Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase

Mishtu Dey, Ryan C. Kunz, Katherine M. Van Heuvelen, Jennifer L. Craft, Yih-Chern Horng, Qun Tang, David F. Bocian, Simon J. George, Thomas C. Brunold, Stephen W. Ragsdale

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Abstract

Methyl-coenzyme M reductase (MCR) catalyzes the final step in methane biosynthesis by methanogenic archaea and contains a redox-active nickel tetrahydrocorphin, coenzyme F 430 , at its active site. Spectroscopic and computational methods have been used to study a novel form of the coenzyme, called F 330 , which is obtained by reducing F 430 with sodium borohydride (NaBH 4 ). F 330 exhibits a prominent absorption peak at 330 nm, which is blue shifted by 100 nm relative to F 430 . Mass spectrometric studies demonstrate that the tetrapyrrole ring in F 330 has undergone reduction, on the basis of the incorporation of protium (or deuterium), upon treatment of F 430 with NaBH 4 (or NaBD 4 ). One- and two-dimensional NMR studies show that the site of reduction is the exocyclic ketone group of the tetrahydrocorphin. Resonance Raman studies indicate that elimination of this π-bond increases the overall π-bond order in the conjugative framework. X-ray absorption, magnetic circular dichroism, and computational results show that F 330 contains low-spin Ni(II). Thus, conversion of F 430 to F 330 reduces the hydrocorphin ring but not the metal. Conversely, reduction of F 430 with Ti(III) citrate to generate F 380 (corresponding to the active MCR red1 state) reduces the Ni(II) to Ni(I) but does not reduce the tetrapyrrole ring system, which is consistent with other studies [Piskorski, R., and Jaun, B. (2003) J. Am. Chem. Soc. 125, 13120-13125; Craft, J. L., et al. (2004) J. Biol. Inorg. Chem. 9, 77-89]. The distinct origins of the absorption band shifts associated with the formation of F 330 and F 380 are discussed within the framework of our computational results. These studies on the nature of the product(s) of reduction of F 430 are of interest in the context of the mechanism of methane formation by MCR and in relation to the chemistry of hydroporphinoid systems in general. The spectroscopic and time-dependent DFT calculations add important insight into the electronic structure of the nickel hydrocorphinate in its Ni(II) and Ni(I) valence states.

Original languageEnglish
Pages (from-to)11915-11933
Number of pages19
JournalBiochemistry
Volume45
Issue number39
DOIs
Publication statusPublished - 2006 Oct 3

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Tetrapyrroles
Coenzymes
Metals
Methane
Nickel
Deuterium
Biosynthesis
Archaea
X ray absorption
Circular Dichroism
Computational methods
factor F430
methyl coenzyme M reductase
Ketones
Discrete Fourier transforms
Citric Acid
Oxidation-Reduction
Electronic structure
Absorption spectra
Catalytic Domain

All Science Journal Classification (ASJC) codes

  • Biochemistry

Cite this

Dey, Mishtu ; Kunz, Ryan C. ; Van Heuvelen, Katherine M. ; Craft, Jennifer L. ; Horng, Yih-Chern ; Tang, Qun ; Bocian, David F. ; George, Simon J. ; Brunold, Thomas C. ; Ragsdale, Stephen W. / Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase In: Biochemistry. 2006 ; Vol. 45, No. 39. pp. 11915-11933.
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title = "Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase",
abstract = "Methyl-coenzyme M reductase (MCR) catalyzes the final step in methane biosynthesis by methanogenic archaea and contains a redox-active nickel tetrahydrocorphin, coenzyme F 430 , at its active site. Spectroscopic and computational methods have been used to study a novel form of the coenzyme, called F 330 , which is obtained by reducing F 430 with sodium borohydride (NaBH 4 ). F 330 exhibits a prominent absorption peak at 330 nm, which is blue shifted by 100 nm relative to F 430 . Mass spectrometric studies demonstrate that the tetrapyrrole ring in F 330 has undergone reduction, on the basis of the incorporation of protium (or deuterium), upon treatment of F 430 with NaBH 4 (or NaBD 4 ). One- and two-dimensional NMR studies show that the site of reduction is the exocyclic ketone group of the tetrahydrocorphin. Resonance Raman studies indicate that elimination of this π-bond increases the overall π-bond order in the conjugative framework. X-ray absorption, magnetic circular dichroism, and computational results show that F 330 contains low-spin Ni(II). Thus, conversion of F 430 to F 330 reduces the hydrocorphin ring but not the metal. Conversely, reduction of F 430 with Ti(III) citrate to generate F 380 (corresponding to the active MCR red1 state) reduces the Ni(II) to Ni(I) but does not reduce the tetrapyrrole ring system, which is consistent with other studies [Piskorski, R., and Jaun, B. (2003) J. Am. Chem. Soc. 125, 13120-13125; Craft, J. L., et al. (2004) J. Biol. Inorg. Chem. 9, 77-89]. The distinct origins of the absorption band shifts associated with the formation of F 330 and F 380 are discussed within the framework of our computational results. These studies on the nature of the product(s) of reduction of F 430 are of interest in the context of the mechanism of methane formation by MCR and in relation to the chemistry of hydroporphinoid systems in general. The spectroscopic and time-dependent DFT calculations add important insight into the electronic structure of the nickel hydrocorphinate in its Ni(II) and Ni(I) valence states.",
author = "Mishtu Dey and Kunz, {Ryan C.} and {Van Heuvelen}, {Katherine M.} and Craft, {Jennifer L.} and Yih-Chern Horng and Qun Tang and Bocian, {David F.} and George, {Simon J.} and Brunold, {Thomas C.} and Ragsdale, {Stephen W.}",
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Dey, M, Kunz, RC, Van Heuvelen, KM, Craft, JL, Horng, Y-C, Tang, Q, Bocian, DF, George, SJ, Brunold, TC & Ragsdale, SW 2006, ' Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase ', Biochemistry, vol. 45, no. 39, pp. 11915-11933. https://doi.org/10.1021/bi0613269

Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase . / Dey, Mishtu; Kunz, Ryan C.; Van Heuvelen, Katherine M.; Craft, Jennifer L.; Horng, Yih-Chern; Tang, Qun; Bocian, David F.; George, Simon J.; Brunold, Thomas C.; Ragsdale, Stephen W.

In: Biochemistry, Vol. 45, No. 39, 03.10.2006, p. 11915-11933.

Research output: Contribution to journalArticle

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T1 - Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase

AU - Dey, Mishtu

AU - Kunz, Ryan C.

AU - Van Heuvelen, Katherine M.

AU - Craft, Jennifer L.

AU - Horng, Yih-Chern

AU - Tang, Qun

AU - Bocian, David F.

AU - George, Simon J.

AU - Brunold, Thomas C.

AU - Ragsdale, Stephen W.

PY - 2006/10/3

Y1 - 2006/10/3

N2 - Methyl-coenzyme M reductase (MCR) catalyzes the final step in methane biosynthesis by methanogenic archaea and contains a redox-active nickel tetrahydrocorphin, coenzyme F 430 , at its active site. Spectroscopic and computational methods have been used to study a novel form of the coenzyme, called F 330 , which is obtained by reducing F 430 with sodium borohydride (NaBH 4 ). F 330 exhibits a prominent absorption peak at 330 nm, which is blue shifted by 100 nm relative to F 430 . Mass spectrometric studies demonstrate that the tetrapyrrole ring in F 330 has undergone reduction, on the basis of the incorporation of protium (or deuterium), upon treatment of F 430 with NaBH 4 (or NaBD 4 ). One- and two-dimensional NMR studies show that the site of reduction is the exocyclic ketone group of the tetrahydrocorphin. Resonance Raman studies indicate that elimination of this π-bond increases the overall π-bond order in the conjugative framework. X-ray absorption, magnetic circular dichroism, and computational results show that F 330 contains low-spin Ni(II). Thus, conversion of F 430 to F 330 reduces the hydrocorphin ring but not the metal. Conversely, reduction of F 430 with Ti(III) citrate to generate F 380 (corresponding to the active MCR red1 state) reduces the Ni(II) to Ni(I) but does not reduce the tetrapyrrole ring system, which is consistent with other studies [Piskorski, R., and Jaun, B. (2003) J. Am. Chem. Soc. 125, 13120-13125; Craft, J. L., et al. (2004) J. Biol. Inorg. Chem. 9, 77-89]. The distinct origins of the absorption band shifts associated with the formation of F 330 and F 380 are discussed within the framework of our computational results. These studies on the nature of the product(s) of reduction of F 430 are of interest in the context of the mechanism of methane formation by MCR and in relation to the chemistry of hydroporphinoid systems in general. The spectroscopic and time-dependent DFT calculations add important insight into the electronic structure of the nickel hydrocorphinate in its Ni(II) and Ni(I) valence states.

AB - Methyl-coenzyme M reductase (MCR) catalyzes the final step in methane biosynthesis by methanogenic archaea and contains a redox-active nickel tetrahydrocorphin, coenzyme F 430 , at its active site. Spectroscopic and computational methods have been used to study a novel form of the coenzyme, called F 330 , which is obtained by reducing F 430 with sodium borohydride (NaBH 4 ). F 330 exhibits a prominent absorption peak at 330 nm, which is blue shifted by 100 nm relative to F 430 . Mass spectrometric studies demonstrate that the tetrapyrrole ring in F 330 has undergone reduction, on the basis of the incorporation of protium (or deuterium), upon treatment of F 430 with NaBH 4 (or NaBD 4 ). One- and two-dimensional NMR studies show that the site of reduction is the exocyclic ketone group of the tetrahydrocorphin. Resonance Raman studies indicate that elimination of this π-bond increases the overall π-bond order in the conjugative framework. X-ray absorption, magnetic circular dichroism, and computational results show that F 330 contains low-spin Ni(II). Thus, conversion of F 430 to F 330 reduces the hydrocorphin ring but not the metal. Conversely, reduction of F 430 with Ti(III) citrate to generate F 380 (corresponding to the active MCR red1 state) reduces the Ni(II) to Ni(I) but does not reduce the tetrapyrrole ring system, which is consistent with other studies [Piskorski, R., and Jaun, B. (2003) J. Am. Chem. Soc. 125, 13120-13125; Craft, J. L., et al. (2004) J. Biol. Inorg. Chem. 9, 77-89]. The distinct origins of the absorption band shifts associated with the formation of F 330 and F 380 are discussed within the framework of our computational results. These studies on the nature of the product(s) of reduction of F 430 are of interest in the context of the mechanism of methane formation by MCR and in relation to the chemistry of hydroporphinoid systems in general. The spectroscopic and time-dependent DFT calculations add important insight into the electronic structure of the nickel hydrocorphinate in its Ni(II) and Ni(I) valence states.

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