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Hyperfine interactions and electron distribution in FeIIFeI and FeIFeI models for the active site of the [FeFe] hydrogenases: Mössbauer spectroscopy studies of low-spin FeI

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Abstract

Mössbauer studies of [{μ-S(CH2C(CH3)2CH2S}(μ-CO)FeIIFeI(PMe3)2(CO)3]PF6 (1 OX ), a model complex for the oxidized state of the [FeFe] hydrogenases, and the parent FeIFeI derivative are reported. The paramagnetic 1 OX is part of a series featuring a dimethylpropanedithiolate bridge, introducing steric hindrance with profound impact on the electronic structure of the diiron complex. Well-resolved spectra of 1 OX allow determination of the magnetic hyperfine couplings for the low-spin distal FeI (\( {\text{Fe}}^{\text{I}} _{\text{ D}} \)) site, A x,y,z  = [−24 (6), −12 (2), 20 (2)] MHz, and the detection of significant internal fields (approximately 2.3 T) at the low-spin ferrous site, confirmed by density functional theory (DFT) calculations. Mössbauer spectra of 1 OX show nonequivalent sites and no evidence of delocalization up to 200 K. Insight from the experimental hyperfine tensors of the FeI site is used in correlation with DFT to reveal the spatial distribution of metal orbitals. The Fe–Fe bond in [Fe2{μ-S(CH2C(CH3)2CH2S}(PMe3)2(CO)4] (1) involving two \( d_{{z^{2} }} \)-type orbitals is crucial in keeping the structure intact in the presence of strain. On oxidation, the distal iron site is not restricted by the Fe–Fe bond, and thus the more stable isomer results from inversion of the square pyramid, rotating the \( d_{{z^{2} }} \) orbital of \( {\text{Fe}}^{\text{I}} _{\text{ D}} \). DFT calculations imply that the Mössbauer properties can be traced to this \( d_{{z^{2} }} \) orbital. The structure of the magnetic hyperfine coupling tensor, A, of the low-spin FeI in 1 OX is discussed in the context of the known A tensors for the oxidized states of the [FeFe] hydrogenases.

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Notes

  1. All cited isomer shifts were adjusted to values at 5 K.

  2. Signs are determined by Mössbauer spectroscopy.

Abbreviations

DFT:

Density functional theory

ENDOR:

Electron–nuclear double resonance

EFG:

Electric field gradient

FeD :

Distal iron

FeP :

Proximal iron

HYSCORE:

Hyperfine sublevel correlation

PES:

Potential energy surface

SCF:

Self-consistent field

TD:

Time dependent

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Acknowledgments

C.V.P. is grateful to Eckard Münck for support and discussions, and for allowing her to use his laboratory to collect spectra and train undergraduate students. C.V.P. thanks Alex Guo and Katlyn Meier for their help and acknowledges the Ursinus College Faculty Development and Summer Fellows programs. The authors acknowledge the reviewers for the useful comments and suggestions for improvement during the review process. Funding for this research was provided by the National Science Foundation (CHE-0956779 to C.V.P., CHE-0910679 to M.Y.D.). S.A.S. acknowledges grant CHE-1012485 to E. Münck. M.Y.D. acknowledges the Welch Foundation (A-0924 to M.Y.D.).

Author information

Authors and Affiliations

  1. Department of Chemistry, Carnegie Mellon University, Pittsburgh, PA, 15213, USA

    Sebastian A. Stoian

  2. Department of Chemistry, Texas A&M University, College Station, TX, 77843, USA

    Chung-Hung Hsieh, Michael L. Singleton & Marcetta Y. Darensbourg

  3. Department of Chemistry, Ursinus College, Collegeville, PA, 19426, USA

    Andrea F. Casuras, Kelsey McNeely, Kurt Sweely & Codrina V. Popescu

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  1. Sebastian A. Stoian
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  2. Chung-Hung Hsieh
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  4. Andrea F. Casuras
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  5. Marcetta Y. Darensbourg
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  6. Kelsey McNeely
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  8. Codrina V. Popescu
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Corresponding author

Correspondence to Codrina V. Popescu.

Electronic supplementary material

The electronic supplementary material contains views of the unit cell of 1, calculated EFG components for conformers of 1, DFT-calculated metric parameters and the optimized geometries of compounds 1 and 1 OX , tabulated experimental and calculated values for components of the A tensors (57Fe and 31P) and visualization of the 57Fe EFG and A tensors for 1 OX , and tabulated gross orbital populations and spin densities of 1 OX .

This material is available free of charge via http://www.chem.umn.edu/jbic/.

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Stoian, S.A., Hsieh, CH., Singleton, M.L. et al. Hyperfine interactions and electron distribution in FeIIFeI and FeIFeI models for the active site of the [FeFe] hydrogenases: Mössbauer spectroscopy studies of low-spin FeI . J Biol Inorg Chem 18, 609–622 (2013). https://doi.org/10.1007/s00775-013-1005-5

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  • DOI: https://doi.org/10.1007/s00775-013-1005-5

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