Photoinduced Reductive Elimination of H2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H2 Intermediate

Dmitriy Lukoyanov, Nimesh Khadka, Dennis R. Dean, Simone Raugei, Lance C. Seefeldt, Brian M. Hoffman

Research output: Contribution to journalArticle

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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 primarily 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 calculations, 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 that 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].

Original languageEnglish
Pages (from-to)2233-2240
Number of pages8
JournalInorganic Chemistry
Volume56
Issue number4
DOIs
Publication statusPublished - Feb 20 2017

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Molybdoferredoxin
Janus
Nitrogenase
dihydrides
elimination
Photolysis
Potential energy
Discrete Fourier transforms
Hydrides
Cryogenics
Paramagnetic resonance
Experiments
Chemical activation
Irradiation
Hydrogen
Enzymes
cryogenic temperature
Temperature
hydrides
photolysis

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Inorganic Chemistry

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Photoinduced Reductive Elimination of H2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H2 Intermediate. / Lukoyanov, Dmitriy; Khadka, Nimesh; Dean, Dennis R.; Raugei, Simone; Seefeldt, Lance C.; Hoffman, Brian M.

In: Inorganic Chemistry, Vol. 56, No. 4, 20.02.2017, p. 2233-2240.

Research output: Contribution to journalArticle

Lukoyanov, Dmitriy ; Khadka, Nimesh ; Dean, Dennis R. ; Raugei, Simone ; Seefeldt, Lance C. ; Hoffman, Brian M. / Photoinduced Reductive Elimination of H2 from the Nitrogenase Dihydride (Janus) State Involves a FeMo-cofactor-H2 Intermediate. In: Inorganic Chemistry. 2017 ; Vol. 56, No. 4. pp. 2233-2240.
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AU - Seefeldt, Lance C.

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AB - 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 primarily 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 calculations, 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 that 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].

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