CO2 Reduction Catalyzed by Nitrogenase

Pathways to Formate, Carbon Monoxide, and Methane

Nimesh Khadka, Dennis R. Dean, Dayle Smith, Brian M. Hoffman, Simone Raugei, Lance C. Seefeldt

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

The reduction of N2 to NH3 by Mo-dependent nitrogenase at its active-site metal cluster FeMo-cofactor utilizes reductive elimination of Fe-bound hydrides with obligatory loss of H2 to activate the enzyme for binding/reduction of N2. Earlier work showed that wild-type nitrogenase and a nitrogenase with amino acid substitutions in the MoFe protein near FeMo-cofactor can catalytically reduce CO2 by two or eight electrons/protons to carbon monoxide (CO) and methane (CH4) at low rates. Here, it is demonstrated that nitrogenase preferentially reduces CO2 by two electrons/protons to formate (HCOO-) at rates >10 times higher than rates of CO2 reduction to CO and CH4. Quantum mechanical calculations on the doubly reduced FeMo-cofactor with a Fe-bound hydride and S-bound proton (E2(2H) state) favor a direct reaction of CO2 with the hydride ("direct hydride transfer" reaction pathway), with facile hydride transfer to CO2 yielding formate. In contrast, a significant barrier is observed for reaction of Fe-bound CO2 with the hydride ("associative" reaction pathway), which leads to CO and CH4. Remarkably, in the direct hydride transfer pathway, the Fe-H behaves as a hydridic hydrogen, whereas in the associative pathway it acts as a protic hydrogen. MoFe proteins with amino acid substitutions near FeMo-cofactor (α-70Val→Ala, α-195His→Gln) are found to significantly alter the distribution of products between formate and CO/CH4.

Original languageEnglish
Pages (from-to)8321-8330
Number of pages10
JournalInorganic Chemistry
Volume55
Issue number17
DOIs
Publication statusPublished - Sep 6 2016

Fingerprint

formic acid
Molybdoferredoxin
Nitrogenase
Methane
formates
Carbon Monoxide
Hydrides
carbon monoxide
hydrides
methane
Protons
amino acids
protons
Hydrogen
Substitution reactions
substitutes
proteins
Amino Acids
Electrons
metal clusters

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Inorganic Chemistry

Cite this

CO2 Reduction Catalyzed by Nitrogenase : Pathways to Formate, Carbon Monoxide, and Methane. / Khadka, Nimesh; Dean, Dennis R.; Smith, Dayle; Hoffman, Brian M.; Raugei, Simone; Seefeldt, Lance C.

In: Inorganic Chemistry, Vol. 55, No. 17, 06.09.2016, p. 8321-8330.

Research output: Contribution to journalArticle

Khadka, Nimesh ; Dean, Dennis R. ; Smith, Dayle ; Hoffman, Brian M. ; Raugei, Simone ; Seefeldt, Lance C. / CO2 Reduction Catalyzed by Nitrogenase : Pathways to Formate, Carbon Monoxide, and Methane. In: Inorganic Chemistry. 2016 ; Vol. 55, No. 17. pp. 8321-8330.
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AB - The reduction of N2 to NH3 by Mo-dependent nitrogenase at its active-site metal cluster FeMo-cofactor utilizes reductive elimination of Fe-bound hydrides with obligatory loss of H2 to activate the enzyme for binding/reduction of N2. Earlier work showed that wild-type nitrogenase and a nitrogenase with amino acid substitutions in the MoFe protein near FeMo-cofactor can catalytically reduce CO2 by two or eight electrons/protons to carbon monoxide (CO) and methane (CH4) at low rates. Here, it is demonstrated that nitrogenase preferentially reduces CO2 by two electrons/protons to formate (HCOO-) at rates >10 times higher than rates of CO2 reduction to CO and CH4. Quantum mechanical calculations on the doubly reduced FeMo-cofactor with a Fe-bound hydride and S-bound proton (E2(2H) state) favor a direct reaction of CO2 with the hydride ("direct hydride transfer" reaction pathway), with facile hydride transfer to CO2 yielding formate. In contrast, a significant barrier is observed for reaction of Fe-bound CO2 with the hydride ("associative" reaction pathway), which leads to CO and CH4. Remarkably, in the direct hydride transfer pathway, the Fe-H behaves as a hydridic hydrogen, whereas in the associative pathway it acts as a protic hydrogen. MoFe proteins with amino acid substitutions near FeMo-cofactor (α-70Val→Ala, α-195His→Gln) are found to significantly alter the distribution of products between formate and CO/CH4.

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