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Title: Terminal Hydride Species in [FeFe]-Hydrogenases are Vibrationally Coupled to the Active Site Environment

Abstract

A combination of nuclear resonance vibrational spectroscopy (NRVS), FTIR spectroscopy, and DFT calculations was used to observe and characterize Fe-H/D bending modes in CrHydA1 [FeFe]-hydrogenase Cys-to-Ser variant C169S. Mutagenesis of cysteine to serine at position169 changes the functional group adjacent to the H-cluster from a -SH to -OH, thus altering the proton transfer pathway. The catalytic activity of C169S is significantly reduced compared to that of native CrHydA1, presumably owing to less efficient proton transfer to the H-cluster. This mutation enabled effective capture of a hydride/deuteride intermediate and facilitated direct detection of the Fe-H/D normal modes. We observed a significant shift to higher frequency in an Fe-H bending mode of the C169S variant, as compared to previous findings with reconstituted native and oxadithiolate (ODT)-substituted CrHydA1. On the basis of DFT calculations, we propose that this shift is caused by the stronger interaction of the -OH group of C169S with the bridgehead -NH- moiety of the active site, as compared to that of the -SH group of C169 in the native enzyme.

Authors:
 [1];  [1];  [2];  [3];  [2];  [2];  [1];  [1];  [4];  [5];  [5];  [6];  [6]
+ Show Author Affiliations
  1. Univ. of California, Davis, CA (United States)
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  3. Technische Univ. Berlin, Berlin (Germany)
  4. Argonne National Lab. (ANL), Argonne, IL (United States)
  5. Argonne National Lab. (ANL), Lemont, IL (United States)
  6. JASRI (Japan)
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1458904
Alternate Identifier(s):
OSTI ID: 1461219; OSTI ID: 1480684
Report Number(s):
NREL/JA-2700-71499
Journal ID: ISSN 1433-7851
Grant/Contract Number:  
AC36-08GO28308; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Angewandte Chemie (International Edition)
Additional Journal Information:
Journal Name: Angewandte Chemie (International Edition); Journal Volume: 57; Journal Issue: 33; Journal ID: ISSN 1433-7851
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; hydrogenase; NRVS; FTIR; synchrotron radiation

