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

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 analysesmore » 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.« less

Authors:
 [1];  [1];  [1]; ORCiD logo [1];  [2]
  1. Univ. of Wisconsin, Madison, WI (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
  2. Univ. of Washington, Seattle, WA (United States)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626102
Grant/Contract Number:  
FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology

Citation Formats

Spero, Melanie A., Aylward, Frank O., Currie, Cameron R., Donohue, Timothy J., and Harwood, Caroline S. Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria. United States: N. p., 2015. Web. doi:10.1128/mbio.00389-15.
Spero, Melanie A., Aylward, Frank O., Currie, Cameron R., Donohue, Timothy J., & Harwood, Caroline S. Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria. United States. https://doi.org/10.1128/mbio.00389-15
Spero, Melanie A., Aylward, Frank O., Currie, Cameron R., Donohue, Timothy J., and Harwood, Caroline S. Tue . "Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria". United States. https://doi.org/10.1128/mbio.00389-15. https://www.osti.gov/servlets/purl/1626102.
@article{osti_1626102,
title = {Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria},
author = {Spero, Melanie A. and Aylward, Frank O. and Currie, Cameron R. and Donohue, Timothy J. and Harwood, Caroline S.},
abstractNote = {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.},
doi = {10.1128/mbio.00389-15},
journal = {mBio (Online)},
number = 2,
volume = 6,
place = {United States},
year = {Tue Apr 14 00:00:00 EDT 2015},
month = {Tue Apr 14 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

FIG 1 FIG 1: The distribution of complex I across bacteria. The distribution of predicted complex I enzymes in sequenced bacterial genomes. (A) The number of bacterial genomes predicted to encode 0, 1, or 2 complex I enzymes, organized by phylum or class. The x axis phylogeny was modeled using data frommore » Ciccarelli et al. (77). (B) The percentage of bacterial genomes predicted to encode 0, 1, or 2 complex I enzymes, organized by trait. An asterisk (*) indicates that the distribution of complex I (0, 1, or 2 or more enzymes) for a specific trait is significantly different from the distribution of complex I in all bacteria (fist bar) at P values of < 0.0005 (chi-square test). “N/A” indicates there were not enough genomes in the category to perform the statistical analysis.« less

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Roles of Staphylococcus aureus Mnh1 and Mnh2 Antiporters in Salt Tolerance, Alkali Tolerance, and Pathogenesis
journal, March 2018

  • Vaish, Manisha; Price-Whelan, Alexa; Reyes-Robles, Tamara
  • Journal of Bacteriology, Vol. 200, Issue 5
  • DOI: 10.1128/jb.00611-17

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.