Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase
Abstract
Hydrogenases couple electrochemical potential to the reversible chemical transformation of H2 and protons, yet the reaction mechanism and composition of intermediates are not fully understood. In this Communication we describe the biophysical properties of a hydride-bound state (Hhyd) of the [FeFe]-hydrogenase from Chlamydomonas reinhardtii. The catalytic H-cluster of [FeFe]-hydrogenase consists of a [4Fe-4S] subcluster ([4Fe-4S]H) linked by a cysteine thiol to an azadithiolate-bridged 2Fe subcluster ([2Fe]H) with CO and CN- ligands. Mossbauer analysis and density functional theory (DFT) calculations show that Hhyd consists of a reduced [4Fe-4S]H+ coupled to a diferrous [2Fe]H with a terminally bound Fe-hydride. The existence of the Fe-hydride in Hhyd was demonstrated by an unusually low Mossbauer isomer shift of the distal Fe of the [2Fe]H subcluster. As a result, a DFT model of Hhyd shows that the Fe-hydride is part of a H-bonding network with the nearby bridging azadithiolate to facilitate fast proton exchange and catalytic turnover.
- Authors:
-
[2];
[1]
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Carnegie Mellon Univ., Pittsburgh, PA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1340645
- Report Number(s):
- NREL/JA-2700-67578
Journal ID: ISSN 0002-7863
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of the American Chemical Society
- Additional Journal Information:
- Journal Volume: 139; Journal Issue: 1; Journal ID: ISSN 0002-7863
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Chlamydomonas reinhardtii; [FeFe]-hydrogenase; electrochemical potential
Citation Formats
Mulder, David W., Guo, Yisong, Ratzloff, Michael W., and King, Paul W. Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase. United States: N. p., 2016.
Web. doi:10.1021/jacs.6b11409.
Mulder, David W., Guo, Yisong, Ratzloff, Michael W., & King, Paul W. Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase. United States. https://doi.org/10.1021/jacs.6b11409
Mulder, David W., Guo, Yisong, Ratzloff, Michael W., and King, Paul W. Wed .
"Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase". United States. https://doi.org/10.1021/jacs.6b11409. https://www.osti.gov/servlets/purl/1340645.
@article{osti_1340645,
title = {Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase},
author = {Mulder, David W. and Guo, Yisong and Ratzloff, Michael W. and King, Paul W.},
abstractNote = {Hydrogenases couple electrochemical potential to the reversible chemical transformation of H2 and protons, yet the reaction mechanism and composition of intermediates are not fully understood. In this Communication we describe the biophysical properties of a hydride-bound state (Hhyd) of the [FeFe]-hydrogenase from Chlamydomonas reinhardtii. The catalytic H-cluster of [FeFe]-hydrogenase consists of a [4Fe-4S] subcluster ([4Fe-4S]H) linked by a cysteine thiol to an azadithiolate-bridged 2Fe subcluster ([2Fe]H) with CO and CN- ligands. Mossbauer analysis and density functional theory (DFT) calculations show that Hhyd consists of a reduced [4Fe-4S]H+ coupled to a diferrous [2Fe]H with a terminally bound Fe-hydride. The existence of the Fe-hydride in Hhyd was demonstrated by an unusually low Mossbauer isomer shift of the distal Fe of the [2Fe]H subcluster. As a result, a DFT model of Hhyd shows that the Fe-hydride is part of a H-bonding network with the nearby bridging azadithiolate to facilitate fast proton exchange and catalytic turnover.},
doi = {10.1021/jacs.6b11409},
journal = {Journal of the American Chemical Society},
number = 1,
volume = 139,
place = {United States},
year = {2016},
month = {12}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 99 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution
journal, December 1998
- Peters, J. W.
