Activation Thermodynamics and H/D Kinetic Isotope Effect of the Hox to Hred H+ Transition in [FeFe] Hydrogenase

Ratzloff, Michael W.; Wilker, Molly B.; Mulder, David W.; Lubner, Carolyn E.; Hamby, Hayden; Brown, Katherine A.; Dukovic, Gordana; King, Paul W.

doi:10.1021/jacs.7b04216

Title: Activation Thermodynamics and H/D Kinetic Isotope Effect of the H_ox to H_red H⁺ Transition in [FeFe] Hydrogenase

Journal Article · 29 August 2017 · Journal of the American Chemical Society

DOI: https://doi.org/10.1021/jacs.7b04216 · OSTI ID:1394746

Ratzloff, Michael W. ^[1]; Wilker, Molly B. ^[2]; Mulder, David W. ^[1];

^[1]; Hamby, Hayden ^[2]; Brown, Katherine A. ^[1];

^[2];

^[1]

National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
Univ. of Colorado, Boulder, CO (United States). Dept. of Chemistry and Biochemistry

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. Overall these results support electron injection from CdSe into CaI involving F-clusters, and that the H_ox→H_redH⁺ step of catalytic proton reduction in CaI proceeds by a proton-dependent process.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC36-08GO28308; SC0010334

OSTI ID:: 1394746

Report Number(s):: NREL/JA--2700-68424

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 37 Vol. 139; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (32)

Identification and Characterization of the “Super-Reduced” State of the H-Cluster in [FeFe] Hydrogenase: A New Building Block for the Catalytic Cycle? Adamska, Agnieszka; Silakov, Alexey; Lambertz, Camilla Angewandte Chemie International Edition, Vol. 51, Issue 46 https://doi.org/10.1002/anie.201204800	journal	October 2012
Isotopic fractionation associated with [NiFe]- and [FeFe]-hydrogenases: Isotopic fractionation associated with [NiFe]- and [FeFe]-hydrogenases Yang, Hui; Gandhi, Hasand; Cornish, Adam J. Rapid Communications in Mass Spectrometry, Vol. 30, Issue 2 https://doi.org/10.1002/rcm.7432	journal	December 2015
The active site of the [FeFe]-hydrogenase from Desulfovibrio desulfuricans. II. Redox properties, light sensitivity and CO-ligand exchange as observed by infrared spectroscopy Roseboom, Winfried; De Lacey, Antonio L.; Fernandez, Victor M. JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 1 https://doi.org/10.1007/s00775-005-0040-2	journal	December 2005
Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center Nicolet, Yvain; Piras, Claudine; Legrand, Pierre Structure, Vol. 7, Issue 1, p. 13-23 https://doi.org/10.1016/S0969-2126(99)80005-7	journal	January 1999
Molecular dynamics study of the proposed proton transport pathways in [FeFe]-hydrogenase Ginovska-Pangovska, Bojana; Ho, Ming-Hsun; Linehan, John C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 1 https://doi.org/10.1016/j.bbabio.2013.08.004	journal	January 2014
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
Photocatalytic Regeneration of Nicotinamide Cofactors by Quantum Dot–Enzyme Biohybrid Complexes Brown, Katherine A.; Wilker, Molly B.; Boehm, Marko ACS Catalysis, Vol. 6, Issue 4 https://doi.org/10.1021/acscatal.5b02850	journal	February 2016
Pre-Steady-State Kinetics of Catalytic Intermediates of an [FeFe]-Hydrogenase Greene, Brandon L.; Schut, Gerrit J.; Adams, Michael W. W. ACS Catalysis, Vol. 7, Issue 3 https://doi.org/10.1021/acscatal.6b03276	journal	February 2017
Theory of Proton-Coupled Electron Transfer in Energy Conversion Processes Hammes-Schiffer, Sharon Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar9001284	journal	December 2009
Hybrid [FeFe]-Hydrogenases with Modified Active Sites Show Remarkable Residual Enzymatic Activity Siebel, Judith F.; Adamska-Venkatesh, Agnieszka; Weber, Katharina Biochemistry, Vol. 54, Issue 7 https://doi.org/10.1021/bi501391d	journal	February 2015
Spectroelectrochemical Characterization of the Active Site of the [FeFe] Hydrogenase HydA1 from Chlamydomonas reinhardtii Silakov, Alexey; Kamp, Christina; Reijerse, Eduard Biochemistry, Vol. 48, Issue 33 https://doi.org/10.1021/bi9009105	journal	August 2009
Reversible Carbon Monoxide Binding and Inhibition at the Active Site of the Fe-Only Hydrogenase ^† Bennett, Brian; Lemon, Brian J.; Peters, John W. Biochemistry, Vol. 39, Issue 25 https://doi.org/10.1021/bi992583z	journal	June 2000
Crystallographic and FTIR Spectroscopic Evidence of Changes in Fe Coordination Upon Reduction of the Active Site of the Fe-Only Hydrogenase from Desulfovibrio d esulfuricans Nicolet, Yvain; de Lacey, Antonio L.; Vernède, Xavier Journal of the American Chemical Society, Vol. 123, Issue 8, p. 1596-1601 https://doi.org/10.1021/ja0020963	journal	February 2001
Controlled Assembly of Hydrogenase-CdTe Nanocrystal Hybrids for Solar Hydrogen Production Brown, Katherine A.; Dayal, Smita; Ai, Xin Journal of the American Chemical Society, Vol. 132, Issue 28 https://doi.org/10.1021/ja101031r	journal	July 2010
Characterization of Photochemical Processes for H ₂ Production by CdS Nanorod–[FeFe] Hydrogenase Complexes Brown, Katherine A.; Wilker, Molly B.; Boehm, Marko Journal of the American Chemical Society, Vol. 134, Issue 12 https://doi.org/10.1021/ja2116348	journal	March 2012
EPR and FTIR Analysis of the Mechanism of H ₂ Activation by [FeFe]-Hydrogenase HydA1 from Chlamydomonas reinhardtii Mulder, David W.; Ratzloff, Michael W.; Shepard, Eric M. Journal of the American Chemical Society, Vol. 135, Issue 18 https://doi.org/10.1021/ja4000257	journal	April 2013
Electron Transfer Kinetics in CdS Nanorod–[FeFe]-Hydrogenase Complexes and Implications for Photochemical H ₂ Generation Wilker, Molly B.; Shinopoulos, Katherine E.; Brown, Katherine A. Journal of the American Chemical Society, Vol. 136, Issue 11 https://doi.org/10.1021/ja413001p	journal	March 2014
Investigations on the Role of Proton-Coupled Electron Transfer in Hydrogen Activation by [FeFe]-Hydrogenase Mulder, David W.; Ratzloff, Michael W.; Bruschi, Maurizio Journal of the American Chemical Society, Vol. 136, Issue 43 https://doi.org/10.1021/ja508629m	journal	October 2014
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
Ultrafast Photoinduced Interfacial Proton Coupled Electron Transfer from CdSe Quantum Dots to 4,4′-Bipyridine Chen, Jinquan; Wu, Kaifeng; Rudshteyn, Benjamin Journal of the American Chemical Society, Vol. 138, Issue 3 https://doi.org/10.1021/jacs.5b10354	journal	January 2016
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
Proton Coupled Electronic Rearrangement within the H-Cluster as an Essential Step in the Catalytic Cycle of [FeFe] Hydrogenases Sommer, Constanze; Adamska-Venkatesh, Agnieszka; Pawlak, Krzysztof Journal of the American Chemical Society, Vol. 139, Issue 4 https://doi.org/10.1021/jacs.6b12636	journal	January 2017
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
Proton Transport in Clostridium pasteurianum [FeFe] Hydrogenase I: A Computational Study Long, Hai; King, Paul W.; Chang, Christopher H. The Journal of Physical Chemistry B, Vol. 118, Issue 4 https://doi.org/10.1021/jp408621r	journal	January 2014
Diameter Dependent Electron Transfer Kinetics in Semiconductor–Enzyme Complexes Brown, Katherine A.; Song, Qing; Mulder, David W. ACS Nano, Vol. 8, Issue 10 https://doi.org/10.1021/nn504561v	journal	October 2014
Biomimetic assembly and activation of [FeFe]-hydrogenases Berggren, G.; Adamska, A.; Lambertz, C. Nature, Vol. 499, Issue 7456 https://doi.org/10.1038/nature12239	journal	June 2013
Competition between electron transfer, trapping, and recombination in CdS nanorod–hydrogenase complexes Utterback, James K.; Wilker, Molly B.; Brown, Katherine A. Physical Chemistry Chemical Physics, Vol. 17, Issue 8 https://doi.org/10.1039/C4CP05993J	journal	January 2015
Vibrational spectroscopy reveals the initial steps of biological hydrogen evolution Katz, S.; Noth, J.; Horch, M. Chemical Science, Vol. 7, Issue 11 https://doi.org/10.1039/C6SC01098A	journal	January 2016
Electrocatalytic mechanism of reversible hydrogen cycling by enzymes and distinctions between the major classes of hydrogenases Hexter, S. V.; Grey, F.; Happe, T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 29 https://doi.org/10.1073/pnas.1204770109	journal	July 2012
Frequency and potential dependence of reversible electrocatalytic hydrogen interconversion by [FeFe]-hydrogenases Pandey, Kavita; Islam, Shams T. A.; Happe, Thomas Proceedings of the National Academy of Sciences, Vol. 114, Issue 15 https://doi.org/10.1073/pnas.1619961114	journal	March 2017
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Peters, J. W. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1853	journal	December 1998
Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid Brown, K. A.; Harris, D. F.; Wilker, M. B. Science, Vol. 352, Issue 6284 https://doi.org/10.1126/science.aaf2091	journal	April 2016

