain L. ; Grigoryants, Vladimir M. ; Scholes, Charles P. ; Myers, William K. ; Chen, Ping Yu ; Whittaker, James W. ; Brudvig, Gary W. / EPR-ENDOR characterization of ( 17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II. In: Journal of the American Chemical Society. 2012 ; Vol. 134, No. 3. pp. 1504-1512.
@article{d7f08e44e38b4ab5ac978ca8627f5229,
title = "EPR-ENDOR characterization of ( 17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II",
abstract = "The synthesis of efficient water-oxidation catalysts demands insight into the only known, naturally occurring water-oxidation catalyst, the oxygen-evolving complex (OEC) of photosystem II (PSII). Understanding the water oxidation mechanism requires knowledge of where and when substrate water binds to the OEC. Mn catalase in its Mn(III)-Mn(IV) state is a protein model of the OEC's S 2 state. From 17O-labeled water exchanged into the di-μ-oxo di-Mn(III,IV) coordination sphere of Mn catalase, CW Q-band ENDOR spectroscopy revealed two distinctly different 17O signals incorporated in distinctly different time regimes. First, a signal appearing after 2 h of 17O exchange was detected with a 13.0 MHz hyperfine coupling. From similarity in the time scale of isotope incorporation and in the 17O μ-oxo hyperfine coupling of the di-μ-oxo di-Mn(III,IV) bipyridine model (Usov, O. M.; Grigoryants, V. M.; Tagore, R.; Brudvig, G. W.; Scholes, C. P.J. Am. Chem. Soc. 2007, 129, 11886-11887), this signal was assigned to μ-oxo oxygen. EPR line broadening was obvious from this 17O μ-oxo species. Earlier exchange proceeded on the minute or faster time scale into a non-μ-oxo position, from which 17O ENDOR showed a smaller 3.8 MHz hyperfine coupling and possible quadrupole splittings, indicating a terminal water of Mn(III). Exchangeable proton/deuteron hyperfine couplings, consistent with terminal water ligation to Mn(III), also appeared. Q-band CW ENDOR from the S 2 state of the OEC was obtained following multihour 17O exchange, which showed a 17O hyperfine signal with a 11 MHz hyperfine coupling, tentatively assigned as μ-oxo- 17O by resemblance to the μ-oxo signals from Mn catalase and the di-μ-oxo di-Mn(III,IV) bipyridine model.",
author = "McConnell, {Iain L.} and Grigoryants, {Vladimir M.} and Scholes, {Charles P.} and Myers, {William K.} and Chen, {Ping Yu} and Whittaker, {James W.} and Brudvig, {Gary W}",
year = "2012",
month = "1",
day = "25",
doi = "10.1021/ja203465y",
language = "English",
volume = "134",
pages = "1504--1512",
journal = "Journal of the American Chemical Society",
issn = "0002-7863",
publisher = "American Chemical Society",
number = "3",

}

TY - JOUR

T1 - EPR-ENDOR characterization of ( 17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II

AU - McConnell, Iain L.

AU - Grigoryants, Vladimir M.

AU - Scholes, Charles P.

AU - Myers, William K.

AU - Chen, Ping Yu

AU - Whittaker, James W.

AU - Brudvig, Gary W

PY - 2012/1/25

Y1 - 2012/1/25

N2 - The synthesis of efficient water-oxidation catalysts demands insight into the only known, naturally occurring water-oxidation catalyst, the oxygen-evolving complex (OEC) of photosystem II (PSII). Understanding the water oxidation mechanism requires knowledge of where and when substrate water binds to the OEC. Mn catalase in its Mn(III)-Mn(IV) state is a protein model of the OEC's S 2 state. From 17O-labeled water exchanged into the di-μ-oxo di-Mn(III,IV) coordination sphere of Mn catalase, CW Q-band ENDOR spectroscopy revealed two distinctly different 17O signals incorporated in distinctly different time regimes. First, a signal appearing after 2 h of 17O exchange was detected with a 13.0 MHz hyperfine coupling. From similarity in the time scale of isotope incorporation and in the 17O μ-oxo hyperfine coupling of the di-μ-oxo di-Mn(III,IV) bipyridine model (Usov, O. M.; Grigoryants, V. M.; Tagore, R.; Brudvig, G. W.; Scholes, C. P.J. Am. Chem. Soc. 2007, 129, 11886-11887), this signal was assigned to μ-oxo oxygen. EPR line broadening was obvious from this 17O μ-oxo species. Earlier exchange proceeded on the minute or faster time scale into a non-μ-oxo position, from which 17O ENDOR showed a smaller 3.8 MHz hyperfine coupling and possible quadrupole splittings, indicating a terminal water of Mn(III). Exchangeable proton/deuteron hyperfine couplings, consistent with terminal water ligation to Mn(III), also appeared. Q-band CW ENDOR from the S 2 state of the OEC was obtained following multihour 17O exchange, which showed a 17O hyperfine signal with a 11 MHz hyperfine coupling, tentatively assigned as μ-oxo- 17O by resemblance to the μ-oxo signals from Mn catalase and the di-μ-oxo di-Mn(III,IV) bipyridine model.

AB - The synthesis of efficient water-oxidation catalysts demands insight into the only known, naturally occurring water-oxidation catalyst, the oxygen-evolving complex (OEC) of photosystem II (PSII). Understanding the water oxidation mechanism requires knowledge of where and when substrate water binds to the OEC. Mn catalase in its Mn(III)-Mn(IV) state is a protein model of the OEC's S 2 state. From 17O-labeled water exchanged into the di-μ-oxo di-Mn(III,IV) coordination sphere of Mn catalase, CW Q-band ENDOR spectroscopy revealed two distinctly different 17O signals incorporated in distinctly different time regimes. First, a signal appearing after 2 h of 17O exchange was detected with a 13.0 MHz hyperfine coupling. From similarity in the time scale of isotope incorporation and in the 17O μ-oxo hyperfine coupling of the di-μ-oxo di-Mn(III,IV) bipyridine model (Usov, O. M.; Grigoryants, V. M.; Tagore, R.; Brudvig, G. W.; Scholes, C. P.J. Am. Chem. Soc. 2007, 129, 11886-11887), this signal was assigned to μ-oxo oxygen. EPR line broadening was obvious from this 17O μ-oxo species. Earlier exchange proceeded on the minute or faster time scale into a non-μ-oxo position, from which 17O ENDOR showed a smaller 3.8 MHz hyperfine coupling and possible quadrupole splittings, indicating a terminal water of Mn(III). Exchangeable proton/deuteron hyperfine couplings, consistent with terminal water ligation to Mn(III), also appeared. Q-band CW ENDOR from the S 2 state of the OEC was obtained following multihour 17O exchange, which showed a 17O hyperfine signal with a 11 MHz hyperfine coupling, tentatively assigned as μ-oxo- 17O by resemblance to the μ-oxo signals from Mn catalase and the di-μ-oxo di-Mn(III,IV) bipyridine model.

UR - http://www.scopus.com/inward/record.url?scp=84863393528&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84863393528&partnerID=8YFLogxK

U2 - 10.1021/ja203465y

DO - 10.1021/ja203465y

M3 - Article

C2 - 22142421

AN - SCOPUS:84863393528

VL - 134

SP - 1504

EP - 1512

JO - Journal of the American Chemical Society

JF - Journal of the American Chemical Society

SN - 0002-7863

IS - 3

ER -