Vibrational characterization of a diiron bridging hydride complex – a model for hydrogen catalysis

Gee, Leland B.; Pelmenschikov, Vladimir; Wang, Hongxin; Mishra, Nakul; Liu, Yu-Chiao; Yoda, Yoshitaka; Tamasaku, Kenji; Chiang, Ming-Hsi; Cramer, Stephen P.

doi:10.1039/d0sc01290d

Title: Vibrational characterization of a diiron bridging hydride complex – a model for hydrogen catalysis

Journal Article · Wed May 06 00:00:00 EDT 2020 · Chemical Science

DOI:https://doi.org/10.1039/d0sc01290d· OSTI ID:1816881

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Stanford Univ., CA (United States). Dept. of Chemistry
Technische Univ. Berlin (Germany). Institut für Chemie
SETI Institute, Mountain View, CA (United States)
Univ. of California, Davis, CA (United States). Dept. of Chemistry
Academia Sinica; Taipei (Taiwan). Inst. of Chemistry; Kaohsiung Medical Univ., Kaohsiung (Taiwan). Dept. of Medicinal and Applied Chemistry
Japan Synchrotron Radiation Research Inst. (JASRI), Hyogo (Japan)
RIKEN, Hyogo (Japan)

A diiron complex containing a bridging hydride and a protonated terminal thiolate of the form [(m,k₂- bdtH)(m-PPh₂)(m-H)Fe₂(CO)₅]⁺ has been investigated through ⁵⁷Fe nuclear resonance vibrational spectroscopy (NRVS) and interpreted using density functional theory (DFT) calculations. We report the Fe–mH–Fe wagging mode, and indications for Fe–mD stretching vibrations in the D-isotopologue, observed by ⁵⁷Fe-NRVS. Our combined approach demonstrates an asymmetric sharing of the hydride between the two iron sites that yields two nondegenerate Fe–mH/D stretching vibrations. The studied complex provides an important model relevant to biological hydrogen catalysis intermediates. The complex mimics proposals for the binuclear metal sites in [FeFe] and [NiFe] hydrogenases. It is also an appealing prototype for the ‘Janus intermediate’ of nitrogenase, which has been proposed to contain two bridging Fe–H–Fe hydrides and two protonated sulfurs at the FeMo-cofactor. The significance of observing indirect effects of the bridging hydride, as well as obstacles in its direct observation, is discussed in the context of biological hydrogen intermediates.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Science Foundation (NSF); Einstein Foundation Berlin; German Research Foundation (DFG); Ministry of Science and Technology of Taiwan and Academia Sinica

Grant/Contract Number:: AC02-05CH11231; GM-65440; CHE 1308384; EVF-2016-277; EXC 2008-390540038; AS-SS-108-02-1

