Metal–ligand cooperativity in the soluble hydrogenase-1 from Pyrococcus furiosus

Vansuch, Gregory E.; Wu, Chang-Hao; Haja, Dominik K.; Blair, Soshawn A.; Chica, Bryant; Johnson, Michael K.; Adams, Michael W. W.; Dyer, R. Brian

doi:10.1039/D0SC00628A

Title: Metal–ligand cooperativity in the soluble hydrogenase-1 from Pyrococcus furiosus

Journal Article · Wed Aug 19 00:00:00 EDT 2020 · Chemical Science

DOI:https://doi.org/10.1039/D0SC00628A· OSTI ID:1646533

Vansuch, Gregory E. ^[1]; Wu, Chang-Hao ^[2]; Haja, Dominik K. ^[3]; Blair, Soshawn A. ^[4]; Chica, Bryant ^[5]; Johnson, Michael K. ^[4]; Adams, Michael W. W. ^[6];

^[1]

Department of Chemistry, Emory University, Atlanta, USA
Department of Biochemistry & Molecular Biology, University of Georgia, Athens, USA, AskGene Pharma Inc.
Department of Biochemistry & Molecular Biology, University of Georgia, Athens, USA
Department of Chemistry, University of Georgia, Athens, USA
Department of Chemistry, Emory University, Atlanta, USA, Biosciences Center
Department of Biochemistry & Molecular Biology, University of Georgia, Athens, USA, Department of Chemistry

Metal–ligand cooperativity is an essential feature of bioinorganic catalysis. The design principles of such cooperativity in metalloenzymes are underexplored, but are critical to understand for developing efficient catalysts designed with earth abundant metals for small molecule activation. The simple substrate requirements of reversible proton reduction by the [NiFe]-hydrogenases make them a model bioinorganic system. A highly conserved arginine residue (R355) directly above the exogenous ligand binding position of the [NiFe]-catalytic core is known to be essential for optimal function because mutation to a lysine results in lower catalytic rates. To expand on our studies of soluble hydrogenase-1 from Pyrococcus furiosus (Pf SH1), we investigated the role of R355 by site-directed-mutagenesis to a lysine (R355K) using infrared and electron paramagnetic resonance spectroscopic probes sensitive to active site redox and protonation events. It was found the mutation resulted in an altered ligand binding environment at the [NiFe] centre. A key observation was destabilization of the Ni_a³⁺–C state, which contains a bridging hydride. Instead, the tautomeric Ni_a⁺–L states were observed. Overall, the results provided insight into complex metal–ligand cooperativity between the active site and protein scaffold that modulates the bridging hydride stability and the proton inventory, which should prove valuable to design principles for efficient bioinspired catalysts.

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Research Organization:: National Renewable Energy Lab. (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG05-95ER20175; AC36-08GO28308

OSTI ID:: 1646533

Alternate ID(s):: OSTI ID: 1665873

Report Number(s):: NREL/JA-2700-77926; CSHCBM

Journal Information:: Chemical Science, Journal Name: Chemical Science Vol. 11 Journal Issue: 32; ISSN 2041-6520

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 5 works

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References (69)

