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Title: Mechanistic insights into energy conservation by flavin-based electron bifurcation

Abstract

The recently realized biochemical phenomenon of energy conservation through electron bifurcation provides biology with an elegant means to maximize utilization of metabolic energy. The mechanism of coordinated coupling of exergonic and endergonic oxidation-reduction reactions by a single enzyme complex has been elucidated through optical and paramagnetic spectroscopic studies revealing unprecedented features. Pairs of electrons are bifurcated over more than 1 volt of electrochemical potential by generating a low-potential, highly energetic, unstable flavin semiquinone and directing electron flow to an iron-sulfur cluster with a highly negative potential to overcome the barrier of the endergonic half reaction. As a result, the unprecedented range of thermodynamic driving force that is generated by flavin-based electron bifurcation accounts for unique chemical reactions that are catalyzed by these enzymes.

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [4];  [4];  [3];  [3];  [4];  [2]; ORCiD logo [5]; ORCiD logo [1];  [3];  [6]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  2. Arizona State Univ., Tempe, AZ (United States)
  3. Univ. of Georgia, Athens, GA (United States)
  4. Montana State Univ., Bozeman, MT (United States)
  5. Univ. of Kentucky, Lexington, KY (United States)
  6. Montana State Univ., Bozeman, MT (United States); Washington State Univ., Pullman, WA (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1358334
Report Number(s):
NREL/JA-2700-67530
Journal ID: ISSN 1552-4450
Grant/Contract Number:
AC36-08GO28308
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Chemical Biology
Additional Journal Information:
Journal Volume: 13; Journal Issue: 6; Journal ID: ISSN 1552-4450
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; structural analysis; spectroscopy; electron bifurcation; flavoenzymes

Citation Formats

Lubner, Carolyn E., Jennings, David P., Mulder, David W., Schut, Gerrit J., Zadvornyy, Oleg A., Hoben, John P., Tokmina-Lukaszewska, Monika, Berry, Luke, Nguyen, Diep M., Lipscomb, Gina L., Bothner, Brian, Jones, Anne K., Miller, Anne-Frances, King, Paul W., Adams, Michael W. W., and Peters, John W. Mechanistic insights into energy conservation by flavin-based electron bifurcation. United States: N. p., 2017. Web. doi:10.1038/nchembio.2348.
Lubner, Carolyn E., Jennings, David P., Mulder, David W., Schut, Gerrit J., Zadvornyy, Oleg A., Hoben, John P., Tokmina-Lukaszewska, Monika, Berry, Luke, Nguyen, Diep M., Lipscomb, Gina L., Bothner, Brian, Jones, Anne K., Miller, Anne-Frances, King, Paul W., Adams, Michael W. W., & Peters, John W. Mechanistic insights into energy conservation by flavin-based electron bifurcation. United States. doi:10.1038/nchembio.2348.
Lubner, Carolyn E., Jennings, David P., Mulder, David W., Schut, Gerrit J., Zadvornyy, Oleg A., Hoben, John P., Tokmina-Lukaszewska, Monika, Berry, Luke, Nguyen, Diep M., Lipscomb, Gina L., Bothner, Brian, Jones, Anne K., Miller, Anne-Frances, King, Paul W., Adams, Michael W. W., and Peters, John W. Mon . "Mechanistic insights into energy conservation by flavin-based electron bifurcation". United States. doi:10.1038/nchembio.2348. https://www.osti.gov/servlets/purl/1358334.
@article{osti_1358334,
title = {Mechanistic insights into energy conservation by flavin-based electron bifurcation},
author = {Lubner, Carolyn E. and Jennings, David P. and Mulder, David W. and Schut, Gerrit J. and Zadvornyy, Oleg A. and Hoben, John P. and Tokmina-Lukaszewska, Monika and Berry, Luke and Nguyen, Diep M. and Lipscomb, Gina L. and Bothner, Brian and Jones, Anne K. and Miller, Anne-Frances and King, Paul W. and Adams, Michael W. W. and Peters, John W.},
abstractNote = {The recently realized biochemical phenomenon of energy conservation through electron bifurcation provides biology with an elegant means to maximize utilization of metabolic energy. The mechanism of coordinated coupling of exergonic and endergonic oxidation-reduction reactions by a single enzyme complex has been elucidated through optical and paramagnetic spectroscopic studies revealing unprecedented features. Pairs of electrons are bifurcated over more than 1 volt of electrochemical potential by generating a low-potential, highly energetic, unstable flavin semiquinone and directing electron flow to an iron-sulfur cluster with a highly negative potential to overcome the barrier of the endergonic half reaction. As a result, the unprecedented range of thermodynamic driving force that is generated by flavin-based electron bifurcation accounts for unique chemical reactions that are catalyzed by these enzymes.},
doi = {10.1038/nchembio.2348},
journal = {Nature Chemical Biology},
number = 6,
volume = 13,
place = {United States},
year = {Mon Apr 10 00:00:00 EDT 2017},
month = {Mon Apr 10 00:00:00 EDT 2017}
}

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Free Publicly Available Full Text
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Cited by: 14works
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  • A newly-recognized third fundamental mechanism of energy conservation in biology, electron bifurcation, uses free energy from exergonic redox reactions to drive endergonic redox reactions. Flavin-based electron bifurcation furnishes low potential electrons to demanding chemical reactions such as reduction of dinitrogen to ammonia. We employed the heterodimeric flavoenzyme FixAB from the diazotrophic bacterium Rhodopseudomonas palustris to elucidate unique properties that underpin flavin-based electron bifurcation.
  • Flavin-based electron transfer bifurcation is emerging as a fundamental and powerful mechanism for conservation and deployment of electrochemical energy in enzymatic systems. In this process, a pair of electrons is acquired at intermediate reduction potential (i.e. intermediate reducing power) and each electron is passed to a different acceptor, one with lower and the other with higher reducing power, leading to 'bifurcation'. It is believed that a strongly reducing semiquinone species is essential for this process, and it is expected that this species should be kinetically short-lived. We now demonstrate that presence of a short-lived anionic flavin semiquinone (ASQ) is notmore » sufficient to infer existence of bifurcating activity, although such a species may be necessary for the process. We have used transient absorption spectroscopy to compare the rates and mechanisms of decay of ASQ generated photochemically in bifurcating NADH-dependent ferredoxin-NADP + oxidoreductase and the non-bifurcating flavoproteins nitroreductase, NADH oxidase and flavodoxin. We found that different mechanisms dominate ASQ decay in the different protein environments, producing lifetimes ranging over two orders of magnitude. Capacity for electron transfer among redox cofactors vs. charge recombination with nearby donors can explain the range of ASQ lifetimes we observe. In conclusion, our results support a model wherein efficient electron propagation can explain the short lifetime of the ASQ of bifurcating NADH-dependent ferredoxin-NADP + oxidoreductase I, and can be an indication of capacity for electron bifurcation.« less
  • Microbial life has evolved a wide range of metabolisms exploiting in many cases unanticipated suites of oxidation-reduction reactions to generate energy. Although many of these suites of reactions don't allow these microbes to enjoy the same quality of energetic life that we enjoy via respiration/oxidative phosphorylation, it has conferred the ability for life to exploit almost any oxidation-reduction reaction. We find in many of these cases when energy is sparing, the difference between life and death may be conserving the maximal amount of energy and minimizing loss of free energy through heat.