- Science, Vol. 282, Issue 5395
Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center
journal, January 1999
- Nicolet, Yvain; Piras, Claudine; Legrand, Pierre
- Structure, Vol. 7, Issue 1, p. 13-23
14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridge
journal, January 2009
- Silakov, Alexey; Wenk, Brian; Reijerse, Eduard
- Physical Chemistry Chemical Physics, Vol. 11, Issue 31
Molecular basis of [FeFe]-hydrogenase function
journal, August 2013
- Winkler, Martin; Esselborn, Julian; Happe, Thomas
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Identification and Characterization of the “Super-Reduced” State of the H-Cluster in [FeFe] Hydrogenase: A New Building Block for the Catalytic Cycle?
journal, October 2012
- Adamska, Agnieszka; Silakov, Alexey; Lambertz, Camilla
- Angewandte Chemie International Edition, Vol. 51, Issue 46
EPR and FTIR Analysis of the Mechanism of H 2 Activation by [FeFe]-Hydrogenase HydA1 from Chlamydomonas reinhardtii
journal, April 2013
- Mulder, David W.; Ratzloff, Michael W.; Shepard, Eric M.
- Journal of the American Chemical Society, Vol. 135, Issue 18
Hydride Binding to the Active Site of [FeFe]-Hydrogenase
journal, October 2014
- Chernev, Petko; Lambertz, Camilla; Brünje, Annika
- Inorganic Chemistry, Vol. 53, Issue 22
New Redox States Observed in [FeFe] Hydrogenases Reveal Redox Coupling Within the H-Cluster
journal, July 2014
- Adamska-Venkatesh, Agnieszka; Krawietz, Danuta; Siebel, Judith
- Journal of the American Chemical Society, Vol. 136, Issue 32
Vibrational spectroscopy reveals the initial steps of biological hydrogen evolution
journal, January 2016
- Katz, S.; Noth, J.; Horch, M.
- Chemical Science, Vol. 7, Issue 11
A Capable Bridging Ligand for Fe-Only Hydrogenase: Density Functional Calculations of a Low-Energy Route for Heterolytic Cleavage and Formation of Dihydrogen
journal, April 2001
- Fan, Hua-Jun; Hall, Michael B.
- Journal of the American Chemical Society, Vol. 123, Issue 16
Bridging-hydride influence on the electronic structure of an [FeFe] hydrogenase active-site model complex revealed by XAES-DFT
journal, January 2013
- Leidel, Nils; Hsieh, Chung-Hung; Chernev, Petko
- Dalton Transactions, Vol. 42, Issue 21
Inaccessibility of the μ-hydride species in [FeFe] hydrogenases
journal, January 2014
- Finkelmann, Arndt R.; Stiebritz, Martin T.; Reiher, Markus
- Chem. Sci., Vol. 5, Issue 1
Combining acid–base, redox and substrate binding functionalities to give a complete model for the [FeFe]-hydrogenase
journal, October 2011
- Camara, James M.; Rauchfuss, Thomas B.
- Nature Chemistry, Vol. 4, Issue 1
Hydrogenase Enzymes and Their Synthetic Models: The Role of Metal Hydrides
journal, June 2016
- Schilter, David; Camara, James M.; Huynh, Mioy T.
- Chemical Reviews, Vol. 116, Issue 15
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
Spectroelectrochemical Characterization of the Active Site of the [FeFe] Hydrogenase HydA1 from Chlamydomonas reinhardtii
journal, August 2009
- Silakov, Alexey; Kamp, Christina; Reijerse, Eduard
- Biochemistry, Vol. 48, Issue 33
All-iron hydrogenase: synthesis, structure and properties of {2Fe3S}-assemblies related to the di-iron sub-site of the H-clusterElectronic supplementary information (ESI) available: crystal and structure refinement data for complexes 4a, 4b and 5a. See http://www.rsc.org/suppdata/dt/b2/b209690k/
journal, January 2003
- Razavet, Mathieu; Davies, Sian C.; Hughes, David L.
- Dalton Transactions, Issue 4
Structural and Spectroscopic Features of Mixed Valent Fe II Fe I Complexes and Factors Related to the Rotated Configuration of Diiron Hydrogenase
journal, July 2012
- Hsieh, Chung-Hung; Erdem, Özlen F.; Harman, Scott D.