OSTI ID:: 1816881

Journal Information:: Chemical Science, Vol. 11, Issue 21; ISSN 2041-6520

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

High-Frequency Fe-H Vibrations in a Bridging Hydride Complex Characterized by NRVS and DFT Pelmenschikov, Vladimir; Gee, Leland B.; Wang, Hongxin Angewandte Chemie, Vol. 130, Issue 30 https://doi.org/10.1002/ange.201804601	journal	June 2018
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview Vignais, Paulette M.; Billoud, Bernard Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272 https://doi.org/10.1021/cr050196r	journal	October 2007
Sterically Stabilized Terminal Hydride of a Diiron Dithiolate Carlson, Michaela R.; Gray, Danielle L.; Richers, Casseday P. Inorganic Chemistry, Vol. 57, Issue 4 https://doi.org/10.1021/acs.inorgchem.7b02903	journal	January 2018
First-principles calculation of nuclear resonance vibrational spectra Petrenko, Taras; Sturhahn, Wolfgang; Neese, Frank Hyperfine Interactions, Vol. 175, Issue 1-3 https://doi.org/10.1007/s10751-008-9600-5	journal	February 2007
[FeFe] hydrogenase active site modeling: a key intermediate bearing a thiolate proton and Fe hydride Liu, Yu-Chiao; Chu, Kai-Ti; Jhang, Ruei-Lin Chemical Communications, Vol. 49, Issue 42 https://doi.org/10.1039/c3cc39008j	journal	January 2013
What Can Be Learned from Nuclear Resonance Vibrational Spectroscopy: Vibrational Dynamics and Hemes Scheidt, W. Robert; Li, Jianfeng; Sage, J. Timothy Chemical Reviews, Vol. 117, Issue 19 https://doi.org/10.1021/acs.chemrev.7b00295	journal	September 2017
Mo-, V-, and Fe-Nitrogenases Use a Universal Eight-Electron Reductive-Elimination Mechanism To Achieve N ₂ Reduction Harris, Derek F.; Lukoyanov, Dmitriy A.; Kallas, Hayden Biochemistry, Vol. 58, Issue 30 https://doi.org/10.1021/acs.biochem.9b00468	journal	June 2019
High-Frequency Fe-H Vibrations in a Bridging Hydride Complex Characterized by NRVS and DFT Pelmenschikov, Vladimir; Gee, Leland B.; Wang, Hongxin Angewandte Chemie International Edition, Vol. 57, Issue 30 https://doi.org/10.1002/anie.201804601	journal	June 2018
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
The atomic-resolution crystal structure of activated [Fe]-hydrogenase Huang, Gangfeng; Wagner, Tristan; Wodrich, Matthew D. Nature Catalysis, Vol. 2, Issue 6 https://doi.org/10.1038/s41929-019-0289-4	journal	June 2019
Mechanism of N ₂ Reduction Catalyzed by Fe-Nitrogenase Involves Reductive Elimination of H ₂ Harris, Derek F.; Lukoyanov, Dmitriy A.; Shaw, Sudipta Biochemistry, Vol. 57, Issue 5 https://doi.org/10.1021/acs.biochem.7b01142	journal	January 2018
An insight into the protonation property of a diiron azadithiolate complex pertinent to the active site of Fe-only hydrogenases Dong, Weibing; Wang, Mei; Liu, Xiaoyang Chem. Commun., Issue 3 https://doi.org/10.1039/B513270C	journal	January 2006
Hydrogenase Enzymes and Their Synthetic Models: The Role of Metal Hydrides Schilter, David; Camara, James M.; Huynh, Mioy T. Chemical Reviews, Vol. 116, Issue 15 https://doi.org/10.1021/acs.chemrev.6b00180	journal	June 2016
Synthetic Analogues of the Active Sites of Nitrogenase and [NiFe] Hydrogenase Ohki, Yasuhiro Bulletin of the Chemical Society of Japan, Vol. 87, Issue 1 https://doi.org/10.1246/bcsj.20130207	journal	January 2014
Identification of a Catalytic Iron-Hydride at the H-Cluster of [FeFe]-Hydrogenase Mulder, David W.; Guo, Yisong; Ratzloff, Michael W. Journal of the American Chemical Society, Vol. 139, Issue 1 https://doi.org/10.1021/jacs.6b11409	journal	December 2016
Direct Observation of an Iron-Bound Terminal Hydride in [FeFe]-Hydrogenase by Nuclear Resonance Vibrational Spectroscopy Reijerse, Edward J.; Pham, Cindy C.; Pelmenschikov, Vladimir Journal of the American Chemical Society, Vol. 139, Issue 12 https://doi.org/10.1021/jacs.7b00686	journal	March 2017
Crystallographic and spectroscopic assignment of the proton transfer pathway in [FeFe]-hydrogenases Duan, Jifu; Senger, Moritz; Esselborn, Julian Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07140-x	journal	November 2018
Direct Detection of the Terminal Hydride Intermediate in [FeFe] Hydrogenase by NMR Spectroscopy Rumpel, Sigrun; Sommer, Constanze; Reijerse, Edward Journal of the American Chemical Society, Vol. 140, Issue 11 https://doi.org/10.1021/jacs.8b00459	journal	March 2018
