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Reaction Mechanism of [NiFe] Hydrogenase Studied by Computational Methods

Dong, Geng LU ; Phung, Quan Manh ; Pierloot, Kristine and Ryde, Ulf LU (2018) In Inorganic Chemistry 57(24). p.15289-15298
Abstract

[NiFe] hydrogenases catalyze the reversible conversion of molecular hydrogen to protons and electrons. This seemingly simple reaction has attracted much attention because of the prospective use of H2 as a clean fuel. In this paper, we have studied the full reaction mechanism of this enzyme with various computational methods. Geometries were obtained with combined quantum mechanical and molecular mechanics (QM/MM) calculations. To get more accurate energies and obtain a detailed account of the surroundings, we performed big-QM calculations with 819 atoms in the QM region. Moreover, QM/MM thermodynamic cycle perturbation calculations were performed to obtain free energies. Finally, density matrix renormalisation group complete... (More)

[NiFe] hydrogenases catalyze the reversible conversion of molecular hydrogen to protons and electrons. This seemingly simple reaction has attracted much attention because of the prospective use of H2 as a clean fuel. In this paper, we have studied the full reaction mechanism of this enzyme with various computational methods. Geometries were obtained with combined quantum mechanical and molecular mechanics (QM/MM) calculations. To get more accurate energies and obtain a detailed account of the surroundings, we performed big-QM calculations with 819 atoms in the QM region. Moreover, QM/MM thermodynamic cycle perturbation calculations were performed to obtain free energies. Finally, density matrix renormalisation group complete active space self-consistent field calculations were carried out to study the electronic structures of the various states in the reaction mechanism. Our calculations indicate that the Ni-L state is not involved in the reaction mechanism. Instead, the Ni-C state is reduced by one electron and then the bridging hydride ion is transferred to the sulfur atom of Cys546 as a proton and the two electrons transfer to the Ni ion. This step turned out to be rate-determining with an energy barrier of 58 kJ/mol, which is consistent with the experimental rate of 750 ± 90 s-1 (corresponding to ∼52 kJ/mol). The cleavage of the H-H bond is facile with an energy barrier of 33 kJ/mol, according to our calculations. We also find that the reaction energies are sensitive to the size of the QM system, the basis set, and the density functional theory method, in agreement with previous studies.

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Contribution to journal
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published
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Inorganic Chemistry
volume
57
issue
24
pages
10 pages
publisher
The American Chemical Society (ACS)
external identifiers
  • scopus:85058546143
  • pmid:30500163
ISSN
0020-1669
DOI
10.1021/acs.inorgchem.8b02590
language
English
LU publication?
yes
id
0006868c-9674-4726-b283-12898ea612ef
date added to LUP
2019-01-03 12:02:16
date last changed
2021-01-19 02:00:00
@article{0006868c-9674-4726-b283-12898ea612ef,
  abstract     = {<p>[NiFe] hydrogenases catalyze the reversible conversion of molecular hydrogen to protons and electrons. This seemingly simple reaction has attracted much attention because of the prospective use of H<sub>2</sub> as a clean fuel. In this paper, we have studied the full reaction mechanism of this enzyme with various computational methods. Geometries were obtained with combined quantum mechanical and molecular mechanics (QM/MM) calculations. To get more accurate energies and obtain a detailed account of the surroundings, we performed big-QM calculations with 819 atoms in the QM region. Moreover, QM/MM thermodynamic cycle perturbation calculations were performed to obtain free energies. Finally, density matrix renormalisation group complete active space self-consistent field calculations were carried out to study the electronic structures of the various states in the reaction mechanism. Our calculations indicate that the Ni-L state is not involved in the reaction mechanism. Instead, the Ni-C state is reduced by one electron and then the bridging hydride ion is transferred to the sulfur atom of Cys546 as a proton and the two electrons transfer to the Ni ion. This step turned out to be rate-determining with an energy barrier of 58 kJ/mol, which is consistent with the experimental rate of 750 ± 90 s<sup>-1</sup> (corresponding to ∼52 kJ/mol). The cleavage of the H-H bond is facile with an energy barrier of 33 kJ/mol, according to our calculations. We also find that the reaction energies are sensitive to the size of the QM system, the basis set, and the density functional theory method, in agreement with previous studies.</p>},
  author       = {Dong, Geng and Phung, Quan Manh and Pierloot, Kristine and Ryde, Ulf},
  issn         = {0020-1669},
  language     = {eng},
  number       = {24},
  pages        = {15289--15298},
  publisher    = {The American Chemical Society (ACS)},
  series       = {Inorganic Chemistry},
  title        = {Reaction Mechanism of [NiFe] Hydrogenase Studied by Computational Methods},
  url          = {https://lup.lub.lu.se/search/ws/files/57285257/246_h2ase_full_reaction.pdf},
  doi          = {10.1021/acs.inorgchem.8b02590},
  volume       = {57},
  year         = {2018},
}