CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI

Ratzloff, Michael W.; Artz, Jacob H.; Mulder, David W.; Collins, Reuben T.; Furtak, Thomas E.; King, Paul W.

doi:10.1021/jacs.8b03072

Title: CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI

Abstract

The [FeFe]-hydrogenases ([FeFe] H₂ases) catalyze reversible H₂ activation at the H-cluster, which is composed of a [4Fe-4S]_H subsite linked by a cysteine thiolate to a bridged, organometallic [2Fe-2S] ([2Fe]_H) subsite. Profoundly different geometric models of the H-cluster redox states that orchestrate the electron/proton transfer steps of H₂ bond activation have been proposed. We have examined this question in the [FeFe] H₂ase I from Clostridium acetobutylicum (CaI) by Fourier-transform infrared (FTIR) spectroscopy with temperature annealing and H/D isotope exchange to identify the relevant redox states and define catalytic transitions. One-electron reduction of H_ox led to formation of H_redH⁺ ([4Fe-4S]_H²⁺-Fe^I-Fe^I) and H_red' ([4Fe-4S]_H¹⁺-Fe^II-Fe^I), with both states characterized by low frequency μ-CO IR modes consistent with a fully bridged [2Fe]_H. Similar μ-CO IR modes were also identified for H_redH⁺ of the [FeFe] H₂ase from Chlamydomonas reinhardtii (CrHydA1). The CaI proton-transfer variant C298S showed enrichment of an H/D isotope-sensitive μ-CO mode, a component of the hydride bound H-cluster IR signal, H_hyd. Equilibrating CaI with increasing amounts of NaDT, and probed at cryogenic temperatures, showed H_redH⁺ was converted to H_hyd. Over an increasing temperature range from 10 to 260 K catalytic turnover led to loss of Hhyd and appearance of H_ox, consistent with enzymatic turnovermore »« less

Authors:

Ratzloff, Michael W. ^[1]; Artz, Jacob H. ^[1]; Mulder, David W. ^[1]; Collins, Reuben T. ^[2]; Furtak, Thomas E. ^[2];

^[1]

National Renewable Energy Lab. (NREL), Golden, CO (United States)
Colorado School of Mines, Golden, CO (United States)

Publication Date:: 2018-05-23

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

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

OSTI Identifier:: 1440310

Report Number(s):: NREL/JA-2700-71170
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: 140; Journal Issue: 24; 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; [FeFe]-hydrogenases; catalysis; catalytic transitions

Citation Formats


                    Ratzloff, Michael W., Artz, Jacob H., Mulder, David W., Collins, Reuben T., Furtak, Thomas E., and King, Paul W. CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI.  United States: N. p., 2018. 
Web.  doi:10.1021/jacs.8b03072.

Copy to clipboard


                    Ratzloff, Michael W., Artz, Jacob H., Mulder, David W., Collins, Reuben T., Furtak, Thomas E., & King, Paul W. CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI.  United States.  https://doi.org/10.1021/jacs.8b03072

Copy to clipboard


                    Ratzloff, Michael W., Artz, Jacob H., Mulder, David W., Collins, Reuben T., Furtak, Thomas E., and King, Paul W. Wed .  
"CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI".  United States.  https://doi.org/10.1021/jacs.8b03072.  https://www.osti.gov/servlets/purl/1440310.

Copy to clipboard


                    
@article{osti_1440310,

  title        = {CO-Bridged H-Cluster Intermediates in the Catalytic Mechanism of [FeFe]-Hydrogenase CaI},

  author       = {Ratzloff, Michael W. and Artz, Jacob H. and Mulder, David W. and Collins, Reuben T. and Furtak, Thomas E. and King, Paul W.},

  abstractNote = {The [FeFe]-hydrogenases ([FeFe] H2ases) catalyze reversible H2 activation at the H-cluster, which is composed of a [4Fe-4S]H subsite linked by a cysteine thiolate to a bridged, organometallic [2Fe-2S] ([2Fe]H) subsite. Profoundly different geometric models of the H-cluster redox states that orchestrate the electron/proton transfer steps of H2 bond activation have been proposed. We have examined this question in the [FeFe] H2ase I from Clostridium acetobutylicum (CaI) by Fourier-transform infrared (FTIR) spectroscopy with temperature annealing and H/D isotope exchange to identify the relevant redox states and define catalytic transitions. One-electron reduction of Hox led to formation of HredH+ ([4Fe-4S]H2+-FeI-FeI) and Hred' ([4Fe-4S]H1+-FeII-FeI), with both states characterized by low frequency μ-CO IR modes consistent with a fully bridged [2Fe]H. Similar μ-CO IR modes were also identified for HredH+ of the [FeFe] H2ase from Chlamydomonas reinhardtii (CrHydA1). The CaI proton-transfer variant C298S showed enrichment of an H/D isotope-sensitive μ-CO mode, a component of the hydride bound H-cluster IR signal, Hhyd. Equilibrating CaI with increasing amounts of NaDT, and probed at cryogenic temperatures, showed HredH+ was converted to Hhyd. Over an increasing temperature range from 10 to 260 K catalytic turnover led to loss of Hhyd and appearance of Hox, consistent with enzymatic turnover and H2 formation. The results show for CaI that the μ-CO of [2Fe]H remains bridging for all of the 'Hred' states and that HredH+ is on pathway to Hhyd and H2 evolution in the catalytic mechanism. Here, this provides a blueprint for designing small molecule catalytic analogs},

  doi          = {10.1021/jacs.8b03072},

  journal      = {Journal of the American Chemical Society},

  number       = 24,

  volume       = 140,

  place        = {United States},

  year         = {2018},

  month        = {5}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1021/jacs.8b03072