- Journal of the American Chemical Society, Vol. 134, Issue 31
EPR/ENDOR, Mössbauer, and Quantum-Chemical Investigations of Diiron Complexes Mimicking the Active Oxidized State of [FeFe]Hydrogenase
journal, July 2012
- Silakov, Alexey; Olsen, Matthew T.; Sproules, Stephen
- Inorganic Chemistry, Vol. 51, Issue 15
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
journal, May 2013
- Stoian, Sebastian A.; Hsieh, Chung-Hung; Singleton, Michael L.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 18, Issue 6
Electronic Structure of the H Cluster in [Fe]-Hydrogenases
journal, September 1999
- Popescu, Codrina V.; Münck, Eckard
- Journal of the American Chemical Society, Vol. 121, Issue 34
Modeling the Active Sites in Metalloenzymes. 3. Density Functional Calculations on Models for [Fe]-Hydrogenase: Structures and Vibrational Frequencies of the Observed Redox Forms and the Reaction Mechanism at the Diiron Active Center
journal, April 2001
- Cao, Zexing; Hall, Michael B.
- Journal of the American Chemical Society, Vol. 123, Issue 16
A Density Functional Theory Study on the Active Center of Fe-Only Hydrogenase: Characterization and Electronic Structure of the Redox States
journal, May 2002
- Liu, Zhi-Pan; Hu, P.
- Journal of the American Chemical Society, Vol. 124, Issue 18
Targeting Intermediates of [FeFe]-Hydrogenase by CO and CN Vibrational Signatures
journal, May 2011
- Yu, Lian; Greco, Claudio; Bruschi, Maurizio
- Inorganic Chemistry, Vol. 50, Issue 9
Refining the Active Site Structure of Iron−Iron Hydrogenase Using Computational Infrared Spectroscopy
journal, April 2008
- Tye, Jesse W.; Darensbourg, Marcetta Y.; Hall, Michael B.
- Inorganic Chemistry, Vol. 47, Issue 7
Design and Characterization of Phosphine Iron Hydrides: Toward Hydrogen-Producing Catalysts
journal, July 2015
- Weber, Katharina; Weyhermüller, Thomas; Bill, Eckhard
- Inorganic Chemistry, Vol. 54, Issue 14
Mössbauer and computational investigation of a functional [NiFe] hydrogenase model complex
journal, January 2015
- Kochem, A.; Bill, E.; Neese, F.
- Chemical Communications, Vol. 51, Issue 11
The active site of the [FeFe]-hydrogenase from Desulfovibrio desulfuricans. II. Redox properties, light sensitivity and CO-ligand exchange as observed by infrared spectroscopy
journal, December 2005
- Roseboom, Winfried; De Lacey, Antonio L.; Fernandez, Victor M.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 1
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
Works referencing / citing this record:
In Vivo EPR Characterization of Semi-Synthetic [FeFe] Hydrogenases
journal, February 2018
- Mészáros, Lívia S.; Németh, Brigitta; Esmieu, Charlène
- Angewandte Chemie, Vol. 130, Issue 10
Accumulating the hydride state in the catalytic cycle of [FeFe]-hydrogenases
journal, July 2017
- Winkler, Martin; Senger, Moritz; Duan, Jifu
- Nature Communications, Vol. 8, Issue 1
Direct Noncovalent Activation of α,β-Unsaturated Aldehydes for the Stereodivergent Synthesis of Substituted Cyclohexenes
journal, April 2017
- Xie, Ji-Kang; Wang, Yang; Lin, Jun-Bing
- Chemistry - A European Journal, Vol. 23, Issue 28
The plasticity of redox cofactors: from metalloenzymes to redox-active DNA
journal, August 2018
- Hemschemeier, Anja; Happe, Thomas
- Nature Reviews Chemistry, Vol. 2, Issue 9
Protonation/reduction dynamics at the [4Fe–4S] cluster of the hydrogen-forming cofactor in [FeFe]-hydrogenases
journal, January 2018
- Senger, Moritz; Mebs, Stefan; Duan, Jifu
- Physical Chemistry Chemical Physics, Vol. 20, Issue 5
A [4Fe–4S]-Fe(CO)(CN)-l-cysteine intermediate is the first organometallic precursor in [FeFe] hydrogenase H-cluster bioassembly
journal, April 2018
- Rao, Guodong; Tao, Lizhi; Suess, Daniel L. M.
