Spectroscopic and computational characterization of the nickel-containing F430 cofactor of methyl-coenzyme M reductase

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

Research output: Contribution to journalArticle

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Abstract

Methyl-coenzyme M reductase (MCR) catalyzes the terminal reaction in methanogenesis, the formation of methane from methyl-coenzyme M and coenzyme B. The active site of MCR binds the prosthetic group F430, a unique nickel hydrocorphin cofactor. Here, spectroscopy and computations are employed in developing detailed electronic descriptions of the Ni(II) and Ni(I) forms of the free cofactor. Absorption, magnetic circular dichroism (MCD), and variable-temperature variable-field MCD data are analyzed within the framework of time-dependent DFT computations to assign key electronic transitions. DFT calculations are further employed to evaluate possible reduced F430 models-a one-electron reduced Ni(I)F430 model and a three-electron reduced Ni(I)Fred430 model (possessing a reduced hydrocorphin ligand)-on the basis of excited-state spectra and published EPR/ENDOR parameters. While calculations on both models yield spectroscopic parameters that are consistent with most experimental data, overall better agreement is achieved using the Ni(I)F430 model, particularly with respect to electronic absorption and 1H ENDOR. The experimentally validated bonding descriptions generated herein show that in Ni(II)F430 the occupied Ni 3d orbitals are too low in energy to significantly perturb the dominant electronic transition involving the π and π* frontier MOs of the macrocycle (i.e., the HOMO → LUMO transition). Upon one-electron reduction of the Ni(II) ion, the occupied Ni 3d orbitals are raised in energy, shifting between the HOMO and the LUMO of the oxidized cofactor. These ground-state changes have a dramatic effect on the excited-state structure, causing a blue shift of the dominant π → π* transition and the appearance of numerous Ni 3d → hydrocorphin π* charge-transfer features in the vis/near-IR region.

Original languageEnglish
Pages (from-to)77-89
Number of pages13
JournalJournal of Biological Inorganic Chemistry
Volume9
Issue number1
DOIs
Publication statusPublished - 2004 Jan 1

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Nickel
Electron Spin Resonance Spectroscopy
Electrons
Circular Dichroism
Excited states
Discrete Fourier transforms
Methane
Magnetic Fields
Catalytic Domain
Spectrum Analysis
Ions
Ligands
Electron transitions
Prosthetics
Temperature
Ground state
Paramagnetic resonance
Charge transfer
methyl coenzyme M reductase
Spectroscopy

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Inorganic Chemistry

Cite this

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title = "Spectroscopic and computational characterization of the nickel-containing F430 cofactor of methyl-coenzyme M reductase",
abstract = "Methyl-coenzyme M reductase (MCR) catalyzes the terminal reaction in methanogenesis, the formation of methane from methyl-coenzyme M and coenzyme B. The active site of MCR binds the prosthetic group F430, a unique nickel hydrocorphin cofactor. Here, spectroscopy and computations are employed in developing detailed electronic descriptions of the Ni(II) and Ni(I) forms of the free cofactor. Absorption, magnetic circular dichroism (MCD), and variable-temperature variable-field MCD data are analyzed within the framework of time-dependent DFT computations to assign key electronic transitions. DFT calculations are further employed to evaluate possible reduced F430 models-a one-electron reduced Ni(I)F430 model and a three-electron reduced Ni(I)Fred430 model (possessing a reduced hydrocorphin ligand)-on the basis of excited-state spectra and published EPR/ENDOR parameters. While calculations on both models yield spectroscopic parameters that are consistent with most experimental data, overall better agreement is achieved using the Ni(I)F430 model, particularly with respect to electronic absorption and 1H ENDOR. The experimentally validated bonding descriptions generated herein show that in Ni(II)F430 the occupied Ni 3d orbitals are too low in energy to significantly perturb the dominant electronic transition involving the π and π* frontier MOs of the macrocycle (i.e., the HOMO → LUMO transition). Upon one-electron reduction of the Ni(II) ion, the occupied Ni 3d orbitals are raised in energy, shifting between the HOMO and the LUMO of the oxidized cofactor. These ground-state changes have a dramatic effect on the excited-state structure, causing a blue shift of the dominant π → π* transition and the appearance of numerous Ni 3d → hydrocorphin π* charge-transfer features in the vis/near-IR region.",
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Spectroscopic and computational characterization of the nickel-containing F430 cofactor of methyl-coenzyme M reductase. / Craft, Jennifer L.; Horng, Yih-Chern; Ragsdale, Stephen W.; Brunold, Thomas C.

