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Title: The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis

Abstract

The biological reduction of dinitrogen (N2) to ammonia (NH3) by nitrogenase is an energetically demanding reaction that requires low-potential electrons and ATP; however, pathways used to deliver the electrons from central metabolism to the reductants of nitrogenase, ferredoxin or flavodoxin, remain unknown for many diazotrophic microbes. The FixABCX protein complex has been proposed to reduce flavodoxin or ferredoxin using NADH as the electron donor in a process known as electron bifurcation. Herein, the FixABCX complex from Azotobacter vinelandii was purified and demonstrated to catalyze an electron bifurcation reaction: oxidation of NADH (Em = -320 mV) coupled to reduction of flavodoxin semiquinone (Em = -460 mV) and reduction of coenzyme Q (Em = 10 mV). Knocking out fix genes rendered ..delta..rnf A. vinelandii cells unable to fix dinitrogen, confirming that the FixABCX system provides another route for delivery of electrons to nitrogenase. Characterization of the purified FixABCX complex revealed the presence of flavin and iron-sulfur cofactors confirmed by native mass spectrometry, electron paramagnetic resonance spectroscopy, and transient absorption spectroscopy. Transient absorption spectroscopy further established the presence of a short-lived flavin semiquinone radical, suggesting that a thermodynamically unstable flavin semiquinone may participate as an intermediate in the transfer of an electron tomore » flavodoxin. A structural model of FixABCX, generated using chemical cross-linking in conjunction with homology modeling, revealed plausible electron transfer pathways to both high- and low-potential acceptors. Altogether, this study informs a mechanism for electron bifurcation, offering insight into a unique method for delivery of low-potential electrons required for energy-intensive biochemical conversions.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [2];  [4];  [2];  [5];  [2];  [6];  [2];  [7];  [6];  [7];  [2]; ORCiD logo [6];  [2]; ORCiD logo [3];  [8]; ORCiD logo [1]
+ Show Author Affiliations
  1. Utah State Univ., Logan, UT (United States)
  2. Montana State Univ., Bozeman, MT (United States)
  3. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  4. Washington State Univ., Pullman, WA (United States)
  5. Idaho State Univ., Pocatello, ID (United States)
  6. Univ. of Kentucky, Lexington, KY (United States)
  7. Univ. of Minnesota, St. Paul, MN (United States)
  8. Montana State Univ., Bozeman, MT (United States); Washington State Univ., Pullman, WA (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:
1376663
Report Number(s):
NREL/JA-2700-68237
Journal ID: ISSN 0006-2960
Grant/Contract Number:  
AC36-08GO28308; SC0012518
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 56; Journal Issue: 32; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; electron paramagnetic resonance; EPR; electron transfer; flavoprotein; nitrogen fixation; oxidation-reduction; redox

Citation Formats

Ledbetter, Rhesa N., Garcia Costas, Amaya M., Lubner, Carolyn E., Mulder, David W., Tokmina-Lukaszewska, Monika, Artz, Jacob H., Patterson, Angela, Magnuson, Timothy S., Jay, Zackary J., Duan, H. Diessel, Miller, Jacquelyn, Plunkett, Mary H., Hoben, John P., Barney, Brett M., Carlson, Ross P., Miller, Anne -Frances, Bothner, Brian, King, Paul W., Peters, John W., and Seefeldt, Lance C. The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis. United States: N. p., 2017. Web. doi:10.1021/acs.biochem.7b00389.
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Ledbetter, Rhesa N., Garcia Costas, Amaya M., Lubner, Carolyn E., Mulder, David W., Tokmina-Lukaszewska, Monika, Artz, Jacob H., Patterson, Angela, Magnuson, Timothy S., Jay, Zackary J., Duan, H. Diessel, Miller, Jacquelyn, Plunkett, Mary H., Hoben, John P., Barney, Brett M., Carlson, Ross P., Miller, Anne -Frances, Bothner, Brian, King, Paul W., Peters, John W., & Seefeldt, Lance C. The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis. United States. https://doi.org/10.1021/acs.biochem.7b00389
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Ledbetter, Rhesa N., Garcia Costas, Amaya M., Lubner, Carolyn E., Mulder, David W., Tokmina-Lukaszewska, Monika, Artz, Jacob H., Patterson, Angela, Magnuson, Timothy S., Jay, Zackary J., Duan, H. Diessel, Miller, Jacquelyn, Plunkett, Mary H., Hoben, John P., Barney, Brett M., Carlson, Ross P., Miller, Anne -Frances, Bothner, Brian, King, Paul W., Peters, John W., and Seefeldt, Lance C. Thu . "The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis". United States. https://doi.org/10.1021/acs.biochem.7b00389. https://www.osti.gov/servlets/purl/1376663.
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@article{osti_1376663,
title = {The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis},
author = {Ledbetter, Rhesa N. and Garcia Costas, Amaya M. and Lubner, Carolyn E. and Mulder, David W. and Tokmina-Lukaszewska, Monika and Artz, Jacob H. and Patterson, Angela and Magnuson, Timothy S. and Jay, Zackary J. and Duan, H. Diessel and Miller, Jacquelyn and Plunkett, Mary H. and Hoben, John P. and Barney, Brett M. and Carlson, Ross P. and Miller, Anne -Frances and Bothner, Brian and King, Paul W. and Peters, John W. and Seefeldt, Lance C.},
abstractNote = {The biological reduction of dinitrogen (N2) to ammonia (NH3) by nitrogenase is an energetically demanding reaction that requires low-potential electrons and ATP; however, pathways used to deliver the electrons from central metabolism to the reductants of nitrogenase, ferredoxin or flavodoxin, remain unknown for many diazotrophic microbes. The FixABCX protein complex has been proposed to reduce flavodoxin or ferredoxin using NADH as the electron donor in a process known as electron bifurcation. Herein, the FixABCX complex from Azotobacter vinelandii was purified and demonstrated to catalyze an electron bifurcation reaction: oxidation of NADH (Em = -320 mV) coupled to reduction of flavodoxin semiquinone (Em = -460 mV) and reduction of coenzyme Q (Em = 10 mV). Knocking out fix genes rendered ..delta..rnf A. vinelandii cells unable to fix dinitrogen, confirming that the FixABCX system provides another route for delivery of electrons to nitrogenase. Characterization of the purified FixABCX complex revealed the presence of flavin and iron-sulfur cofactors confirmed by native mass spectrometry, electron paramagnetic resonance spectroscopy, and transient absorption spectroscopy. Transient absorption spectroscopy further established the presence of a short-lived flavin semiquinone radical, suggesting that a thermodynamically unstable flavin semiquinone may participate as an intermediate in the transfer of an electron to flavodoxin. A structural model of FixABCX, generated using chemical cross-linking in conjunction with homology modeling, revealed plausible electron transfer pathways to both high- and low-potential acceptors. Altogether, this study informs a mechanism for electron bifurcation, offering insight into a unique method for delivery of low-potential electrons required for energy-intensive biochemical conversions.},
doi = {10.1021/acs.biochem.7b00389},
journal = {Biochemistry},
number = 32,
volume = 56,
place = {United States},
year = {Thu Jul 13 00:00:00 EDT 2017},
month = {Thu Jul 13 00:00:00 EDT 2017}
}
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https://doi.org/10.1021/acs.biochem.7b00389
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