Citation Formats

Cramer, Stephen Paul, Pham, Cindy C., Mulder, David W., Pelmenschikov, Vladimir, King, Paul W., Ratzloff, Michael W., Wang, Hongxin, Mishra, Nakul, Alp, Ercan, Zhao, Jiyong, Hu, Michael Y., Tamasaku, Kenji, and Yoda, Yoshitaka. Terminal Hydride Species in [FeFe]-Hydrogenases are Vibrationally Coupled to the Active Site Environment. United States: N. p., 2018. Web. doi:10.1002/anie.201805144.
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Cramer, Stephen Paul, Pham, Cindy C., Mulder, David W., Pelmenschikov, Vladimir, King, Paul W., Ratzloff, Michael W., Wang, Hongxin, Mishra, Nakul, Alp, Ercan, Zhao, Jiyong, Hu, Michael Y., Tamasaku, Kenji, & Yoda, Yoshitaka. Terminal Hydride Species in [FeFe]-Hydrogenases are Vibrationally Coupled to the Active Site Environment. United States. https://doi.org/10.1002/anie.201805144
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Cramer, Stephen Paul, Pham, Cindy C., Mulder, David W., Pelmenschikov, Vladimir, King, Paul W., Ratzloff, Michael W., Wang, Hongxin, Mishra, Nakul, Alp, Ercan, Zhao, Jiyong, Hu, Michael Y., Tamasaku, Kenji, and Yoda, Yoshitaka. Tue . "Terminal Hydride Species in [FeFe]-Hydrogenases are Vibrationally Coupled to the Active Site Environment". United States. https://doi.org/10.1002/anie.201805144. https://www.osti.gov/servlets/purl/1458904.
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@article{osti_1458904,
title = {Terminal Hydride Species in [FeFe]-Hydrogenases are Vibrationally Coupled to the Active Site Environment},
author = {Cramer, Stephen Paul and Pham, Cindy C. and Mulder, David W. and Pelmenschikov, Vladimir and King, Paul W. and Ratzloff, Michael W. and Wang, Hongxin and Mishra, Nakul and Alp, Ercan and Zhao, Jiyong and Hu, Michael Y. and Tamasaku, Kenji and Yoda, Yoshitaka},
abstractNote = {A combination of nuclear resonance vibrational spectroscopy (NRVS), FTIR spectroscopy, and DFT calculations was used to observe and characterize Fe-H/D bending modes in CrHydA1 [FeFe]-hydrogenase Cys-to-Ser variant C169S. Mutagenesis of cysteine to serine at position169 changes the functional group adjacent to the H-cluster from a -SH to -OH, thus altering the proton transfer pathway. The catalytic activity of C169S is significantly reduced compared to that of native CrHydA1, presumably owing to less efficient proton transfer to the H-cluster. This mutation enabled effective capture of a hydride/deuteride intermediate and facilitated direct detection of the Fe-H/D normal modes. We observed a significant shift to higher frequency in an Fe-H bending mode of the C169S variant, as compared to previous findings with reconstituted native and oxadithiolate (ODT)-substituted CrHydA1. On the basis of DFT calculations, we propose that this shift is caused by the stronger interaction of the -OH group of C169S with the bridgehead -NH- moiety of the active site, as compared to that of the -SH group of C169 in the native enzyme.},
doi = {10.1002/anie.201805144},
journal = {Angewandte Chemie (International Edition)},
number = 33,
volume = 57,
place = {United States},
year = {Tue Jun 19 00:00:00 EDT 2018},
month = {Tue Jun 19 00:00:00 EDT 2018}
}
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https://doi.org/10.1002/anie.201805144
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Cited by: 23 works
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Figures / Tables:

Figure 1 Figure 1: Structural representation of the primary proton transport chain and H2 bond activation at the H-cluster of [FeFe]-H2ase. The ADT ligand and C169 residue link proton transfer events to terminal hydride formation at [2Fe]H through an extended hydrogen-bonding network (dotted lines) composed of several conserved amino acids; crystal structuremore » from PDB 3C8Y was used for this illustration, and the amino-acid numbering is from the CrHydA1 primary sequence. Protonation sites (-H) on [2Fe]H of the Hhyd state are shown.« less
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Works referenced in this record:

Exploring Properties of a Hyperthermophilic Membrane-Bound Hydrogenase at Carbon Nanotube Modified Electrodes for a Powerful H 2 /O 2 Biofuel Cell
journal, January 2013

  • De Poulpiquet, Anne; Ciaccafava, Alexandre; Szot, Katarzyna
  • Electroanalysis, Vol. 25, Issue 3
  • DOI: 10.1002/elan.201200405

A structural view of synthetic cofactor integration into [FeFe]-hydrogenases
journal, January 2016

  • Esselborn, J.; Muraki, N.; Klein, K.
  • Chemical Science, Vol. 7, Issue 2
  • DOI: 10.1039/C5SC03397G

Structure/Function Relationships of [NiFe]- and [FeFe]-Hydrogenases. ( Chem. Rev. 2007 , 107 , 4273−4303. Published on the Web September 13, 2007.)
journal, November 2007

  • Fontecilla-Camps, Juan C.; Volbeda, Anne; Cavazza, Christine
  • Chemical Reviews, Vol. 107, Issue 11
  • DOI: 10.1021/cr078107t

Cyanide-bridged iron complexes as biomimetics of tri-iron arrangements in maturases of the H cluster of the di-iron hydrogenase
journal, January 2016

  • Lunsford, Allen M.; Beto, Christopher C.; Ding, Shengda
  • Chemical Science, Vol. 7, Issue 6
  • DOI: 10.1039/C6SC00213G

The quest for a functional substrate access tunnel in FeFe hydrogenase
journal, January 2011

