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Title: Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H 2 Intermediate

Abstract

N2 reduction by nitrogenase involves the accumulation of four reducing equivalents at the active site FeMo-cofactor to form a state with two [Fe-H-Fe] bridging hydrides (denoted E4(4H), the Janus intermediate), and we recently demonstrated that the enzyme is activated to cleave the N≡N triple bond by the reductive elimination (re) of H2 from this state. We are exploring a photochemical approach to obtaining atomic-level details of the re activation process. We have shown that when E4(4H) at cryogenic temperatures is subjected to 450 nm irradiation in an EPR cavity, it cleanly undergoes photoinduced re of H2 to give a reactive doubly-reduced intermediate, denoted E4(2H)*, which corresponds to the intermediate that would form if thermal dissociative re loss of H2 preceded N2 binding. Experiments reported here establish that photoinduced re occurs in two steps. Photolysis of E4(4H) generates an intermediate state that undergoes subsequent photoinduced conversion to [E4(2H)* + H2]. The experiments, supported by DFT calculation, indicate that the trapped intermediate is an H2 complex on the ground adiabatic potential energy suface that connects E4(4H) with [E4(2H)* + H2]. We suggest this complex, denoted E4(H2; 2H), is a thermally populated intermediate in the catalytically central re of H2 by E4(4H), andmore » that N2 reacts with this complex to complete the activated conversion of [E4(4H) + N2] into [E4(2N2H) + H2].« less

Authors:
 [1];  [2];  [3];  [4]; ORCiD logo [2]; ORCiD logo [1]
+ Show Author Affiliations
  1. Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry
  2. Utah State Univ., Logan, UT (United States). Dept. of Chemistry and Biochemistry
  3. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Biochemistry
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1356487
Report Number(s):
PNNL-SA-123286
Journal ID: ISSN 0020-1669; 49374; KC0304020
Grant/Contract Number:  
AC05-76RL01830; SC0010687; SC0010834
Resource Type:
Accepted Manuscript
Journal Name:
Inorganic Chemistry
Additional Journal Information:
Journal Volume: 56; Journal Issue: 4; 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; Environmental Molecular Sciences Laboratory

Citation Formats

Lukoyanov, Dmitriy, Khadka, Nimesh, Dean, Dennis R., Raugei, Simone, Seefeldt, Lance C., and Hoffman, Brian M. Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H 2 Intermediate. United States: N. p., 2017. Web. doi:10.1021/acs.inorgchem.6b02899.
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Lukoyanov, Dmitriy, Khadka, Nimesh, Dean, Dennis R., Raugei, Simone, Seefeldt, Lance C., & Hoffman, Brian M. Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H 2 Intermediate. United States. https://doi.org/10.1021/acs.inorgchem.6b02899
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Lukoyanov, Dmitriy, Khadka, Nimesh, Dean, Dennis R., Raugei, Simone, Seefeldt, Lance C., and Hoffman, Brian M. Wed . "Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H 2 Intermediate". United States. https://doi.org/10.1021/acs.inorgchem.6b02899. https://www.osti.gov/servlets/purl/1356487.
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@article{osti_1356487,
title = {Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H 2 Intermediate},
author = {Lukoyanov, Dmitriy and Khadka, Nimesh and Dean, Dennis R. and Raugei, Simone and Seefeldt, Lance C. and Hoffman, Brian M.},
abstractNote = {N2 reduction by nitrogenase involves the accumulation of four reducing equivalents at the active site FeMo-cofactor to form a state with two [Fe-H-Fe] bridging hydrides (denoted E4(4H), the Janus intermediate), and we recently demonstrated that the enzyme is activated to cleave the N≡N triple bond by the reductive elimination (re) of H2 from this state. We are exploring a photochemical approach to obtaining atomic-level details of the re activation process. We have shown that when E4(4H) at cryogenic temperatures is subjected to 450 nm irradiation in an EPR cavity, it cleanly undergoes photoinduced re of H2 to give a reactive doubly-reduced intermediate, denoted E4(2H)*, which corresponds to the intermediate that would form if thermal dissociative re loss of H2 preceded N2 binding. Experiments reported here establish that photoinduced re occurs in two steps. Photolysis of E4(4H) generates an intermediate state that undergoes subsequent photoinduced conversion to [E4(2H)* + H2]. The experiments, supported by DFT calculation, indicate that the trapped intermediate is an H2 complex on the ground adiabatic potential energy suface that connects E4(4H) with [E4(2H)* + H2]. We suggest this complex, denoted E4(H2; 2H), is a thermally populated intermediate in the catalytically central re of H2 by E4(4H), and that N2 reacts with this complex to complete the activated conversion of [E4(4H) + N2] into [E4(2N2H) + H2].},
doi = {10.1021/acs.inorgchem.6b02899},
journal = {Inorganic Chemistry},
number = 4,
volume = 56,
place = {United States},
year = {Wed Feb 08 00:00:00 EST 2017},
month = {Wed Feb 08 00:00:00 EST 2017}
}
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https://doi.org/10.1021/acs.inorgchem.6b02899
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    Works referencing / citing this record:

    Critical computational analysis illuminates the reductive-elimination mechanism that activates nitrogenase for N 2 reduction
    journal, October 2018

    • Raugei, Simone; Seefeldt, Lance C.; Hoffman, Brian M.
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 45
    • DOI: 10.1073/pnas.1810211115

    A Systematic DFT Approach for Studying Mechanisms of Redox Active Enzymes
    journal, December 2018

    The mechanism for nitrogenase including all steps
    journal, January 2019

    • Siegbahn, Per E. M.
    • Physical Chemistry Chemical Physics, Vol. 21, Issue 28
    • DOI: 10.1039/c9cp02073j

    Is there computational support for an unprotonated carbon in the E 4 state of nitrogenase?
    journal, December 2017

    • Siegbahn, Per E. M.
    • Journal of Computational Chemistry, Vol. 39, Issue 12
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    A model for dinitrogen binding in the E 4 state of nitrogenase
    journal, January 2019

    • Thorhallsson, Albert Th.; Benediktsson, Bardi; Bjornsson, Ragnar
    • Chemical Science, Vol. 10, Issue 48
    • DOI: 10.1039/c9sc03610e

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    journal, January 2019

    • Cao, Lili; Ryde, Ulf
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