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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
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DOI: 10.1128/mBio.00389-15
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  • FIG 1 
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    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 from 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.

  • FIG 2 
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    FIG 2 

    Phylogeny of bacterial complex I. A phylogeny of predicted complex I enzymes from 508 sequenced bacterial genomes was generated using amino acid sequences from all 14 concatenated complex I subunits. There are five main clades of bacterial complex I (clades A to E), which can be distinguished by specific subunit features. Genome names and most of the support values were omitted for clarity.

  • FIG 3 
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    FIG 3 

    The extended C terminus of clade A NuoE is poorly conserved. Protein alignment of the first 300 amino acids of the complex I subunit NuoE from clade E E. coli and clade A R. sphaeroides, R. capsulatus, and Agrobacterium tumefaciens. The first ~170 amino acids of NuoE are well conserved between all organisms. Most clade A NuoE subunits have an extended C terminus, which is poorly conserved even between closely related bacteria.

  • FIG 4 
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    FIG 4 

    Inheritance pattern of complex I in specific bacterial groups. A species phylogeny of representative members of Bacteroidetes, Actinobacteria, Deltaproteobacteria, and Gammaproteobacteria was generated using the amino acid sequences of 9 highly conserved housekeeping genes. The absence or presence of complex I (by complex I clade) was mapped onto the phylogeny to show the patchwork inheritance pattern of complex I within specific groups of bacteria. For visualization purposes, Bacillus cereus was used to root the tree, as the Firmicutes phylum represents a distantly related phylum in which no complex I enzymes were identified. Support values were omitted for clarity, but the full phylogeny is available in Fig. S8 in the supplemental material. Abbreviations: C. Amoebophilus asiaticus, “Candidatus Amoebophilus asiaticus”; Blattabacterium sp. B. germ, Blattabacterium sp. Blattella germanica; Anaeromyxo. sp. Fw109-5, Anaeromyxobacter sp. Fw109-5; Syntrophobact. fumaroxidans, Syntrophobacter fumaroxidans; Pseudoxanthomonas s., Pseudoxanthomonas suwonensis; Pseuodoaltero. sp. SM9913, Pseudoalteromonas sp. SM9913; Actinobacillus pleuro., Actinobacillus pleuropneumoniae.

  • FIG 5 
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    FIG 5 

    Biochemical pathways enriched in bacterial genomes that encode complex I. (A) Heat map showing the biochemical pathways (KEGG modules) that are enriched in bacterial genomes predicted to encode complex I compared to members of the same class/phylum that are predicted to lack complex I. We present pathways that show significant enrichment with a P value of <0.01 (see Data Set S2 in the supplemental materials for full results). Pathways are colored according to their level of significance, which was calculated by −log10(P value), so that the most significantly enriched pathways have a higher value on the color key and are darker shades of blue. For visual purposes, the value of the most significant pathway (“NADH:quinone oxidoreductase, prokaryotes” in Actinobacteria) was adjusted from 44 to 25, which still represents the upper limit of the scale, while improving the resolution of other enriched pathways found in the analysis. Pathway names highlighted in pink produce NADH as a byproduct (72). (B) Schematic of biochemical pathways that are enriched across different groups of bacteria predicted to encode complex I. Beta-oxidation produces NADH and acetyl-CoA, the latter of which feeds into the TCA cycle to produce additional NADH. The glyoxylate cycle and ethylmalonyl pathway (not shown) assimilate acetyl-CoA by bypassing the CO2-generating reactions of the TCA cycle.

Tables

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  • Supplemental Material
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  • TABLE 1 

    Genomes predicted to encode two or more complex I isozymes

    Phylum or class (no. of strains)StrainEnzyme clades
    Alphaproteobacteria (18)Acidiphilium cryptum JF-5A, E
    Gluconacetobacter diazotrophicus PAl 5A, E
    Rhizobium etli (2 strains)A, other
    Rhodobacter sphaeroides (4 strains)A, E
    Rhodopseudomonas palustris (7 strains)A, E
    Sinorhizobium fredii NGR234A, other
    Sinorhizobium medicae WSM419A, other
    Sinorhizobium meliloti 1021A, other
    Bacteroidetes (1)Chitinophaga pinensis DSM 2588C, E
    Betaproteobacteria (1)Nitrosospira multiformis ATCC 25196B, E
    Deltaproteobacteria (9)Geobacter bemidjiensis BemE, other
    Geobacter metallireducens GS-15E, other
    Geobacter sp. FRC-32E, other
    Geobacter sp. M18E, other
    Geobacter sp. M21E, other
    Geobacter sulfurreducens PCAE, other
    Geobacter uraniireducens Rf4E, other
    Pelobacter propionicus DSM 2379aC, C, C
    Syntrophobacter fumaroxidans MPOBbE, E
    Gammaproteobacteria (4)Gammaproteobacterium HdN1E, E
    Nitrosococcus halophilus Nc4B, E
    Nitrosococcus oceani ATCC 19707B, E
    Nitrosococcus watsoni C-113B, E
    Gemmatimonadetes (1)Gemmatimonas aurantiaca T-27C, C
    • ↵a The genome of this strain encoded three identical copies of operons predicted to encode complex I.

    • ↵b The genome of this strain was predicted to encode one copy of nuoEFG genes and two copies of the remaining genes encoding complex I. Two isozymes could potentially be made from these components.

