Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy

Hideaki Ogata; Tobias Krämer; Hongxin Wang; David Schilter; Vladimir Pelmenschikov; Maurice Van Gastel; Frank Neese; Thomas B. Rauchfuss; Leland B. Gee; Aubrey D. Scott; Yoshitaka Yoda; Yoshihito Tanaka; Wolfgang Lubitz; Stephen P. Cramer

doi:10.1038/ncomms8890

Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy

Hideaki Ogata, Tobias Krämer, Hongxin Wang, David Schilter, Vladimir Pelmenschikov, Maurice Van Gastel, Frank Neese, Thomas B. Rauchfuss, Leland B. Gee, Aubrey D. Scott, Yoshitaka Yoda, Yoshihito Tanaka, Wolfgang Lubitz, Stephen P. Cramer

Chemistry

Research output: Contribution to journal › Article › peer-review

Abstract

The metabolism of many anaerobes relies on [NiFe]-hydrogenases, whose characterization when bound to substrates has proven non-trivial. Presented here is direct evidence for a hydride bridge in the active site of the 57 Fe-labelled fully reduced Ni-R form of Desulfovibrio vulgaris Miyazaki F [NiFe]-hydrogenase. A unique ' wagging' mode involving H^- motion perpendicular to the Ni(μ1/4-H)⁵⁷ Fe plane was studied using ⁵⁷ Fe-specific nuclear resonance vibrational spectroscopy and density functional theory (DFT) calculations. On Ni(μ1/4-D) ⁵⁷ Fe deuteride substitution, this wagging causes a characteristic perturbation of Fe-CO/CN bands. Spectra have been interpreted by comparison with Ni(μ1/4-H/D) ⁵⁷ Fe enzyme mimics [(dppe)Ni(μ1/4-pdt)(μ1/4-H/D) ⁵⁷ Fe(CO)₃ ]⁺ and DFT calculations, which collectively indicate a low-spin Ni(II)(μ1/4-H)Fe(II) core for Ni-R, with H^- binding Ni more tightly than Fe. The present methodology is also relevant to characterizing Fe-H moieties in other important natural and synthetic catalysts.

Original language	English (US)
Article number	7890
Journal	Nature communications
Volume	6
DOIs	https://doi.org/10.1038/ncomms8890
State	Published - Aug 10 2015

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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title = "Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy",

abstract = "The metabolism of many anaerobes relies on [NiFe]-hydrogenases, whose characterization when bound to substrates has proven non-trivial. Presented here is direct evidence for a hydride bridge in the active site of the 57 Fe-labelled fully reduced Ni-R form of Desulfovibrio vulgaris Miyazaki F [NiFe]-hydrogenase. A unique ' wagging' mode involving H- motion perpendicular to the Ni(μ1/4-H)57 Fe plane was studied using 57 Fe-specific nuclear resonance vibrational spectroscopy and density functional theory (DFT) calculations. On Ni(μ1/4-D) 57 Fe deuteride substitution, this wagging causes a characteristic perturbation of Fe-CO/CN bands. Spectra have been interpreted by comparison with Ni(μ1/4-H/D) 57 Fe enzyme mimics [(dppe)Ni(μ1/4-pdt)(μ1/4-H/D) 57 Fe(CO)3 ]+ and DFT calculations, which collectively indicate a low-spin Ni(II)(μ1/4-H)Fe(II) core for Ni-R, with H- binding Ni more tightly than Fe. The present methodology is also relevant to characterizing Fe-H moieties in other important natural and synthetic catalysts.",

author = "Hideaki Ogata and Tobias Kr{\"a}mer and Hongxin Wang and David Schilter and Vladimir Pelmenschikov and {Van Gastel}, Maurice and Frank Neese and Rauchfuss, {Thomas B.} and Gee, {Leland B.} and Scott, {Aubrey D.} and Yoshitaka Yoda and Yoshihito Tanaka and Wolfgang Lubitz and Cramer, {Stephen P.}",

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T1 - Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy

AU - Ogata, Hideaki

AU - Krämer, Tobias

AU - Wang, Hongxin

AU - Schilter, David

AU - Pelmenschikov, Vladimir

AU - Van Gastel, Maurice

AU - Neese, Frank

AU - Rauchfuss, Thomas B.

AU - Gee, Leland B.

AU - Scott, Aubrey D.

AU - Yoda, Yoshitaka

AU - Tanaka, Yoshihito

AU - Lubitz, Wolfgang

AU - Cramer, Stephen P.

PY - 2015/8/10

Y1 - 2015/8/10

N2 - The metabolism of many anaerobes relies on [NiFe]-hydrogenases, whose characterization when bound to substrates has proven non-trivial. Presented here is direct evidence for a hydride bridge in the active site of the 57 Fe-labelled fully reduced Ni-R form of Desulfovibrio vulgaris Miyazaki F [NiFe]-hydrogenase. A unique ' wagging' mode involving H- motion perpendicular to the Ni(μ1/4-H)57 Fe plane was studied using 57 Fe-specific nuclear resonance vibrational spectroscopy and density functional theory (DFT) calculations. On Ni(μ1/4-D) 57 Fe deuteride substitution, this wagging causes a characteristic perturbation of Fe-CO/CN bands. Spectra have been interpreted by comparison with Ni(μ1/4-H/D) 57 Fe enzyme mimics [(dppe)Ni(μ1/4-pdt)(μ1/4-H/D) 57 Fe(CO)3 ]+ and DFT calculations, which collectively indicate a low-spin Ni(II)(μ1/4-H)Fe(II) core for Ni-R, with H- binding Ni more tightly than Fe. The present methodology is also relevant to characterizing Fe-H moieties in other important natural and synthetic catalysts.

AB - The metabolism of many anaerobes relies on [NiFe]-hydrogenases, whose characterization when bound to substrates has proven non-trivial. Presented here is direct evidence for a hydride bridge in the active site of the 57 Fe-labelled fully reduced Ni-R form of Desulfovibrio vulgaris Miyazaki F [NiFe]-hydrogenase. A unique ' wagging' mode involving H- motion perpendicular to the Ni(μ1/4-H)57 Fe plane was studied using 57 Fe-specific nuclear resonance vibrational spectroscopy and density functional theory (DFT) calculations. On Ni(μ1/4-D) 57 Fe deuteride substitution, this wagging causes a characteristic perturbation of Fe-CO/CN bands. Spectra have been interpreted by comparison with Ni(μ1/4-H/D) 57 Fe enzyme mimics [(dppe)Ni(μ1/4-pdt)(μ1/4-H/D) 57 Fe(CO)3 ]+ and DFT calculations, which collectively indicate a low-spin Ni(II)(μ1/4-H)Fe(II) core for Ni-R, with H- binding Ni more tightly than Fe. The present methodology is also relevant to characterizing Fe-H moieties in other important natural and synthetic catalysts.

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Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy

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