- Nature Chemistry, Vol. 10, Issue 5
A coordinatively saturated nickel complex supported by triazenido ligands: a new electrocatalyst for hydrogen generation via ligand-centered proton-transfer
journal, January 2017
- Xue, Dan; Luo, Su-Ping; Zhan, Shu-Zhong
- New Journal of Chemistry, Vol. 41, Issue 16
Crystallographic and spectroscopic assignment of the proton transfer pathway in [FeFe]-hydrogenases
journal, November 2018
- Duan, Jifu; Senger, Moritz; Esselborn, Julian
- Nature Communications, Vol. 9, Issue 1
Serine is the molecular source of the NH(CH 2 ) 2 bridgehead moiety of the in vitro assembled [FeFe] hydrogenase H-cluster
journal, January 2020
- Rao, Guodong; Tao, Lizhi; Britt, R. David
- Chemical Science, Vol. 11, Issue 5
The binuclear cluster of [FeFe] hydrogenase is formed with sulfur donated by cysteine of an [Fe(Cys)(CO) 2 (CN)] organometallic precursor
journal, September 2019
- Rao, Guodong; Pattenaude, Scott A.; Alwan, Katherine
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 42
A [RuRu] Analogue of an [FeFe]-Hydrogenase Traps the Key Hydride Intermediate of the Catalytic Cycle
journal, March 2018
- Sommer, Constanze; Richers, Casseday P.; Lubitz, Wolfgang
- Angewandte Chemie, Vol. 130, Issue 19
[FeFe]-Hydrogenases: recent developments and future perspectives
journal, January 2018
- Wittkamp, F.; Senger, M.; Stripp, S. T.
- Chemical Communications, Vol. 54, Issue 47
From protein engineering to artificial enzymes – biological and biomimetic approaches towards sustainable hydrogen production
journal, January 2018
- Esmieu, C.; Raleiras, P.; Berggren, G.
- Sustainable Energy & Fuels, Vol. 2, Issue 4
DFT methods applied to answer the question: how accurate is the ligand acidity constant method for estimating the p K a of transition metal hydride complexes MHXL 4 when X is varied?
journal, January 2018
- Unsleber, Jan P.; Neugebauer, Johannes; Morris, Robert H.
- Dalton Transactions, Vol. 47, Issue 8
In Vivo EPR Characterization of Semi-Synthetic [FeFe] Hydrogenases
journal, February 2018
- Mészáros, Lívia S.; Németh, Brigitta; Esmieu, Charlène
- Angewandte Chemie International Edition, Vol. 57, Issue 10
Recent advances in the mechanisms of the hydrogen evolution reaction by non-innocent sulfur-coordinating metal complexes
journal, January 2020
- Drosou, Maria; Kamatsos, Fotios; Mitsopoulou, Christiana A.
- Inorganic Chemistry Frontiers, Vol. 7, Issue 1
A [RuRu] Analogue of an [FeFe]-Hydrogenase Traps the Key Hydride Intermediate of the Catalytic Cycle
journal, March 2018
- Sommer, Constanze; Richers, Casseday P.; Lubitz, Wolfgang
- Angewandte Chemie International Edition, Vol. 57, Issue 19
[FeFe]-Hydrogenases: recent developments and future perspectives
text, January 2018
- Wittkamp, F.; Senger, M.; Stripp, S. T.
- Freie Universität Berlin