How thermal fluctuations influence the function of the FeMo cofactor in nitrogenase enzymes

Li，Wan Lu1,3; Li，Yong4,5,7; Li，Jun4,6; Head-Gordon，Teresa1,2,3

2023-07-20

10.1016/j.checat.2023.100662

Chem Catalysis   Impact Factor & Quartile

2667-1107

2667-1093

The catalytic mechanism of N fixation by nitrogenase remains unresolved in how the strong N≡N bond is activated and why the reductive elimination of H is required. Here, we use density functional theory and physiologically relevant thermal simulations to elucidate the mechanism of the complete nitrogenase catalytic cycle. Over the accumulation of four reducing equivalents, we find that protons and electrons transfer to the FeMo cofactor to weaken and break its bridge Fe–S bond, leading to temporary HS formation that exposes the Fe sites to weakly bind N. Remarkably, we find that subsequent H formation is responsible for chemical activation to an N=N double bond accompanied by a low barrier for H release. We emphasize that finite temperature effects smooth out mechanistic differences between DFT functionals observed at 0 K, thus leading to a consistent understanding as to why H formation is an obligatory step in N adsorption and activation.

catalytic mechanism DFT molecular dynamics nitrogenase SDG6: Clean water and sanitation SDG7: Affordable and clean energy thermal fluctuations

ESCI

English

Corresponding

Guangdong Provincial Key Laboratory Of Catalysis[2020B121201002];National Natural Science Foundation of China[22033005];National Energy Research Scientific Computing Center[DE-AC02-05CH11231];

Chemistry

Chemistry, Physical

WOS:001047556700001

CELL PRESS

2-s2.0-85166017285

Scopus

1.Kenneth S. Pitzer Theory Center and Department of Chemistry,University of California,Berkeley,Berkeley,94720,United States
2.Departments of Bioengineering and Chemical and Biomolecular Engineering,University of California,Berkeley,Berkeley,94720,United States
3.Chemical Sciences Division,Lawrence Berkeley National Laboratory,Berkeley,94720,United States
4.Department of Chemistry and Engineering Research Center of Advanced Rare-Earth Materials of Ministry of Education,Tsinghua University,Beijing,100084,China
5.Institute of Applied and Physical Chemistry and Center for Environmental Research and Sustainable Technology,University of Bremen,Bremen,28359,Germany
6.Department of Chemistry and Guangdong Provincial Key Laboratory of Catalytic Chemistry,Southern University of Science and Technology,Shenzhen,518055,China
7.Department of Chemistry-Ångström Laboratory,Uppsala University,Uppsala,75121,Sweden

Li，Wan Lu,Li，Yong,Li，Jun,et al. How thermal fluctuations influence the function of the FeMo cofactor in nitrogenase enzymes[J]. Chem Catalysis,2023,3(7).

Li，Wan Lu,Li，Yong,Li，Jun,&Head-Gordon，Teresa.(2023).How thermal fluctuations influence the function of the FeMo cofactor in nitrogenase enzymes.Chem Catalysis,3(7).

Li，Wan Lu,et al."How thermal fluctuations influence the function of the FeMo cofactor in nitrogenase enzymes".Chem Catalysis 3.7(2023).