Dynamics of Rhodobacter capsulatus [2Fe-2S] Ferredoxin VI and Aquifex aeolicus Ferredoxin 5 via Nuclear Resonance Vibrational Spectroscopy (NRVS) and Resonance Raman Spectroscopy ^† Xiao, Yuming; Tan, Ming-Liang; Ichiye, Toshiko Biochemistry, Vol. 47, Issue 25 https://doi.org/10.1021/bi701433m	journal	June 2008
Protonation/Reduction of Carbonyl-Rich Diiron Complexes and the Direct Observation of Triprotonated Species: Insights into the Electrocatalytic Mechanism of Hydrogen Formation Liu, Yu-Chiao; Chu, Kai-Ti; Huang, Yi-Lan ACS Catalysis, Vol. 6, Issue 4 https://doi.org/10.1021/acscatal.5b02646	journal	March 2016
H2 and O2 activation by [NiFe]hydrogenases – Insights from model complexes Ogo, Seiji Coordination Chemistry Reviews, Vol. 334 https://doi.org/10.1016/j.ccr.2016.07.001	journal	March 2017
Models for the Active Site in [FeFe] Hydrogenase with Iron-Bound Ligands Derived from Bis-, Tris-, and Tetrakis(mercaptomethyl)silanes Apfel, Ulf-Peter; Troegel, Dennis; Halpin, Yvonne Inorganic Chemistry, Vol. 49, Issue 21 https://doi.org/10.1021/ic101399k	journal	November 2010
Reversible Photoinduced Reductive Elimination of H ₂ from the Nitrogenase Dihydride State, the E ₄ (4H) Janus Intermediate Lukoyanov, Dmitriy; Khadka, Nimesh; Yang, Zhi-Yong Journal of the American Chemical Society, Vol. 138, Issue 4 https://doi.org/10.1021/jacs.5b11650	journal	January 2016
Differential Protonation at the Catalytic Six-Iron Cofactor of [FeFe]-Hydrogenases Revealed by ⁵⁷ Fe Nuclear Resonance X-ray Scattering and Quantum Mechanics/Molecular Mechanics Analyses Mebs, Stefan; Duan, Jifu; Wittkamp, Florian Inorganic Chemistry, Vol. 58, Issue 6 https://doi.org/10.1021/acs.inorgchem.9b00100	journal	February 2019
Reaction Coordinate Leading to H ₂ Production in [FeFe]-Hydrogenase Identified by Nuclear Resonance Vibrational Spectroscopy and Density Functional Theory Pelmenschikov, Vladimir; Birrell, James A.; Pham, Cindy C. Journal of the American Chemical Society, Vol. 139, Issue 46 https://doi.org/10.1021/jacs.7b09751	journal	November 2017
Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenase Ogata, Hideaki; Nishikawa, Koji; Lubitz, Wolfgang Nature, Vol. 520, Issue 7548 https://doi.org/10.1038/nature14110	journal	January 2015
Classification and phylogeny of hydrogenases Vignais, Paulette M.; Billoud, Bernard; Meyer, Jacques FEMS Microbiology Reviews, Vol. 25, Issue 4, p. 455-501 https://doi.org/10.1111/j.1574-6976.2001.tb00587.x	journal	August 2001
Proton affinity studies of nickel N2S2 complexes and control of aggregation Arnet, Nicholas A.; Bhuvanesh, Nattamai; Darensbourg, Marcetta Y. JBIC Journal of Biological Inorganic Chemistry, Vol. 24, Issue 6 https://doi.org/10.1007/s00775-019-01671-4	journal	June 2019
Normal Mode Analysis of Pyrococcus furiosus Rubredoxin via Nuclear Resonance Vibrational Spectroscopy (NRVS) and Resonance Raman Spectroscopy Xiao, Yuming; Wang, Hongxin; George, Simon J. Journal of the American Chemical Society, Vol. 127, Issue 42 https://doi.org/10.1021/ja042960h	journal	October 2005
Terminal Hydride Species in [FeFe]‐Hydrogenases Are Vibrationally Coupled to the Active Site Environment Pham, Cindy C.; Mulder, David W.; Pelmenschikov, Vladimir Angewandte Chemie International Edition, Vol. 57, Issue 33 https://doi.org/10.1002/anie.201805144	journal	August 2018
Directing protonation in [FeFe] hydrogenase active site models by modifications in their second coordination sphere Ezzaher, Salah; Gogoll, Adolf; Bruhn, Clemens Chemical Communications, Vol. 46, Issue 31 https://doi.org/10.1039/c0cc00724b	journal	January 2010
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
Metallodithiolates as Ligands in Coordination, Bioinorganic, and Organometallic Chemistry Denny, Jason A.; Darensbourg, Marcetta Y. Chemical Reviews, Vol. 115, Issue 11 https://doi.org/10.1021/cr500659u	journal	May 2015
Spectroscopic and Computational Evidence that [FeFe] Hydrogenases Operate Exclusively with CO-Bridged Intermediates Birrell, James A.; Pelmenschikov, Vladimir; Mishra, Nakul Journal of the American Chemical Society, Vol. 142, Issue 1 https://doi.org/10.1021/jacs.9b09745	journal	December 2019
Hydride Binding to the Active Site of [FeFe]-Hydrogenase Chernev, Petko; Lambertz, Camilla; Brünje, Annika Inorganic Chemistry, Vol. 53, Issue 22 https://doi.org/10.1021/ic502047q	journal	October 2014
Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy Ogata, Hideaki; Krämer, Tobias; Wang, Hongxin Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8890	journal	August 2015

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