Spectroscopic and kinetic characterization of active site mutants of Desulfovibrio fructosovorans Ni-Fe hydrogenase De Lacey, Antonio L.; Fernandez, Victor M.; Rousset, Marc JBIC Journal of Biological Inorganic Chemistry, Vol. 8, Issue 1 https://doi.org/10.1007/s00775-002-0397-4	journal	January 2003
Great Metalloclusters in Enzymology Rees, Douglas C. Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135406	journal	June 2002
Infrared Spectroscopy During Electrocatalytic Turnover Reveals the Ni-L Active Site State During H ₂ Oxidation by a NiFe Hydrogenase Hidalgo, Ricardo; Ash, Philip A.; Healy, Adam J. Angewandte Chemie International Edition, Vol. 54, Issue 24 https://doi.org/10.1002/anie.201502338	journal	April 2015
A Glutamate Is the Essential Proton Transfer Gate during the Catalytic Cycle of the [NiFe] Hydrogenase Dementin, Sébastien; Burlat, Bénédicte; De Lacey, Antonio L. Journal of Biological Chemistry, Vol. 279, Issue 11 https://doi.org/10.1074/jbc.M312716200	journal	December 2003
Accumulating the hydride state in the catalytic cycle of [FeFe]-hydrogenases Winkler, Martin; Senger, Moritz; Duan, Jifu Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms16115	journal	July 2017
Natural inspirations for metal–ligand cooperative catalysis Wodrich, Matthew D.; Hu, Xile Nature Reviews Chemistry, Vol. 2, Issue 1 https://doi.org/10.1038/s41570-017-0099	journal	December 2017
Mechanism of hydrogen activation by [NiFe] hydrogenases Evans, Rhiannon M.; Brooke, Emily J.; Wehlin, Sara A. M. Nature Chemical Biology, Vol. 12, Issue 1 https://doi.org/10.1038/nchembio.1976	journal	November 2015
Metalloenzymes: the entatic nature of their active sites. Vallee, B. L.; Williams, R. J. Proceedings of the National Academy of Sciences, Vol. 59, Issue 2 https://doi.org/10.1073/pnas.59.2.498	journal	February 1968
Reinvestigation of the Steady-State Kinetics and Physiological Function of the Soluble NiFe-Hydrogenase I of Pyrococcus furiosus van Haaster, D. J.; Silva, P. J.; Hagedoorn, P. -L. Journal of Bacteriology, Vol. 190, Issue 5 https://doi.org/10.1128/JB.01562-07	journal	December 2007
Nickel L-Edge Soft X-ray Spectroscopy of Nickel−Iron Hydrogenases and Model CompoundsEvidence for High-Spin Nickel(II) in the Active Enzyme Wang, Hongxin; Ralston, C. Y.; Patil, D. S. Journal of the American Chemical Society, Vol. 122, Issue 43 https://doi.org/10.1021/ja000945g	journal	November 2000
Anion control of tautomeric equilibria: Fe–H vs. N–H influenced by NH⋯F hydrogen bonding Chambers, Geoffrey M.; Johnson, Samantha I.; Raugei, Simone Chemical Science, Vol. 10, Issue 5 https://doi.org/10.1039/C8SC04239J	journal	January 2019
Proton Inventory and Dynamics in the Ni _a -S to Ni _a -C Transition of a [NiFe] Hydrogenase Greene, Brandon L.; Wu, Chang-Hao; Vansuch, Gregory E. Biochemistry, Vol. 55, Issue 12 https://doi.org/10.1021/acs.biochem.5b01348	journal	March 2016
Importance of the Active Site “Canopy” Residues in an O ₂ -Tolerant [NiFe]-Hydrogenase Brooke, Emily J.; Evans, Rhiannon M.; Islam, Shams T. A. Biochemistry, Vol. 56, Issue 1 https://doi.org/10.1021/acs.biochem.6b00868	journal	December 2016
[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
Multiscale Simulations Give Insight into the Hydrogen In and Out Pathways of [NiFe]-Hydrogenases from Aquifex aeolicus and Desulfovibrio fructosovorans Oteri, Francesco; Baaden, Marc; Lojou, Elisabeth The Journal of Physical Chemistry B, Vol. 118, Issue 48 https://doi.org/10.1021/jp5089965	journal	November 2014
Comprehensive reaction mechanisms at and near the Ni–Fe active sites of [NiFe] hydrogenases Tai, Hulin; Higuchi, Yoshiki; Hirota, Shun Dalton Transactions, Vol. 47, Issue 13 https://doi.org/10.1039/C7DT04910B	journal	January 2018
Chicken fat for catalysis: a scaffold is as important for molecular complexes for energy transformations as it is for enzymes in catalytic function Laureanti, Joseph A.; O'Hagan, Molly; Shaw, Wendy J. Sustainable Energy & Fuels, Vol. 3, Issue 12 https://doi.org/10.1039/C9SE00229D	journal	January 2019
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
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
