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Research Article

Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria

Melanie A. Spero, Frank O. Aylward, Cameron R. Currie, Timothy J. Donohue
Caroline S. Harwood, Editor
Melanie A. Spero
aDepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA
bGreat Lakes Bioenergy Research Center, Madison, Wisconsin, USA
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Frank O. Aylward
aDepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA
bGreat Lakes Bioenergy Research Center, Madison, Wisconsin, USA
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Cameron R. Currie
aDepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA
bGreat Lakes Bioenergy Research Center, Madison, Wisconsin, USA
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Timothy J. Donohue
aDepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA
bGreat Lakes Bioenergy Research Center, Madison, Wisconsin, USA
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  • ORCID record for Timothy J. Donohue
Caroline S. Harwood
University of Washington
Roles: Editor
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DOI: 10.1128/mBio.00389-15
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ABSTRACT

The proton-translocating NADH:quinone oxidoreductase (complex I) is a multisubunit integral membrane enzyme found in the respiratory chains of both bacteria and eukaryotic organelles. Although much research has focused on the enzyme's central role in the mitochondrial respiratory chain, comparatively little is known about its role in the diverse energetic lifestyles of different bacteria. Here, we used a phylogenomic approach to better understand the distribution of complex I across bacteria, the evolution of this enzyme, and its potential roles in shaping the physiology of different bacterial groups. By surveying 970 representative bacterial genomes, we predict complex I to be present in ~50% of bacteria. While this includes bacteria with a wide range of energetic schemes, the presence of complex I is associated with specific lifestyles, including aerobic respiration and specific types of phototrophy (bacteria with only a type II reaction center). A phylogeny of bacterial complex I revealed five main clades of enzymes whose evolution is largely congruent with the evolution of the bacterial groups that encode complex I. A notable exception includes the gammaproteobacteria, whose members encode one of two distantly related complex I enzymes predicted to participate in different types of respiratory chains (aerobic versus anaerobic). Comparative genomic analyses suggest a broad role for complex I in reoxidizing NADH produced from various catabolic reactions, including the tricarboxylic acid (TCA) cycle and fatty acid beta-oxidation. Together, these findings suggest diverse roles for complex I across bacteria and highlight the importance of this enzyme in shaping diverse physiologies across the bacterial domain.

IMPORTANCE Living systems use conserved energy currencies, including a proton motive force (PMF), NADH, and ATP. The respiratory chain enzyme, complex I, connects these energy currencies by using NADH produced during nutrient breakdown to generate a PMF, which is subsequently used for ATP synthesis. Our goal is to better understand the role of complex I in bacteria, whose energetic diversity allows us to view its function in a range of biological contexts. We analyzed sequenced bacterial genomes to predict the presence, evolution, and function of complex I in bacteria. We identified five main classes of bacterial complex I and predict that different classes participate in different types of respiratory chains (aerobic and anaerobic). We also predict that complex I helps maintain a cellular redox state by reoxidizing NADH produced from central metabolism. Our findings suggest diverse roles for complex I in bacterial physiology, highlighting the need for future laboratory-based studies.

FOOTNOTES

    • Received 19 March 2015
    • Accepted 20 March 2015
    • Published 14 April 2015
  • Copyright © 2015 Spero et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria
Melanie A. Spero, Frank O. Aylward, Cameron R. Currie, Timothy J. Donohue
mBio Apr 2015, 6 (2) e00389-15; DOI: 10.1128/mBio.00389-15

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Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria
Melanie A. Spero, Frank O. Aylward, Cameron R. Currie, Timothy J. Donohue
mBio Apr 2015, 6 (2) e00389-15; DOI: 10.1128/mBio.00389-15
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