In: Journal of Biological Inorganic Chemistry, Vol. 9, No. 1, 01.01.2004, p. 77-89.

Research output: Contribution to journalArticle

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N2 - Methyl-coenzyme M reductase (MCR) catalyzes the terminal reaction in methanogenesis, the formation of methane from methyl-coenzyme M and coenzyme B. The active site of MCR binds the prosthetic group F430, a unique nickel hydrocorphin cofactor. Here, spectroscopy and computations are employed in developing detailed electronic descriptions of the Ni(II) and Ni(I) forms of the free cofactor. Absorption, magnetic circular dichroism (MCD), and variable-temperature variable-field MCD data are analyzed within the framework of time-dependent DFT computations to assign key electronic transitions. DFT calculations are further employed to evaluate possible reduced F430 models-a one-electron reduced Ni(I)F430 model and a three-electron reduced Ni(I)Fred430 model (possessing a reduced hydrocorphin ligand)-on the basis of excited-state spectra and published EPR/ENDOR parameters. While calculations on both models yield spectroscopic parameters that are consistent with most experimental data, overall better agreement is achieved using the Ni(I)F430 model, particularly with respect to electronic absorption and 1H ENDOR. The experimentally validated bonding descriptions generated herein show that in Ni(II)F430 the occupied Ni 3d orbitals are too low in energy to significantly perturb the dominant electronic transition involving the π and π* frontier MOs of the macrocycle (i.e., the HOMO → LUMO transition). Upon one-electron reduction of the Ni(II) ion, the occupied Ni 3d orbitals are raised in energy, shifting between the HOMO and the LUMO of the oxidized cofactor. These ground-state changes have a dramatic effect on the excited-state structure, causing a blue shift of the dominant π → π* transition and the appearance of numerous Ni 3d → hydrocorphin π* charge-transfer features in the vis/near-IR region.

AB - Methyl-coenzyme M reductase (MCR) catalyzes the terminal reaction in methanogenesis, the formation of methane from methyl-coenzyme M and coenzyme B. The active site of MCR binds the prosthetic group F430, a unique nickel hydrocorphin cofactor. Here, spectroscopy and computations are employed in developing detailed electronic descriptions of the Ni(II) and Ni(I) forms of the free cofactor. Absorption, magnetic circular dichroism (MCD), and variable-temperature variable-field MCD data are analyzed within the framework of time-dependent DFT computations to assign key electronic transitions. DFT calculations are further employed to evaluate possible reduced F430 models-a one-electron reduced Ni(I)F430 model and a three-electron reduced Ni(I)Fred430 model (possessing a reduced hydrocorphin ligand)-on the basis of excited-state spectra and published EPR/ENDOR parameters. While calculations on both models yield spectroscopic parameters that are consistent with most experimental data, overall better agreement is achieved using the Ni(I)F430 model, particularly with respect to electronic absorption and 1H ENDOR. The experimentally validated bonding descriptions generated herein show that in Ni(II)F430 the occupied Ni 3d orbitals are too low in energy to significantly perturb the dominant electronic transition involving the π and π* frontier MOs of the macrocycle (i.e., the HOMO → LUMO transition). Upon one-electron reduction of the Ni(II) ion, the occupied Ni 3d orbitals are raised in energy, shifting between the HOMO and the LUMO of the oxidized cofactor. These ground-state changes have a dramatic effect on the excited-state structure, causing a blue shift of the dominant π → π* transition and the appearance of numerous Ni 3d → hydrocorphin π* charge-transfer features in the vis/near-IR region.

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