An orientation-selected ENDOR and HYSCORE study of the Ni-C active state of Desulfovibrio vulgaris Miyazaki F hydrogenase Foerster, Stefanie; Gastel, Maurice van; Brecht, Marc JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 1 https://doi.org/10.1007/s00775-004-0613-5	journal	December 2004
Investigating the role of chain and linker length on the catalytic activity of an H ₂ production catalyst containing a β-hairpin peptide Reback, Matthew L.; Ginovska, Bojana; Buchko, Garry W. Journal of Coordination Chemistry, Vol. 69, Issue 11-13 https://doi.org/10.1080/00958972.2016.1188924	journal	June 2016
Glutamate Gated Proton-Coupled Electron Transfer Activity of a [NiFe]-Hydrogenase Greene, Brandon L.; Vansuch, Gregory E.; Wu, Chang-Hao Journal of the American Chemical Society, Vol. 138, Issue 39 https://doi.org/10.1021/jacs.6b07789	journal	September 2016
Spectroelectrochemical Characterization of the [NiFe] Hydrogenase of Desulfovibrio vulgaris Miyazaki F ^† Fichtner, Caroline; Laurich, Christoph; Bothe, Eberhard Biochemistry, Vol. 45, Issue 32 https://doi.org/10.1021/bi0602462	journal	August 2006
Spectroscopic characterization of the key catalytic intermediate Ni–C in the O ₂ -tolerant [NiFe] hydrogenase I from Aquifex aeolicus: evidence of a weakly bound hydride Pandelia, Maria-Eirini; Infossi, Pascale; Stein, Matthias Chem. Commun., Vol. 48, Issue 6 https://doi.org/10.1039/C1CC16109A	journal	January 2012
The bio-organometallic chemistry of active site iron in hydrogenases Darensbourg, Marcetta Y.; Lyon, Erica J.; Smee, Jason J. Coordination Chemistry Reviews, Vol. 206-207 https://doi.org/10.1016/S0010-8545(00)00268-X	journal	September 2000
Computational study of the electronic structure and magnetic properties of the Ni–C state in [NiFe] hydrogenases including the second coordination sphere Kampa, Mario; Lubitz, Wolfgang; van Gastel, Maurice JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 8 https://doi.org/10.1007/s00775-012-0941-9	journal	October 2012
Reversibility and efficiency in electrocatalytic energy conversion and lessons from enzymes Armstrong, F. A.; Hirst, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1103697108	journal	August 2011
QM/MM Investigation of the Role of a Second Coordination Shell Arginine in [NiFe]-Hydrogenases Escorcia, Andrés M.; Stein, Matthias Frontiers in Chemistry, Vol. 6 https://doi.org/10.3389/fchem.2018.00164	journal	May 2018
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
Enzymatic and spectroscopic properties of a thermostable [NiFe]‑hydrogenase performing H2-driven NAD+-reduction in the presence of O2 Preissler, Janina; Wahlefeld, Stefan; Lorent, Christian Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 1 https://doi.org/10.1016/j.bbabio.2017.09.006	journal	January 2018
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
Cysteine SH and Glutamate COOH Contributions to [NiFe] Hydrogenase Proton Transfer Revealed by Highly Sensitive FTIR Spectroscopy Tai, Hulin; Nishikawa, Koji; Higuchi, Yoshiki Angewandte Chemie, Vol. 131, Issue 38 https://doi.org/10.1002/ange.201904472	journal	August 2019
Direct Detection of a Hydrogen Ligand in the [NiFe] Center of the Regulatory H ₂ -Sensing Hydrogenase from Ralstonia e utropha in Its Reduced State by HYSCORE and ENDOR Spectroscopy Brecht, Marc; van Gastel, Maurice; Buhrke, Thorsten Journal of the American Chemical Society, Vol. 125, Issue 43 https://doi.org/10.1021/ja036624x	journal	October 2003
Shedding Light on Proton and Electron Dynamics in [FeFe] Hydrogenases Lorent, Christian; Katz, Sagie; Duan, Jifu Journal of the American Chemical Society, Vol. 142, Issue 12 https://doi.org/10.1021/jacs.9b13075	journal	March 2020
Infrared Studies on the Interaction of Carbon Monoxide with Divalent Nickel in Hydrogenase from Chromatium vinosum Bagley, Kimberly A.; Van Garderen, Carla J.; Chen, Min Biochemistry, Vol. 33, Issue 31 https://doi.org/10.1021/bi00197a026	journal	August 1994
A Threonine Stabilizes the NiC and NiR Catalytic Intermediates of [NiFe]-hydrogenase Abou-Hamdan, Abbas; Ceccaldi, Pierre; Lebrette, Hugo Journal of Biological Chemistry, Vol. 290, Issue 13 https://doi.org/10.1074/jbc.M114.630491	journal	February 2015