  • Lautier, Thomas; Ezanno, Pierre; Baffert, Carole
  • Faraday Discuss., Vol. 148
  • DOI: 10.1039/C004099C

Biomimetic assembly and activation of [FeFe]-hydrogenases
journal, June 2013

  • Berggren, G.; Adamska, A.; Lambertz, C.
  • Nature, Vol. 499, Issue 7456
  • DOI: 10.1038/nature12239

Sterically Stabilized Terminal Hydride of a Diiron Dithiolate
journal, January 2018

Spontaneous activation of [FeFe]-hydrogenases by an inorganic [2Fe] active site mimic
journal, August 2013

  • Esselborn, Julian; Lambertz, Camilla; Adamska-Venkatesh, Agnieszka
  • Nature Chemical Biology, Vol. 9, Issue 10
  • DOI: 10.1038/nchembio.1311

Investigations on the Role of Proton-Coupled Electron Transfer in Hydrogen Activation by [FeFe]-Hydrogenase
journal, October 2014

  • Mulder, David W.; Ratzloff, Michael W.; Bruschi, Maurizio
  • Journal of the American Chemical Society, Vol. 136, Issue 43
  • DOI: 10.1021/ja508629m

Catalytic Turnover of [FeFe]-Hydrogenase Based on Single-Molecule Imaging
journal, October 2011

  • Madden, Christopher; Vaughn, Michael D.; Díez-Pérez, Ismael
  • Journal of the American Chemical Society, Vol. 134, Issue 3
  • DOI: 10.1021/ja207461t

Artificial hydrogenases
journal, June 2010

  • Barton, Bryan E.; Olsen, Matthew T.; Rauchfuss, Thomas B.
  • Current Opinion in Biotechnology, Vol. 21, Issue 3
  • DOI: 10.1016/j.copbio.2010.03.003

[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation
journal, June 2015

  • Peters, John W.; Schut, Gerrit J.; Boyd, Eric S.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6
  • DOI: 10.1016/j.bbamcr.2014.11.021

Proton Coupled Electronic Rearrangement within the H-Cluster as an Essential Step in the Catalytic Cycle of [FeFe] Hydrogenases
journal, January 2017

  • Sommer, Constanze; Adamska-Venkatesh, Agnieszka; Pawlak, Krzysztof
  • Journal of the American Chemical Society, Vol. 139, Issue 4
  • DOI: 10.1021/jacs.6b12636

Identification of a Catalytic Iron-Hydride at the H-Cluster of [FeFe]-Hydrogenase
journal, December 2016

  • Mulder, David W.; Guo, Yisong; Ratzloff, Michael W.
  • Journal of the American Chemical Society, Vol. 139, Issue 1
  • DOI: 10.1021/jacs.6b11409

Heterolytic Cleavage of Hydrogen by an Iron Hydrogenase Model: An Fe-H⋅⋅⋅H-N Dihydrogen Bond Characterized by Neutron Diffraction
journal, April 2014

  • Liu, Tianbiao; Wang, Xiaoping; Hoffmann, Christina
  • Angewandte Chemie International Edition, Vol. 53, Issue 21
  • DOI: 10.1002/anie.201402090

Direct Observation of an Iron-Bound Terminal Hydride in [FeFe]-Hydrogenase by Nuclear Resonance Vibrational Spectroscopy
journal, March 2017

  • Reijerse, Edward J.; Pham, Cindy C.; Pelmenschikov, Vladimir
  • Journal of the American Chemical Society, Vol. 139, Issue 12
  • DOI: 10.1021/jacs.7b00686

Dithiomethylether as a Ligand in the Hydrogenase H-Cluster
journal, April 2008

  • Pandey, Arti S.; Harris, Travis V.; Giles, Logan J.
  • Journal of the American Chemical Society, Vol. 130, Issue 13
  • DOI: 10.1021/ja711187e

Phonon Density of States Measured by Inelastic Nuclear Resonant Scattering
journal, May 1995

Artificially maturated [FeFe] hydrogenase from Chlamydomonas reinhardtii: a HYSCORE and ENDOR study of a non-natural H-cluster
journal, January 2015

