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Title: CO2 Reduction Catalyzed by Nitrogenase: Pathways to Formate, Carbon Monoxide, and Methane

Abstract

The reduction of N2 to NH3 by Mo-dependent nitrogenase at its active-site metal cluster FeMo-cofactor utilizes reductive elimination (re) 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 having amino acid substitutions in the MoFe protein near FeMo-cofactor can catalytically reduce CO2 by 2 or 8 electrons/protons to carbon monoxide (CO) and methane (CH4) at low rates. Here, it is demonstrated that nitrogenase preferentially reduces CO2 by 2 electrons/protons to formate (HCOO–) at rates >10 times higher than rates of CO2 reduction to yield CO and CH4. Quantum mechanical (QM) 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. In conclusion, MoFe proteins having amino acid substitutionsmore » near FeMo-cofactor (α-70Val→Ala, α -195His→Gln) are found to significantly alter the distribution of products between formate and CO/CH4.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [1]
+ Show Author Affiliations
  1. Utah State Univ., Logan, UT (United States)
  2. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
  3. Intel Corp., Hillsboro, OR (United States)
  4. Northwestern Univ., Evanston, IL (United States)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Utah State Univ., Logan, UT (United States). Dept. of Chemistry and Biochemistry
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1466794
Grant/Contract Number:  
SC0010687
Resource Type:
Accepted Manuscript
Journal Name:
Inorganic Chemistry
Additional Journal Information:
Journal Volume: 55; Journal Issue: 17; Journal ID: ISSN 0020-1669
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; FeS cluster; Mechanism; Calculation; Metalloenzyme

Citation Formats

Khadka, Nimesh, Dean, Dennis R., Smith, Dayle, Hoffman, Brian M., Raugei, Simone, and Seefeldt, Lance C. CO2 Reduction Catalyzed by Nitrogenase: Pathways to Formate, Carbon Monoxide, and Methane. United States: N. p., 2016. Web. doi:10.1021/acs.inorgchem.6b00388.
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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. United States. https://doi.org/10.1021/acs.inorgchem.6b00388
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Khadka, Nimesh, Dean, Dennis R., Smith, Dayle, Hoffman, Brian M., Raugei, Simone, and Seefeldt, Lance C. Mon . "CO2 Reduction Catalyzed by Nitrogenase: Pathways to Formate, Carbon Monoxide, and Methane". United States. https://doi.org/10.1021/acs.inorgchem.6b00388. https://www.osti.gov/servlets/purl/1466794.
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@article{osti_1466794,
title = {CO2 Reduction Catalyzed by Nitrogenase: Pathways to Formate, Carbon Monoxide, and Methane},
author = {Khadka, Nimesh and Dean, Dennis R. and Smith, Dayle and Hoffman, Brian M. and Raugei, Simone and Seefeldt, Lance C.},
abstractNote = {The reduction of N2 to NH3 by Mo-dependent nitrogenase at its active-site metal cluster FeMo-cofactor utilizes reductive elimination (re) 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 having amino acid substitutions in the MoFe protein near FeMo-cofactor can catalytically reduce CO2 by 2 or 8 electrons/protons to carbon monoxide (CO) and methane (CH4) at low rates. Here, it is demonstrated that nitrogenase preferentially reduces CO2 by 2 electrons/protons to formate (HCOO–) at rates >10 times higher than rates of CO2 reduction to yield CO and CH4. Quantum mechanical (QM) 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. In conclusion, MoFe proteins having 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.},
doi = {10.1021/acs.inorgchem.6b00388},
journal = {Inorganic Chemistry},
number = 17,
volume = 55,
place = {United States},
year = {Mon Aug 08 00:00:00 EDT 2016},
month = {Mon Aug 08 00:00:00 EDT 2016}
}
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