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

Journal Article · · Inorganic Chemistry
 [1];  [2];  [3];  [4]; ORCiD logo [2]; ORCiD logo [1]
  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)
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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].

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
Grant/Contract Number:
AC05-76RL01830; SC0010687; SC0010834
OSTI ID:
1356487
Report Number(s):
PNNL-SA-123286; 49374; KC0304020
Journal Information:
Inorganic Chemistry, Vol. 56, Issue 4; ISSN 0020-1669
Publisher:
American Chemical Society (ACS)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 36 works
Citation information provided by
Web of Science

References (32)

Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage journal January 2014
Nitrogenase: A Draft Mechanism journal December 2012
Identification of a Key Catalytic Intermediate Demonstrates That Nitrogenase Is Activated by the Reversible Exchange of N 2 for H 2 journal March 2015
Reductive Elimination of H 2 Activates Nitrogenase to Reduce the N≡N Triple Bond: Characterization of the E 4 (4H) Janus Intermediate in Wild-Type Enzyme journal August 2016
Trapping H - Bound to the Nitrogenase FeMo-Cofactor Active Site during H 2 Evolution:  Characterization by ENDOR Spectroscopy journal May 2005
Is Mo Involved in Hydride Binding by the Four-Electron Reduced (E 4 ) Intermediate of the Nitrogenase MoFe Protein? journal March 2010
Connecting nitrogenase intermediates with the kinetic scheme for N2 reduction by a relaxation protocol and identification of the N2 binding state journal January 2007
Mechanism of Molybdenum Nitrogenase journal January 1996
Reversible Photoinduced Reductive Elimination of H 2 from the Nitrogenase Dihydride State, the E 4 (4H) Janus Intermediate journal January 2016
Photochemistry of Transition Metal Hydrides journal June 2016
Metal dihydride complexes: Photochemical mechanisms for reductive elimination journal November 1998
Ultrafast reductive elimination of hydrogen from a metal carbonyl dihydride complex; a study by time-resolved IR and visible spectroscopy journal January 1997
Transient and matrix photochemistry of Fe(dmpe)2H2 (dmpe = Me2PCH2CH2Me2): dynamics of C-H and H-H activation journal September 1993
The hydride route to the preparation of dinitrogen complexes journal January 2010
The photoreversible oxidative-addition, reductive-elimination reactions iron + molecular hydrogen .dblharw. iron hydride (FeH2) in low-temperature matrixes journal February 1984
New routes to low-coordinate iron hydride complexes: The binuclear oxidative addition of H2 journal August 2009
Binding Affinity of Alkynes and Alkenes to Low-Coordinate Iron journal April 2006
Studies of Low-Coordinate Iron Dinitrogen Complexes journal January 2006
The Reactivity Patterns of Low-Coordinate Iron−Hydride Complexes journal May 2008
Catalytic and Biophysical Properties of a Nitrogenase Apo-MoFe Protein Produced by a n ifB -Deletion Mutant of Azotobacter v inelandii † journal September 1998
Avoided crossings in photochemistry journal January 1975
One and two-photon photochemistry in rigid solutions of durene in 3-methylpentane at 77°K journal April 1971
A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase journal June 1984
Fundamentals of H 2 Binding and Reactivity on Transition Metals Underlying Hydrogenase Function and H 2 Production and Storage journal October 2007
Activation of dihydrogen and coordination of molecular H2 on transition metals journal February 2014
Dihydrogen Complexation journal March 2016
Dihydrogen binding in hydrogenase and nitrogenase journal September 1986
Photolysis of hexacarbonylchromium in hydrogen-containing matrixes: evidence of simple adducts of molecular hydrogen journal April 1985
Photolysis of (cyclopentadienyl)- and (pentamethylcyclopentadienyl)tricarbonylhydridometal complexes of tungsten and molybdenum in dihydrogen-containing matrixes: evidence for adducts of molecular hydrogen journal October 1986
Hydrogen generation: catalytic acceleration and control by light journal January 2009
Kinetics and Thermodynamics of Small Molecule Binding to Pincer-PCP Rhodium(I) Complexes journal March 2013
Stretched exponential relaxation in molecular and electronic glasses journal September 1996

Cited By (7)

Critical computational analysis illuminates the reductive-elimination mechanism that activates nitrogenase for N 2 reduction journal October 2018
Survey of the Geometric and Electronic Structures of the Key Hydrogenated Forms of FeMo-co, the Active Site of the Enzyme Nitrogenase: Principles of the Mechanistically Significant Coordination Chemistry journal January 2019
A Systematic DFT Approach for Studying Mechanisms of Redox Active Enzymes journal December 2018
The mechanism for nitrogenase including all steps journal January 2019
Is there computational support for an unprotonated carbon in the E 4 state of nitrogenase? journal December 2017
A model for dinitrogen binding in the E 4 state of nitrogenase journal January 2019
Extremely large differences in DFT energies for nitrogenase models journal January 2019

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