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

Abstract

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 for each cluster were determined. The data suggest a large degree of magnetic coupling between the clusters. The distal [4Fe-4S] cluster is shown to have a lower reduction potential (~ < -450 mV) than the other clusters, and molecular docking experiments indicate that the physiological electron donor, ferredoxin (Fd), most favorably interacts with this cluster. The low reduction potential of the distal [4Fe-4S] cluster thermodynamically restricts the Fdox/Fdred ratio at which CpI can operate, consistent with the role of CpI in recycling Fdredthat accumulates during fermentation. In conclusion, subsequent electron transfer through the additional accessory [FeS] clusters to the H-cluster ismore » thermodynamically favorable.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2];  [1];  [3];  [4];  [5];  [4]; ORCiD logo [2];  [1]
+ Show Author Affiliations
  1. Washington State Univ., Pullman, WA (United States)
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  3. Montana State Univ., Bozeman, MT (United States)
  4. Arizona State Univ., Tempe, AZ (United States)
  5. The Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1374131
Report Number(s):
NREL/JA-2700-68072
Journal ID: ISSN 0002-7863; TRN: US1702343
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: 28; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; [FeFe]-hydrogenase; Clostridium pasteurianum; iron sulfur clusters; electron paramagnetic resonance; potentiometric titrations; spectral deconvolution; electron-transfer; catalysis

Citation Formats

Artz, Jacob H., Mulder, David W., Ratzloff, Michael W., Lubner, Carolyn E., Zadvornyy, Oleg A., LeVan, Axl X., Williams, S. Garrett, Adams, Michael W. W., Jones, Anne K., King, Paul W., and Peters, John W. Reduction Potentials of [FeFe]-Hydrogenase Accessory Iron–Sulfur Clusters Provide Insights into the Energetics of Proton Reduction Catalysis. United States: N. p., 2017. Web. doi:10.1021/jacs.7b02099.
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Artz, Jacob H., Mulder, David W., Ratzloff, Michael W., Lubner, Carolyn E., Zadvornyy, Oleg A., LeVan, Axl X., Williams, S. Garrett, Adams, Michael W. W., Jones, Anne K., King, Paul W., & Peters, John W. Reduction Potentials of [FeFe]-Hydrogenase Accessory Iron–Sulfur Clusters Provide Insights into the Energetics of Proton Reduction Catalysis. United States. https://doi.org/10.1021/jacs.7b02099
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Artz, Jacob H., Mulder, David W., Ratzloff, Michael W., Lubner, Carolyn E., Zadvornyy, Oleg A., LeVan, Axl X., Williams, S. Garrett, Adams, Michael W. W., Jones, Anne K., King, Paul W., and Peters, John W. Wed . "Reduction Potentials of [FeFe]-Hydrogenase Accessory Iron–Sulfur Clusters Provide Insights into the Energetics of Proton Reduction Catalysis". United States. https://doi.org/10.1021/jacs.7b02099. https://www.osti.gov/servlets/purl/1374131.
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@article{osti_1374131,
title = {Reduction Potentials of [FeFe]-Hydrogenase Accessory Iron–Sulfur Clusters Provide Insights into the Energetics of Proton Reduction Catalysis},
author = {Artz, Jacob H. and Mulder, David W. and Ratzloff, Michael W. and Lubner, Carolyn E. and Zadvornyy, Oleg A. and LeVan, Axl X. and Williams, S. Garrett and Adams, Michael W. W. and Jones, Anne K. and King, Paul W. and Peters, John W.},
abstractNote = {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 for each cluster were determined. The data suggest a large degree of magnetic coupling between the clusters. The distal [4Fe-4S] cluster is shown to have a lower reduction potential (~ < -450 mV) than the other clusters, and molecular docking experiments indicate that the physiological electron donor, ferredoxin (Fd), most favorably interacts with this cluster. The low reduction potential of the distal [4Fe-4S] cluster thermodynamically restricts the Fdox/Fdred ratio at which CpI can operate, consistent with the role of CpI in recycling Fdredthat accumulates during fermentation. In conclusion, subsequent electron transfer through the additional accessory [FeS] clusters to the H-cluster is thermodynamically favorable.},
doi = {10.1021/jacs.7b02099},
journal = {Journal of the American Chemical Society},
number = 28,
volume = 139,
place = {United States},
year = {Wed Jun 21 00:00:00 EDT 2017},
month = {Wed Jun 21 00:00:00 EDT 2017}
}
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https://doi.org/10.1021/jacs.7b02099
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