The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5
Abstract
Here, the first generation of biochemical studies of complex, iron-sulfur-cluster-containing [FeFe]-hydrogenases and Mo-nitrogenase were carried out on enzymes purified from Clostridium pasteurianum (strain W5). Previous studies suggested that two distinct [FeFe]-hydrogenases are expressed differentially under nitrogen-fixing and non-nitrogen-fixing conditions. As a result, the first characterized [FeFe]-hydrogenase (CpI) is presumed to have a primary role in central metabolism, recycling reduced electron carriers that accumulate during fermentation via proton reduction. A role for capturing reducing equivalents released as hydrogen during nitrogen fixation has been proposed for the second hydrogenase, CpII. Biochemical characterization of CpI and CpII indicated CpI has extremely high hydrogen production activity in comparison to CpII, while CpII has elevated hydrogen oxidation activity in comparison to CpI when assayed under the same conditions. This suggests that these enzymes have evolved a catalytic bias to support their respective physiological functions. Using the published genome of C. pasteurianum (strain W5) hydrogenase sequences were identified, including the already known [NiFe]-hydrogenase, CpI, and CpII sequences, and a third hydrogenase, CpIII was identified in the genome as well. Quantitative real-time PCR experiments were performed in order to analyze transcript abundance of the hydrogenases under diazotrophic and non-diazotrophic growth conditions. There is a markedly reduced levelmore »
- Authors:
-
- Montana State Univ., Bozeman, MT (United States)
- Montana State Univ., Bozeman, MT (United States); Washington State Univ., Pullman, WA (United States)
- Montana State Univ., Bozeman, MT (United States); Univ. of Cincinnati, Cincinnati, OH (United States)
- The Pennsylvania State Univ., University Park, PA (United States); Univ. of Southern California, Los Angeles, CA (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Univ. of Georgia, Athens, GA (United States)
- Montana State Univ., Bozeman, MT (United States); The Pennsylvania State Univ., University Park, PA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1371832
- Report Number(s):
- NREL/JA-2700-68736
Journal ID: ISSN 1664-302X
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; hydrogenase; nitrogenase Clostridium pasteurianum; hydrogen metabolism; nitrogen metabolism; CpI; CpII
Citation Formats
Therien, Jesse B., Artz, Jacob H., Poudel, Saroj, Hamilton, Trinity L., Liu, Zhenfeng, Noone, Seth M., Adams, Michael W. W., King, Paul W., Bryant, Donald A., Boyd, Eric S., and Peters, John W. The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5. United States: N. p., 2017.
Web. doi:10.3389/fmicb.2017.01305.
Therien, Jesse B., Artz, Jacob H., Poudel, Saroj, Hamilton, Trinity L., Liu, Zhenfeng, Noone, Seth M., Adams, Michael W. W., King, Paul W., Bryant, Donald A., Boyd, Eric S., & Peters, John W. The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5. United States. https://doi.org/10.3389/fmicb.2017.01305
Therien, Jesse B., Artz, Jacob H., Poudel, Saroj, Hamilton, Trinity L., Liu, Zhenfeng, Noone, Seth M., Adams, Michael W. W., King, Paul W., Bryant, Donald A., Boyd, Eric S., and Peters, John W. Wed .
"The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5". United States. https://doi.org/10.3389/fmicb.2017.01305. https://www.osti.gov/servlets/purl/1371832.
@article{osti_1371832,
title = {The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5},
author = {Therien, Jesse B. and Artz, Jacob H. and Poudel, Saroj and Hamilton, Trinity L. and Liu, Zhenfeng and Noone, Seth M. and Adams, Michael W. W. and King, Paul W. and Bryant, Donald A. and Boyd, Eric S. and Peters, John W.},
abstractNote = {Here, the first generation of biochemical studies of complex, iron-sulfur-cluster-containing [FeFe]-hydrogenases and Mo-nitrogenase were carried out on enzymes purified from Clostridium pasteurianum (strain W5). Previous studies suggested that two distinct [FeFe]-hydrogenases are expressed differentially under nitrogen-fixing and non-nitrogen-fixing conditions. As a result, the first characterized [FeFe]-hydrogenase (CpI) is presumed to have a primary role in central metabolism, recycling reduced electron carriers that accumulate during fermentation via proton reduction. A role for capturing reducing equivalents released as hydrogen during nitrogen fixation has been proposed for the second hydrogenase, CpII. Biochemical characterization of CpI and CpII indicated CpI has extremely high hydrogen production activity in comparison to CpII, while CpII has elevated hydrogen oxidation activity in comparison to CpI when assayed under the same conditions. This suggests that these enzymes have evolved a catalytic bias to support their respective physiological functions. Using the published genome of C. pasteurianum (strain W5) hydrogenase sequences were identified, including the already known [NiFe]-hydrogenase, CpI, and CpII sequences, and a third hydrogenase, CpIII was identified in the genome as well. Quantitative real-time PCR experiments were performed in order to analyze transcript abundance of the hydrogenases under diazotrophic and non-diazotrophic growth conditions. There is a markedly reduced level of CpI gene expression together with concomitant increases in CpII gene expression under nitrogen-fixing conditions. Structure-based analyses of the CpI and CpII sequences reveal variations in their catalytic sites that may contribute to their alternative physiological roles. This work demonstrates that the physiological roles of CpI and CpII are to evolve and to consume hydrogen, respectively, in concurrence with their catalytic activities in vitro, with CpII capturing excess reducing equivalents under nitrogen fixation conditions. Comparison of the primary sequences of CpI and CpII and their homologs provides an initial basis for identifying key structural determinants that modulate hydrogen production and hydrogen oxidation activities.},
doi = {10.3389/fmicb.2017.01305},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Wed Jul 12 00:00:00 EDT 2017},
month = {Wed Jul 12 00:00:00 EDT 2017}
}
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