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Title: Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds

Abstract

Nitrogenase catalyzes the reduction of dinitrogen (N2) using low-potential electrons from ferredoxin (Fd) or flavodoxin (Fld) through an ATP-dependent process. Since its emergence in an anaerobic chemoautotroph, this oxygen (O2)-sensitive enzyme complex has evolved to operate in a variety of genomic and metabolic backgrounds, including those of aerobes, anaerobes, chemotrophs, and phototrophs. However, whether pathways of electron delivery to nitrogenase are influenced by these different metabolic backgrounds is not well understood. Here, we report the distribution of homologs of Fds, Flds, and Fd-/Fld-reducing enzymes in 359 genomes of putative N2 fixers (diazotrophs). Six distinct lineages of nitrogenase were identified, and their distributions largely corresponded to differences in the host cells' ability to integrate O2 or light into energy metabolism. The predicted pathways of electron transfer to nitrogenase in aerobes, facultative anaerobes, and phototrophs varied from those in anaerobes at the levels of Fds/Flds used to reduce nitrogenase, the enzymes that generate reduced Fds/Flds, and the putative substrates of these enzymes. Proteins that putatively reduce Fd with hydrogen or pyruvate were enriched in anaerobes, while those that reduce Fd with NADH/NADPH were enriched in aerobes, facultative anaerobes, and anoxygenic phototrophs. Here, the energy metabolism of aerobic, facultatively anaerobic, and anoxygenic phototrophicmore » diazotrophs often yields reduced NADH/NADPH that is not sufficiently reduced to drive N2 reduction. At least two mechanisms have been acquired by these taxa to overcome this limitation and to generate electrons with potentials capable of reducing Fd. These include the bifurcation of electrons or the coupling of Fd reduction to reverse ion translocation.« less

Authors:
 [1];  [1]; ORCiD logo [2];  [3];  [4];  [5];  [3];  [5]; ORCiD logo [4]; ORCiD logo [1];  [6]
+ Show Author Affiliations
  1. Montana State Univ., Bozeman, MT (United States)
  2. Univ. of Minnesota, St. Paul, MN (United States)
  3. Utah State Univ., Logan, UT (United States)
  4. Univ. of Washington, Seattle, WA (United States)
  5. Washington State Univ., Pullman, WA (United States)
  6. Univ. of Illinois at Urbana Champaign, Urbana, IL (United States)
Publication Date:
Research Org.:
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:
1470211
Grant/Contract Number:  
SC0012518
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 200; Journal Issue: 10; Related Information: BETCy partners with Montana State University (lead); Arizona State University; National Renewable Energy Laboratory; University of Georgia; University of Kentucky; University of Washington; Utah State University; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; solar (fuels); biofuels (including algae and biomass); bio-inspired; hydrogen and fuel cells

Citation Formats

Poudel, Saroj, Colman, Daniel R., Fixen, Kathryn R., Ledbetter, Rhesa N., Zheng, Yanning, Pence, Natasha, Seefeldt, Lance C., Peters, John W., Harwood, Caroline S., Boyd, Eric S., and Metcalf, William W. Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds. United States: N. p., 2018. Web. doi:10.1128/JB.00757-17.
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Poudel, Saroj, Colman, Daniel R., Fixen, Kathryn R., Ledbetter, Rhesa N., Zheng, Yanning, Pence, Natasha, Seefeldt, Lance C., Peters, John W., Harwood, Caroline S., Boyd, Eric S., & Metcalf, William W. Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds. United States. https://doi.org/10.1128/JB.00757-17
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Poudel, Saroj, Colman, Daniel R., Fixen, Kathryn R., Ledbetter, Rhesa N., Zheng, Yanning, Pence, Natasha, Seefeldt, Lance C., Peters, John W., Harwood, Caroline S., Boyd, Eric S., and Metcalf, William W. Mon . "Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds". United States. https://doi.org/10.1128/JB.00757-17. https://www.osti.gov/servlets/purl/1470211.
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@article{osti_1470211,
title = {Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds},
author = {Poudel, Saroj and Colman, Daniel R. and Fixen, Kathryn R. and Ledbetter, Rhesa N. and Zheng, Yanning and Pence, Natasha and Seefeldt, Lance C. and Peters, John W. and Harwood, Caroline S. and Boyd, Eric S. and Metcalf, William W.},
abstractNote = {Nitrogenase catalyzes the reduction of dinitrogen (N2) using low-potential electrons from ferredoxin (Fd) or flavodoxin (Fld) through an ATP-dependent process. Since its emergence in an anaerobic chemoautotroph, this oxygen (O2)-sensitive enzyme complex has evolved to operate in a variety of genomic and metabolic backgrounds, including those of aerobes, anaerobes, chemotrophs, and phototrophs. However, whether pathways of electron delivery to nitrogenase are influenced by these different metabolic backgrounds is not well understood. Here, we report the distribution of homologs of Fds, Flds, and Fd-/Fld-reducing enzymes in 359 genomes of putative N2 fixers (diazotrophs). Six distinct lineages of nitrogenase were identified, and their distributions largely corresponded to differences in the host cells' ability to integrate O2 or light into energy metabolism. The predicted pathways of electron transfer to nitrogenase in aerobes, facultative anaerobes, and phototrophs varied from those in anaerobes at the levels of Fds/Flds used to reduce nitrogenase, the enzymes that generate reduced Fds/Flds, and the putative substrates of these enzymes. Proteins that putatively reduce Fd with hydrogen or pyruvate were enriched in anaerobes, while those that reduce Fd with NADH/NADPH were enriched in aerobes, facultative anaerobes, and anoxygenic phototrophs. Here, the energy metabolism of aerobic, facultatively anaerobic, and anoxygenic phototrophic diazotrophs often yields reduced NADH/NADPH that is not sufficiently reduced to drive N2 reduction. At least two mechanisms have been acquired by these taxa to overcome this limitation and to generate electrons with potentials capable of reducing Fd. These include the bifurcation of electrons or the coupling of Fd reduction to reverse ion translocation.},
doi = {10.1128/JB.00757-17},
journal = {Journal of Bacteriology},
number = 10,
volume = 200,
place = {United States},
year = {Mon Feb 26 00:00:00 EST 2018},
month = {Mon Feb 26 00:00:00 EST 2018}
}
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