Cited By (1)

Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis Brown, Katherine A.; King, Paul W. Photosynthesis Research, Vol. 143, Issue 2 https://doi.org/10.1007/s11120-019-00670-5	journal	October 2019

Similar Records

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

Journal Article · 2018 · Journal of the American Chemical Society · OSTI ID:1440310

Ratzloff, Michael W.; Artz, Jacob H.; Mulder, David W.; +3 more

The Contribution of Proton-Donor pKa on Reactivity Profiles of [FeFe]-hydrogenases

Journal Article · 2022 · Frontiers in Microbiology · OSTI ID:1890512

Kisgeropoulos, Effie C.; Bharadwaj, Vivek S.; Mulder, David W.; +1 more

Pre-Steady-State Kinetics of Catalytic Intermediates of an [FeFe]-Hydrogenase

Journal Article · 2017 · ACS Catalysis · OSTI ID:1469905

Greene, Brandon L.; Schut, Gerrit J.; Adams, Michael W. W.; +1 more

Related Subjects

09 BIOMASS FUELS
H2 catalysis
hydrogenase
thermodynamics

Title: Activation Thermodynamics and H/D Kinetic Isotope Effect of the Hox to Hred H+ Transition in [FeFe] Hydrogenase

Citation Formats

References (32)

Cited By (1)

Similar Records

Related Subjects

Title: Activation Thermodynamics and H/D Kinetic Isotope Effect of the H_ox to H_red H⁺ Transition in [FeFe] Hydrogenase