Nickel Oxidation States of F430 Cofactor in Methyl-Coenzyme M Reductase

Jennifer L. Craft, Yih Chern Horng, Stephen W. Ragsdale, Thomas C. Brunold

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

Magnetic circular dichroism (MCD) spectroscopy and variable-temperature variable-field MCD are used in combination with density functional theory (DFT) and time-dependent DFT (TD-DFT) calculations to characterize the so-called ox1-silent, red1, and ox1 forms of the Ni-containing cofactor F430 in methyl-coenzyme M reductase (MCR). Previous studies concluded that the ox1 state, which is the precursor of the key reactive red1 state of MCR, is a Ni(I) species that derives from one-electron reduction of the Ni(II)-containing ox1-silent state. However, our absorption and MCD data provide compelling evidence that ox1 is actually a Ni(II) species. In support of this proposal, our DFT and TD-DFT calculations indicate that addition of an electron to the ox1-silent state leads to formation of a hydrocorphin anion radical rather than a Ni(I) center. These results and biochemical evidence suggest that ox1 is more oxidized than red1, which prompted us to test a new model for ox1 in which the ox1-silent species is oxidized by one electron to form a thiyl radical derived from coenzyme M that couples antiferromagnetically to the Ni(II) ion. This alternative ox1 model, formally corresponding to a Ni(III)/thiolate resonance form but with predicted S = 1/2 EPR parameters reminiscent of a Ni(I) (3dx2?y2)1 species, rationalizes the requirement for reduction of ox1 to yield the red1 species and the seemingly incongruent EPR and electronic spectra of the ox1 state.

Original languageEnglish
Pages (from-to)4068-4069
Number of pages2
JournalJournal of the American Chemical Society
Volume126
Issue number13
DOIs
Publication statusPublished - 2004 Apr 7

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Coenzymes
Circular Dichroism
Nickel
Density functional theory
Dichroism
Electrons
Oxidation
Paramagnetic resonance
Mesna
Circular dichroism spectroscopy
Magnetic Fields
Discrete Fourier transforms
Anions
Spectrum Analysis
Negative ions
Ions
Magnetic fields
Temperature
Oxidoreductases
methyl coenzyme M reductase

All Science Journal Classification (ASJC) codes

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

Cite this

Craft, Jennifer L. ; Horng, Yih Chern ; Ragsdale, Stephen W. ; Brunold, Thomas C. / Nickel Oxidation States of F430 Cofactor in Methyl-Coenzyme M Reductase. In: Journal of the American Chemical Society. 2004 ; Vol. 126, No. 13. pp. 4068-4069.
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Nickel Oxidation States of F430 Cofactor in Methyl-Coenzyme M Reductase. / Craft, Jennifer L.; Horng, Yih Chern; Ragsdale, Stephen W.; Brunold, Thomas C.

In: Journal of the American Chemical Society, Vol. 126, No. 13, 07.04.2004, p. 4068-4069.

Research output: Contribution to journalArticle

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N2 - Magnetic circular dichroism (MCD) spectroscopy and variable-temperature variable-field MCD are used in combination with density functional theory (DFT) and time-dependent DFT (TD-DFT) calculations to characterize the so-called ox1-silent, red1, and ox1 forms of the Ni-containing cofactor F430 in methyl-coenzyme M reductase (MCR). Previous studies concluded that the ox1 state, which is the precursor of the key reactive red1 state of MCR, is a Ni(I) species that derives from one-electron reduction of the Ni(II)-containing ox1-silent state. However, our absorption and MCD data provide compelling evidence that ox1 is actually a Ni(II) species. In support of this proposal, our DFT and TD-DFT calculations indicate that addition of an electron to the ox1-silent state leads to formation of a hydrocorphin anion radical rather than a Ni(I) center. These results and biochemical evidence suggest that ox1 is more oxidized than red1, which prompted us to test a new model for ox1 in which the ox1-silent species is oxidized by one electron to form a thiyl radical derived from coenzyme M that couples antiferromagnetically to the Ni(II) ion. This alternative ox1 model, formally corresponding to a Ni(III)/thiolate resonance form but with predicted S = 1/2 EPR parameters reminiscent of a Ni(I) (3dx2?y2)1 species, rationalizes the requirement for reduction of ox1 to yield the red1 species and the seemingly incongruent EPR and electronic spectra of the ox1 state.

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