  • Adamska-Venkatesh, Agnieszka; Simmons, Trevor R.; Siebel, Judith F.
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 7
  • DOI: 10.1039/C4CP05426A

Spectroscopic Investigations of [FeFe] Hydrogenase Maturated with [ 57 Fe 2 (adt)(CN) 2 (CO) 4 ] 2–
journal, July 2015

  • Gilbert-Wilson, Ryan; Siebel, Judith F.; Adamska-Venkatesh, Agnieszka
  • Journal of the American Chemical Society, Vol. 137, Issue 28
  • DOI: 10.1021/jacs.5b03270

Molecular dynamics study of the proposed proton transport pathways in [FeFe]-hydrogenase
journal, January 2014

  • Ginovska-Pangovska, Bojana; Ho, Ming-Hsun; Linehan, John C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 1
  • DOI: 10.1016/j.bbabio.2013.08.004

Importance of the Protein Framework for Catalytic Activity of [FeFe]-Hydrogenases
journal, November 2011

  • Knörzer, Philipp; Silakov, Alexey; Foster, Carina E.
  • Journal of Biological Chemistry, Vol. 287, Issue 2
  • DOI: 10.1074/jbc.M111.305797

Proton Transport in Clostridium pasteurianum [FeFe] Hydrogenase I: A Computational Study
journal, January 2014

  • Long, Hai; King, Paul W.; Chang, Christopher H.
  • The Journal of Physical Chemistry B, Vol. 118, Issue 4
  • DOI: 10.1021/jp408621r

Reaction Coordinate Leading to H 2 Production in [FeFe]-Hydrogenase Identified by Nuclear Resonance Vibrational Spectroscopy and Density Functional Theory
journal, November 2017

  • Pelmenschikov, Vladimir; Birrell, James A.; Pham, Cindy C.
  • Journal of the American Chemical Society, Vol. 139, Issue 46
  • DOI: 10.1021/jacs.7b09751

Mechanism of Proton Transfer in [FeFe]-Hydrogenase from Clostridium pasteurianum
journal, September 2011

  • Cornish, Adam J.; Gärtner, Katrin; Yang, Hui
  • Journal of Biological Chemistry, Vol. 286, Issue 44
  • DOI: 10.1074/jbc.M111.254664

Heterolytic Cleavage of Hydrogen by an Iron Hydrogenase Model: An Fe-H⋅⋅⋅H-N Dihydrogen Bond Characterized by Neutron Diffraction
journal, April 2014

  • Liu, Tianbiao; Wang, Xiaoping; Hoffmann, Christina
  • Angewandte Chemie, Vol. 126, Issue 21
  • DOI: 10.1002/ange.201402090

Hydrogenases
journal, March 2014

  • Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf
  • Chemical Reviews, Vol. 114, Issue 8
  • DOI: 10.1021/cr4005814
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    Works referencing / citing this record:

    Crystallographic and spectroscopic assignment of the proton transfer pathway in [FeFe]-hydrogenases
    journal, November 2018

    Asymmetry in the Ligand Coordination Sphere of the [FeFe] Hydrogenase Active Site Is Reflected in the Magnetic Spin Interactions of the Aza-propanedithiolate Ligand
    journal, October 2019

    • Reijerse, Edward J.; Pelmenschikov, Vladimir; Birrell, James A.
    • The Journal of Physical Chemistry Letters, Vol. 10, Issue 21
    • DOI: 10.1021/acs.jpclett.9b02354

    Spectroscopic and Computational Evidence that [FeFe] Hydrogenases Operate Exclusively with CO-Bridged Intermediates
    journal, December 2019

    • Birrell, James A.; Pelmenschikov, Vladimir; Mishra, Nakul
    • Journal of the American Chemical Society, Vol. 142, Issue 1
    • DOI: 10.1021/jacs.9b09745

    Crystallographic and spectroscopic assignment of the proton transfer pathway in [FeFe]-hydrogenases
    journal, November 2018

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