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 language | English |
|---|---|
| Pages (from-to) | 11915-11933 |
| Number of pages | 19 |
| Journal | Biochemistry |
| Volume | 45 |
| Issue number | 39 |
| DOIs | |
| Publication status | Published - 2006 Oct 3 |
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All Science Journal Classification (ASJC) codes
- Biochemistry
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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 journal › Article
TY - JOUR
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.
UR - http://www.scopus.com/inward/record.url?scp=33749323024&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=33749323024&partnerID=8YFLogxK
U2 - 10.1021/bi0613269
DO - 10.1021/bi0613269
M3 - Article
C2 - 17002292
AN - SCOPUS:33749323024
VL - 45
SP - 11915
EP - 11933
JO - Biochemistry
JF - Biochemistry
SN - 0006-2960
IS - 39
ER -