EPR/ENDOR, Mössbauer, and quantum-chemical investigations of diiron complexes mimicking the active oxidized state of [FeFe]hydrogenase

Alexey Silakov, Matthew T. Olsen, Stephen Sproules, Eduard J. Reijerse, Thomas B. Rauchfuss, Wolfgang Lubitz

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Understanding the catalytic process of the heterolytic splitting and formation of molecular hydrogen is one of the key topics for the development of a future hydrogen economy. With an interest in elucidating the enzymatic mechanism of the [Fe 2 (S 2 C 2 H 4 NH)(CN) 2 (CO) 2 (μ-CO)] active center uniquely found in [FeFe]hydrogenases, we present a detailed spectroscopic and theoretical analysis of its inorganic model [Fe 2 (S 2 X)(CO) 3 (dppv) (PMe 3 )] + [dppv = cis-1,2-bis(diphenylphosphino)ethylene] in two forms with S 2 X = ethanedithiolate (1edt) and azadithiolate (1adt). These complexes represent models for the oxidized mixed-valent Fe I Fe II state analogous to the active oxidized "H ox " state of the native H-cluster. For both complexes, the 31 P hyperfine interactions were determined by pulse electron paramagnetic resonance and electron nuclear double resonance (ENDOR) methods. For 1edt, the 57 Fe parameters were measured by electron spin-echo envelope modulation and Mössbauer spectroscopy, while for 1adt, 14 N and selected 1 H couplings could be obtained by ENDOR and hyperfine sublevel correlation spectroscopy. The spin density was found to be predominantly localized on the Fe(dppv) site. This spin distribution is different from that of the H-cluster, where both the spin and charge densities are delocalized over the two Fe centers. This difference is attributed to the influence of the "native" cubane subcluster that is lacking in the inorganic models. The degree and character of the unpaired spin delocalization was found to vary from 1edt, with an abiological dithiolate, to 1adt, which features the authentic cofactor. For 1adt, we find two 14 N signals, which are indicative for two possible isomers of the azadithiolate, demonstrating its high flexibility. All interaction parameters were also evaluated through density functional theory calculations at various levels.

Original languageEnglish (US)
Pages (from-to)8617-8628
Number of pages12
JournalInorganic Chemistry
Volume51
Issue number15
DOIs
StatePublished - Aug 6 2012

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Hydrogenase
Paramagnetic resonance
Carbon Monoxide
Electrons
Hydrogen
Spectroscopy
electrons
Charge density
cubane
Isomers
Density functional theory
spectroscopic analysis
economy
hydrogen
Modulation
electron spin
spectroscopy
echoes
electron paramagnetic resonance
flexibility

All Science Journal Classification (ASJC) codes

  • Physical and Theoretical Chemistry
  • Inorganic Chemistry

Cite this

Silakov, Alexey ; Olsen, Matthew T. ; Sproules, Stephen ; Reijerse, Eduard J. ; Rauchfuss, Thomas B. ; Lubitz, Wolfgang. / EPR/ENDOR, Mössbauer, and quantum-chemical investigations of diiron complexes mimicking the active oxidized state of [FeFe]hydrogenase. In: Inorganic Chemistry. 2012 ; Vol. 51, No. 15. pp. 8617-8628.
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abstract = "Understanding the catalytic process of the heterolytic splitting and formation of molecular hydrogen is one of the key topics for the development of a future hydrogen economy. With an interest in elucidating the enzymatic mechanism of the [Fe 2 (S 2 C 2 H 4 NH)(CN) 2 (CO) 2 (μ-CO)] active center uniquely found in [FeFe]hydrogenases, we present a detailed spectroscopic and theoretical analysis of its inorganic model [Fe 2 (S 2 X)(CO) 3 (dppv) (PMe 3 )] + [dppv = cis-1,2-bis(diphenylphosphino)ethylene] in two forms with S 2 X = ethanedithiolate (1edt) and azadithiolate (1adt). These complexes represent models for the oxidized mixed-valent Fe I Fe II state analogous to the active oxidized {"}H ox {"} state of the native H-cluster. For both complexes, the 31 P hyperfine interactions were determined by pulse electron paramagnetic resonance and electron nuclear double resonance (ENDOR) methods. For 1edt, the 57 Fe parameters were measured by electron spin-echo envelope modulation and M{\"o}ssbauer spectroscopy, while for 1adt, 14 N and selected 1 H couplings could be obtained by ENDOR and hyperfine sublevel correlation spectroscopy. The spin density was found to be predominantly localized on the Fe(dppv) site. This spin distribution is different from that of the H-cluster, where both the spin and charge densities are delocalized over the two Fe centers. This difference is attributed to the influence of the {"}native{"} cubane subcluster that is lacking in the inorganic models. The degree and character of the unpaired spin delocalization was found to vary from 1edt, with an abiological dithiolate, to 1adt, which features the authentic cofactor. For 1adt, we find two 14 N signals, which are indicative for two possible isomers of the azadithiolate, demonstrating its high flexibility. All interaction parameters were also evaluated through density functional theory calculations at various levels.",
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EPR/ENDOR, Mössbauer, and quantum-chemical investigations of diiron complexes mimicking the active oxidized state of [FeFe]hydrogenase. / Silakov, Alexey; Olsen, Matthew T.; Sproules, Stephen; Reijerse, Eduard J.; Rauchfuss, Thomas B.; Lubitz, Wolfgang.