Hydrogen production from pyruvate by enzymes purified from the hyperthermophilic archaeon, Pyrococcus furiosus : A key role for NADPH Ma, Kesen; Hao, Zhi; Adams, Michael W.W. FEMS Microbiology Letters, Vol. 122, Issue 3, p. 245-250 https://doi.org/10.1111/j.1574-6968.1994.tb07175.x	journal	October 1994
Kinetic Evidence for Intramolecular Proton Transfer Between Nickel and Coordinated Thiolate Clegg, William Inorganic Chemistry, Vol. 41, Issue 5 https://doi.org/10.1021/ic0104306	journal	March 2002
The plasticity of redox cofactors: from metalloenzymes to redox-active DNA Hemschemeier, Anja; Happe, Thomas Nature Reviews Chemistry, Vol. 2, Issue 9 https://doi.org/10.1038/s41570-018-0029-3	journal	August 2018
Testing the Push–Pull Hypothesis: Lewis Acid Augmented N ₂ Activation at Iron Geri, Jacob B.; Shanahan, James P.; Szymczak, Nathaniel K. Journal of the American Chemical Society, Vol. 139, Issue 16 https://doi.org/10.1021/jacs.7b01982	journal	April 2017
Analyses of the Large Subunit Histidine-Rich Motif Expose an Alternative Proton Transfer Pathway in [NiFe] Hydrogenases Szőri-Dorogházi, Emma; Maróti, Gergely; Szőri, Milán PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0034666	journal	April 2012
Hydrogenases in the "active" state: determination of g-matrix axes and electron spin distribution at the active site by 1H ENDOR spectroscopy Müller, Arnd; Tscherny, Irene; Kappl, Reinhard JBIC Journal of Biological Inorganic Chemistry, Vol. 7, Issue 1-2 https://doi.org/10.1007/s007750100285	journal	September 2001
Proton Transfer in the Catalytic Cycle of [NiFe] Hydrogenases: Insight from Vibrational Spectroscopy Ash, Philip A.; Hidalgo, Ricardo; Vincent, Kylie A. ACS Catalysis, Vol. 7, Issue 4 https://doi.org/10.1021/acscatal.6b03182	journal	March 2017
Modulation of active site electronic structure by the protein matrix to control [NiFe] hydrogenase reactivity Smith, Dayle M. A.; Raugei, Simone; Squier, Thomas C. Phys. Chem. Chem. Phys., Vol. 16, Issue 43 https://doi.org/10.1039/C4CP03518F	journal	January 2014
Spectroscopic Insights into the Oxygen-tolerant Membrane-associated [NiFe] Hydrogenase of Ralstonia eutropha H16 Saggu, Miguel; Zebger, Ingo; Ludwig, Marcus Journal of Biological Chemistry, Vol. 284, Issue 24 https://doi.org/10.1074/jbc.M805690200	journal	March 2009
[NiFe] hydrogenases: A common active site for hydrogen metabolism under diverse conditions Shafaat, Hannah S.; Rüdiger, Olaf; Ogata, Hideaki Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2013.01.015	journal	August 2013
A Metal–Metal Bond in the Light-Induced State of [NiFe] Hydrogenases with Relevance to Hydrogen Evolution Kampa, Mario; Pandelia, Maria-Eirini; Lubitz, Wolfgang Journal of the American Chemical Society, Vol. 135, Issue 10 https://doi.org/10.1021/ja3115899	journal	February 2013
Density functional study of the catalytic cycle of nickel–iron [NiFe] hydrogenases and the involvement of high-spin nickel(II) Pardo, Alejandro; De Lacey, Antonio L.; Fernández, Víctor M. JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 3 https://doi.org/10.1007/s00775-005-0076-3	journal	March 2006
On the prosthetic groups of the NiFe sulfhydrogenase from Pyrococcus furiosus: topology, structure, and temperature-dependent redox chemistry Silva, Pedro J.; de Castro, Baltazar; Hagen, W. R. JBIC Journal of Biological Inorganic Chemistry, Vol. 4, Issue 3 https://doi.org/10.1007/s007750050314	journal	July 1999
Proton-Coupled Electron Transfer Dynamics in the Catalytic Mechanism of a [NiFe]-Hydrogenase Greene, Brandon L.; Wu, Chang-Hao; McTernan, Patrick M. Journal of the American Chemical Society, Vol. 137, Issue 13 https://doi.org/10.1021/jacs.5b01791	journal	March 2015
504. The stereochemistry of the bridged quaternary salts of 2,2′-bipyridyl Homer, R. F.; Tomlinson, T. E. J. Chem. Soc., Vol. 0, Issue 0 https://doi.org/10.1039/JR9600002498	journal	January 1960
Monovalent nickel in hydrogenase from Chromatium vinosum: Light sensitivity and evidence for direct interaction with hydrogen van der Zwaan, J. W.; Albracht, S. P. J.; Fontijn, R. D. FEBS Letters, Vol. 179, Issue 2 https://doi.org/10.1016/0014-5793(85)80533-0	journal	January 1985
