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

All Science Journal Classification (ASJC) codes

  • Biochemistry

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    Dey, M., Kunz, R. C., Van Heuvelen, K. M., Craft, J. L., Horng, Y-C., Tang, Q., Bocian, D. F., George, S. J., Brunold, T. C., & Ragsdale, S. W. (2006). Spectroscopic and computational studies of reduction of the metal versus the tetrapyrrole ring of coenzyme F 430 from methyl-coenzyme M reductase Biochemistry, 45(39), 11915-11933. https://doi.org/10.1021/bi0613269