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Title: Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases

Abstract

Hydrogenases display a wide range of catalytic rates and biases in reversible hydrogen gas oxidation catalysis. The interactions of the iron-sulfur containing catalytic site with the local protein environment are thought to contribute to differences in reactivity but this has not been demonstrated. The microbe Clostridium pasteurianum produces three [FeFe]-hydrogenases that differ in their “catalytic bias” exerting a disproportionate rate acceleration in one direction or the other spanning a remarkable 7-orders of magnitude. The combination of high-resolution structural work, biochemical analyses, and computational modeling demonstrate the catalytic bias can be explained through a simple yet elegant model involving the relative stabilization and destabilization of different states of the catalytic active site metal cluster through protein secondary interactions allowing it to operate under different reduction-oxidation regimes.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [5];  [3]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [7];  [5];  [5]; ORCiD logo [5];  [5]; ORCiD logo [2];  [8]; ORCiD logo [6];  [5]; ORCiD logo [8]; ORCiD logo [9]; ORCiD logo [3] more »; ORCiD logo [10] « less
  1. Washington State Univ., Pullman, WA (United States); National Renewable Energy Lab. (NREL), Golden, CO (United States)
  2. Washington State Univ., Pullman, WA (United States)
  3. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  4. Montana State Univ., Bozeman, MT (United States)
  5. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  6. Arizona State Univ., Tempe, AZ (United States)
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  8. Univ. of Georgia, Athens, GA (United States)
  9. Washington State Univ., Pullman, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  10. Washington State Univ., Pullman, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Biological Electron Transfer and Catalysis (BETCy). Center for Molecular Electrocatalysis (CME); National Renewable Energy Lab. (NREL), Golden, CO (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1593682
Alternate Identifier(s):
OSTI ID: 1597671; OSTI ID: 1633991
Report Number(s):
NREL/JA-2700-74582; PNNL-SA-140081
Journal ID: ISSN 0002-7863
Grant/Contract Number:  
AC36-08GO28308; AC05-76RL01830; AC02-76SF00515; SC0012518; P41GM103393
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 142; Journal Issue: 3; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
08 HYDROGEN; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; hydrogenases; catalytic bias; hydrogen

Citation Formats

Artz, Jacob H., Zadvornyy, Oleg A., Mulder, David W., Keable, Stephen M., Cohen, Aina E., Ratzloff, Michael W., Williams, S. Garrett, Ginovska, Bojana, Kumar, Neeraj, Song, Jinhu, McPhillips, Scott E., Davidson, Catherine M., Lyubimov, Artem Y., Pence, Natasha, Schut, Gerrit J., Jones, Anne K., Soltis, S. Michael, Adams, Michael W. W., Raugei, Simone, King, Paul W., and Peters, John W. Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases. United States: N. p., 2019. Web. https://doi.org/10.1021/jacs.9b08756.
Artz, Jacob H., Zadvornyy, Oleg A., Mulder, David W., Keable, Stephen M., Cohen, Aina E., Ratzloff, Michael W., Williams, S. Garrett, Ginovska, Bojana, Kumar, Neeraj, Song, Jinhu, McPhillips, Scott E., Davidson, Catherine M., Lyubimov, Artem Y., Pence, Natasha, Schut, Gerrit J., Jones, Anne K., Soltis, S. Michael, Adams, Michael W. W., Raugei, Simone, King, Paul W., & Peters, John W. Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases. United States. https://doi.org/10.1021/jacs.9b08756
Artz, Jacob H., Zadvornyy, Oleg A., Mulder, David W., Keable, Stephen M., Cohen, Aina E., Ratzloff, Michael W., Williams, S. Garrett, Ginovska, Bojana, Kumar, Neeraj, Song, Jinhu, McPhillips, Scott E., Davidson, Catherine M., Lyubimov, Artem Y., Pence, Natasha, Schut, Gerrit J., Jones, Anne K., Soltis, S. Michael, Adams, Michael W. W., Raugei, Simone, King, Paul W., and Peters, John W. Mon . "Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases". United States. https://doi.org/10.1021/jacs.9b08756. https://www.osti.gov/servlets/purl/1593682.
@article{osti_1593682,
title = {Tuning Catalytic Bias of Hydrogen Gas Producing Hydrogenases},
author = {Artz, Jacob H. and Zadvornyy, Oleg A. and Mulder, David W. and Keable, Stephen M. and Cohen, Aina E. and Ratzloff, Michael W. and Williams, S. Garrett and Ginovska, Bojana and Kumar, Neeraj and Song, Jinhu and McPhillips, Scott E. and Davidson, Catherine M. and Lyubimov, Artem Y. and Pence, Natasha and Schut, Gerrit J. and Jones, Anne K. and Soltis, S. Michael and Adams, Michael W. W. and Raugei, Simone and King, Paul W. and Peters, John W.},
abstractNote = {Hydrogenases display a wide range of catalytic rates and biases in reversible hydrogen gas oxidation catalysis. The interactions of the iron-sulfur containing catalytic site with the local protein environment are thought to contribute to differences in reactivity but this has not been demonstrated. The microbe Clostridium pasteurianum produces three [FeFe]-hydrogenases that differ in their “catalytic bias” exerting a disproportionate rate acceleration in one direction or the other spanning a remarkable 7-orders of magnitude. The combination of high-resolution structural work, biochemical analyses, and computational modeling demonstrate the catalytic bias can be explained through a simple yet elegant model involving the relative stabilization and destabilization of different states of the catalytic active site metal cluster through protein secondary interactions allowing it to operate under different reduction-oxidation regimes.},
doi = {10.1021/jacs.9b08756},
journal = {Journal of the American Chemical Society},
number = 3,
volume = 142,
place = {United States},
year = {2019},
month = {12}
}

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