Mechanistic Exploitation of a Self-Repairing, Blocked Proton Transfer Pathway in an O ₂ -Tolerant [NiFe]-Hydrogenase Evans, Rhiannon M.; Ash, Philip A.; Beaton, Stephen E. Journal of the American Chemical Society, Vol. 140, Issue 32 https://doi.org/10.1021/jacs.8b04798	journal	July 2018
An x-ray absorption spectroscopic study of nickel redox chemistry in hydrogenase Bagyinka, Csaba; Whitehead, Joyce P.; Maroney, Michael J. Journal of the American Chemical Society, Vol. 115, Issue 9 https://doi.org/10.1021/ja00062a022	journal	May 1993
The activation of the [NiFe]-hydrogenase from Allochromatium vinosum. An infrared spectro-electrochemical study Bleijlevens, Boris; van Broekhuizen, Fleur A.; De Lacey, Antonio L. JBIC Journal of Biological Inorganic Chemistry, Vol. 9, Issue 6 https://doi.org/10.1007/s00775-004-0570-z	journal	July 2004
X‐ray Crystallography and Vibrational Spectroscopy Reveal the Key Determinants of Biocatalytic Dihydrogen Cycling by [NiFe] Hydrogenases Ilina, Yulia; Lorent, Christian; Katz, Sagie Angewandte Chemie International Edition, Vol. 58, Issue 51 https://doi.org/10.1002/anie.201908258	journal	October 2019
Hydrogen bonding effect between active site and protein environment on catalysis performance in H ₂ -producing [NiFe] hydrogenases Qiu, Siyao; Azofra, Luis Miguel; MacFarlane, Douglas R. Physical Chemistry Chemical Physics, Vol. 20, Issue 9 https://doi.org/10.1039/C7CP07685A	journal	January 2018
IR spectroelectrochemical study of the binding of carbon monoxide to the active site of Desulfovibrio fructosovorans Ni-Fe hydrogenase De Lacey, Antonio L.; Stadler, Christian; Fernandez, Victor M. JBIC Journal of Biological Inorganic Chemistry, Vol. 7, Issue 3 https://doi.org/10.1007/s00775-001-0301-7	journal	March 2002
Structure/Function Relationships of [NiFe]- and [FeFe]-Hydrogenases Fontecilla-Camps, Juan C.; Volbeda, Anne; Cavazza, Christine Chemical Reviews, Vol. 107, Issue 10 https://doi.org/10.1021/cr050195z	journal	October 2007
Positional effects of second-sphere amide pendants on electrochemical CO ₂ reduction catalyzed by iron porphyrins Nichols, Eva M.; Derrick, Jeffrey S.; Nistanaki, Sepand K. Chemical Science, Vol. 9, Issue 11 https://doi.org/10.1039/C7SC04682K	journal	January 2018
New assay method based on Raman spectroscopy for enzymes reacting with gaseous substrates: H/D exchange reaction of H2ase by Raman method Kawahara-Nakagawa, Yuka; Nishikawa, Koji; Nakashima, Satoru Protein Science, Vol. 28, Issue 3 https://doi.org/10.1002/pro.3569	journal	January 2019
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
Structural Studies of the Carbon Monoxide Complex of [NiFe]hydrogenase from Desulfovibrio vulgaris Miyazaki F: Suggestion for the Initial Activation Site for Dihydrogen Ogata, Hideaki; Mizoguchi, Yasutaka; Mizuno, Nobuhiro Journal of the American Chemical Society, Vol. 124, Issue 39 https://doi.org/10.1021/ja012645k	journal	October 2002
Cytochrome oxidase (a3) heme and copper observed by low-temperature Fourier transform infrared spectroscopy of the CO complex. Alben, J. O.; Moh, P. P.; Fiamingo, F. G. Proceedings of the National Academy of Sciences, Vol. 78, Issue 1 https://doi.org/10.1073/pnas.78.1.234	journal	January 1981
How Can a Single Second Sphere Amino Acid Substitution Cause Reduction Midpoint Potential Changes of Hundreds of Millivolts? Yikilmaz, Emine; Porta, Jason; Grove, Laurie E. Journal of the American Chemical Society, Vol. 129, Issue 32 https://doi.org/10.1021/ja069224t	journal	August 2007
How [FeFe]-Hydrogenase Facilitates Bidirectional Proton Transfer Senger, Moritz; Eichmann, Viktor; Laun, Konstantin Journal of the American Chemical Society, Vol. 141, Issue 43 https://doi.org/10.1021/jacs.9b09225	journal	October 2019
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
Protonation mechanisms of Nickel Complexes Relevant to Industrial and Biological Catalysis Henderson, Richard A. Journal of Chemical Research, Vol. 2002, Issue 9 https://doi.org/10.3184/030823402103172554	journal	September 2002
Synthetic Models for the Active Site of the [FeFe]-Hydrogenase: Catalytic Proton Reduction and the Structure of the Doubly Protonated Intermediate Carroll, Maria E.; Barton, Bryan E.; Rauchfuss, Thomas B. Journal of the American Chemical Society, Vol. 134, Issue 45 https://doi.org/10.1021/ja309216v	journal	November 2012