In: Inorganic Chemistry, Vol. 51, No. 15, 06.08.2012, p. 8617-8628.

Research output: Contribution to journalArticle

TY - JOUR

T1 - EPR/ENDOR, Mössbauer, and quantum-chemical investigations of diiron complexes mimicking the active oxidized state of [FeFe]hydrogenase

AU - Silakov, Alexey

AU - Olsen, Matthew T.

AU - Sproules, Stephen

AU - Reijerse, Eduard J.

AU - Rauchfuss, Thomas B.

AU - Lubitz, Wolfgang

PY - 2012/8/6

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N2 - Understanding the catalytic process of the heterolytic splitting and formation of molecular hydrogen is one of the key topics for the development of a future hydrogen economy. With an interest in elucidating the enzymatic mechanism of the [Fe 2 (S 2 C 2 H 4 NH)(CN) 2 (CO) 2 (μ-CO)] active center uniquely found in [FeFe]hydrogenases, we present a detailed spectroscopic and theoretical analysis of its inorganic model [Fe 2 (S 2 X)(CO) 3 (dppv) (PMe 3 )] + [dppv = cis-1,2-bis(diphenylphosphino)ethylene] in two forms with S 2 X = ethanedithiolate (1edt) and azadithiolate (1adt). These complexes represent models for the oxidized mixed-valent Fe I Fe II state analogous to the active oxidized "H ox " state of the native H-cluster. For both complexes, the 31 P hyperfine interactions were determined by pulse electron paramagnetic resonance and electron nuclear double resonance (ENDOR) methods. For 1edt, the 57 Fe parameters were measured by electron spin-echo envelope modulation and Mössbauer spectroscopy, while for 1adt, 14 N and selected 1 H couplings could be obtained by ENDOR and hyperfine sublevel correlation spectroscopy. The spin density was found to be predominantly localized on the Fe(dppv) site. This spin distribution is different from that of the H-cluster, where both the spin and charge densities are delocalized over the two Fe centers. This difference is attributed to the influence of the "native" cubane subcluster that is lacking in the inorganic models. The degree and character of the unpaired spin delocalization was found to vary from 1edt, with an abiological dithiolate, to 1adt, which features the authentic cofactor. For 1adt, we find two 14 N signals, which are indicative for two possible isomers of the azadithiolate, demonstrating its high flexibility. All interaction parameters were also evaluated through density functional theory calculations at various levels.

AB - Understanding the catalytic process of the heterolytic splitting and formation of molecular hydrogen is one of the key topics for the development of a future hydrogen economy. With an interest in elucidating the enzymatic mechanism of the [Fe 2 (S 2 C 2 H 4 NH)(CN) 2 (CO) 2 (μ-CO)] active center uniquely found in [FeFe]hydrogenases, we present a detailed spectroscopic and theoretical analysis of its inorganic model [Fe 2 (S 2 X)(CO) 3 (dppv) (PMe 3 )] + [dppv = cis-1,2-bis(diphenylphosphino)ethylene] in two forms with S 2 X = ethanedithiolate (1edt) and azadithiolate (1adt). These complexes represent models for the oxidized mixed-valent Fe I Fe II state analogous to the active oxidized "H ox " state of the native H-cluster. For both complexes, the 31 P hyperfine interactions were determined by pulse electron paramagnetic resonance and electron nuclear double resonance (ENDOR) methods. For 1edt, the 57 Fe parameters were measured by electron spin-echo envelope modulation and Mössbauer spectroscopy, while for 1adt, 14 N and selected 1 H couplings could be obtained by ENDOR and hyperfine sublevel correlation spectroscopy. The spin density was found to be predominantly localized on the Fe(dppv) site. This spin distribution is different from that of the H-cluster, where both the spin and charge densities are delocalized over the two Fe centers. This difference is attributed to the influence of the "native" cubane subcluster that is lacking in the inorganic models. The degree and character of the unpaired spin delocalization was found to vary from 1edt, with an abiological dithiolate, to 1adt, which features the authentic cofactor. For 1adt, we find two 14 N signals, which are indicative for two possible isomers of the azadithiolate, demonstrating its high flexibility. All interaction parameters were also evaluated through density functional theory calculations at various levels.

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