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 13 works

Citation information provided by
Web of Science

Figures / Tables:

Figure 1: Top. Structural representation of Clostridium acetobu-tylicum [FeFe] H₂ase I (CaI) showing the convergence of electron (e^-) and proton (H⁺) transfer pathways. The F-cluster (green) and H-cluster (blue) domains are based on the crystal structure of Clostridium pasteurianum [FeFe] H₂ase I (CpI), PDB 3C8Y.²⁴ Bottom. Models of the H-clustermore »

All figures and tables (7 total)

Save / Share:

Export Metadata

Save to My Library

Figures / Tables found in this record:

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

Similar Records in DOE PAGES and OSTI.GOV collections:

Identification of a catalytic iron-hydride at the H-cluster of [FeFe]-hydrogenase

Journal Article Mulder, David W. ; Guo, Yisong ; Ratzloff, Michael W. ; ... - Journal of the American Chemical Society

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 (H_hyd) 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 H_hyd consists of a reduced [4Fe-4S]_H⁺ coupled to a diferrous [2Fe]_H with a terminally bound Fe-hydride. The existence ofmore »« less
Cited by 28
https://doi.org/10.1021/jacs.6b11409

Full Text Available
Reduction Potentials of [FeFe]-Hydrogenase Accessory Iron–Sulfur Clusters Provide Insights into the Energetics of Proton Reduction Catalysis

Journal Article Artz, Jacob H. ; Mulder, David W. ; Ratzloff, Michael W. ; ... - Journal of the American Chemical Society

An [FeFe]-hydrogenase from Clostridium pasteurianum, CpI, is a model system for biological H₂ activation. In addition to the catalytic H-cluster, CpI contains four accessory iron-sulfur [FeS] clusters in a branched series that transfer electrons to and from the active site. In this work, potentiometric titrations have been employed in combination with electron paramagnetic resonance (EPR) spectroscopy at defined electrochemical potentials to gain insights into the role of the accessory clusters in catalysis. EPR spectra collected over a range of potentials were deconvoluted into individual components attributable to the accessory [FeS] clusters and the active site H-cluster, and reduction potentials formore »« less
Cited by 7
https://doi.org/10.1021/jacs.7b02099

Full Text Available
Cysteine as a ligand platform in the biosynthesis of the FeFe hydrogenase H cluster

Journal Article Suess, Daniel L. M. ; Bürstel, Ingmar ; De La Paz, Liliana ; ... - Proceedings of the National Academy of Sciences of the United States of America

Hydrogenases catalyze the redox interconversion of protons and H₂, an important reaction for a number of metabolic processes and for solar fuel production. In FeFe hydrogenases, catalysis occurs at the H cluster, a metallocofactor comprising a [4Fe–4S]_H subcluster coupled to a [2Fe]_H subcluster bound by CO, CN–, and azadithiolate ligands. The [2Fe]_H subcluster is assembled by the maturases HydE, HydF, and HydG. HydG is a member of the radical S-adenosyl-L-methionine family of enzymes that transforms Fe and L-tyrosine into an [Fe(CO)₂(CN)] synthon that is incorporated into the H cluster. Though it is thought that the site of synthon formation inmore »« less
Cited by 12
https://doi.org/10.1073/pnas.1508440112
Electron Spin Relaxation and Biochemical Characterization of the Hydrogenase Maturase HydF: Insights into [2Fe-2S] and [4Fe-4S] Cluster Communication and Hydrogenase Activation

Journal Article Shepard, Eric M. ; Byer, Amanda S. ; Aggarwal, Priyanka ; ... - Biochemistry

Nature utilizes [FeFe]-hydrogenase enzymes to catalyze the interconversion between H₂ and protons and electrons. Catalysis occurs at the H-cluster, a carbon monoxide-, cyanide-, and dithiomethylamine-coordinated 2Fe subcluster bridged via a cysteine to a [4Fe-4S] cluster. Biosynthesis of this unique metallocofactor is accomplished by three maturase enzymes denoted HydE, HydF, and HydG. HydE and HydG belong to the radical S-adenosylmethionine superfamily of enzymes and synthesize the nonprotein ligands of the H-cluster. These enzymes interact with HydF, a GTPase that acts as a scaffold or carrier protein during 2Fe subcluster assembly. Prior characterization of HydF demonstrated the protein exists in both dimericmore »« less
Cited by 9
https://doi.org/10.1021/acs.biochem.7b00169
Activation Thermodynamics and H/D Kinetic Isotope Effect of the H_ox to H_red H⁺ Transition in [FeFe] Hydrogenase

Journal Article Ratzloff, Michael W. ; Wilker, Molly B. ; Mulder, David W. ; ... - Journal of the American Chemical Society

Molecular complexes between CdSe nanocrystals and Clostridium acetobutylicum [FeFe] hydrogenase I (CaI) enabled light-driven control of electron transfer for spectroscopic detection of redox intermediates during catalytic proton reduction. Here in this paper we address the route of electron transfer from CdSe→CaI and activation thermodynamics of the initial step of proton reduction in CaI. The electron paramagnetic spectroscopy of illuminated CdSe:CaI showed how the CaI accessory FeS cluster chain (F-clusters) functions in electron transfer with CdSe. The H_ox→H_redH⁺ reduction step measured by Fourier-transform infrared spectroscopy showed an enthalpy of activation of 19 kJ mol^-1 and a ~2.5-fold kinetic isotope effect. Overallmore »« less
Cited by 3
https://doi.org/10.1021/jacs.7b04216

Full Text Available

Similar Records