  • TABLE 2 

    Most significantly enriched biochemical pathways when comparing clade B- to clade E-containing gammaproteobacteria

    Pathways enriched in clade B-containing gammaproteobacteria, P  < 0.05Pathways enriched in clade E-containing gammaproteobacteria, P < 0.05
    Cytochrome bc1 complex respiratory unitFumarate reductase, prokaryotes
    Cytochrome bc1 complexDissimilatory nitrate reduction, nitrate → ammonia
    Cytochrome c oxidaseMalonate semialdehyde pathway, propionyl-CoA → acetyl-CoA
    Cytochrome c oxidase, prokaryotesValine/isoleucine biosynthesis, pyruvate → valine/2-oxobutanoate → isoleucine
    RaxAB-RaxC type I secretion systemIsoleucine biosynthesis, threonine → 2-oxobutanoate → isoleucine
    Type IV secretion systemAscorbate degradation, ascorbate → d-xylulose-5P
    Helicobacter pylori pathogenicity signature, cagA pathogenicity islandCatechol ortho-cleavage, catechol → 3-oxoadipate
    HydH-HydG (metal tolerance) two-component regulatory systemType III secretion system
    CheA-CheYBV (chemotaxis) two-component regulatory systemEnterohemorrhagic/enteropathogenic E. coli pathogenicity signature, T3SS and effectors
    Cph1-Rcp1 (light response) two-component regulatory systemRstB-RstA two-component regulatory system
    PleC-PleD (cell fate control) two-component regulatory systemSulfate transport system
    Cysteine biosynthesis, homocysteine and serine → cysteineIron(III) transport system
    Putative ABC transport systemThiamine transport system
    ABC-2-type transport systemPutative spermidine/putrescine transport system
    Fatty acid biosynthesis, elongationGlycine betaine/proline transport system
    Ribosome, bacterial-Arabinose transport system
    NADH:quinone oxidoreductase, prokaryotesaLysine/arginine/ornithine transport system
    Histidine transport system
    Glutamate/aspartate transport system
    General l-amino acid transport system
    Cystine transport system
    Branched-chain amino acid transport system
    Peptides/nickel transport system
    Iron complex transport system
    PTS system, glucose-specific II component
    PTS system, cellobiose-specific II component
    PTS system, ascorbate-specific II component
    Dipeptide transport system
    Microcin C transport system
    Taurine transport system
    Sulfonate transport system
    Oligopeptide transport system
    • ↵a Only 2 of the 14 genes encoding complex I (nuoC and nuoD) were enriched in clade B-containing gammaproteobacteria. This is because these genes are separate in clade B operons (counted as 2 genes) and fused in clade E operons (counted as 0 genes). Thus, clade B-containing gammaproteobacteria appear to be enriched for complex I (NADH:quinone oxidoreductase, prokaryotes).

Supplemental Material

  • Figures
  • Tables
  • Additional Files
  • Figure S1 

    Phylogeny of concatenated complex I subunits NuoBCD. A concatenated phylogeny of predicted NuoBCD complex I subunits from sequenced bacterial genomes. Download Figure S1, PDF file, 2.4 MB.

    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.

  • Figure S2 

    Phylogeny of complex I subunit NuoF. A phylogeny of predicted NuoF complex I subunits from sequenced bacterial genomes. Download Figure S2, PDF file, 2.3 MB.

    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.

  • Figure S3 

    Phylogeny of complex I subunit NuoG. A phylogeny of predicted NuoG complex I subunits from sequenced bacterial genomes. Download Figure S3, PDF file, 2.1 MB.

    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.

  • Figure S4 

    Phylogeny of complex I subunit NuoH. A phylogeny of predicted NuoH complex I subunits from sequenced bacterial genomes. Download Figure S4, PDF file, 2.4 MB.

    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.

  • Figure S5 

    Phylogeny of complex I subunit NuoL. A phylogeny of predicted NuoL complex I subunits from sequenced bacterial genomes. Download Figure S5, PDF file, 2.3 MB.

    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.

  • Figure S6 

    Phylogeny of complex I subunit NuoM. A phylogeny of predicted NuoM complex I subunits from sequenced bacterial genomes. Download Figure S6, PDF file, 2.1 MB.

    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.

  • Figure S7 

    Phylogeny of complex I subunit NuoN. A phylogeny of predicted NuoN complex I subunits from sequenced bacterial genomes. Download Figure S7, PDF file, 2.5 MB.

    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.

  • Figure S8 

    Inheritance pattern of complex I in specific bacterial groups with support values. An identical phylogeny as depicted in Fig. 4 with SH-like support values provided for each node. Specifically, a species phylogeny of representative members of Bacteroidetes, Actinobacteria, Deltaproteobacteria, and Gammaproteobacteria was generated using the amino acid sequences of 9 highly conserved housekeeping genes. The absence or presence of complex I (by complex I clade) was mapped onto the phylogeny to show the patchwork inheritance pattern of complex I within specific groups of bacteria. For visualization purposes, Bacillus cereus was used to root the tree, as the Firmicutes phylum represents a distantly related phylum in which no complex I enzymes were identified. Abbreviations: C. Amoebophilus asiaticus, “Candidatus Amoebophilus asiaticus”; Blattabacterium sp. B. germ, Blattabacterium sp. Blattella germanica; Anaeromyxo. sp. Fw109-5; Anaeromyxobacter sp. Fw109-5; Syntrophobact. fumaroxidans, Syntrophobacter fumaroxidans; Pseudoxanthomonas s., Pseudoxanthomonas suwonensis; Pseuodoaltero. sp. SM9913, Pseudoalteromonas sp. SM9913; Actinobacillus pleuro., Actinobacillus pleuropneumoniae. Download Figure S8, PDF file, 1.7 MB.

    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.

  • Data Set S2 

    KEGG modules enriched in Actinobacteria, Bacteroidetes, Chloroflexi, Deltaproteobacteria, and Spirochaetes with complex I or in clade B-containing, clade E-containing Gammaproteobacteria. Download Data Set S2, XLSX file, 0.1 MB.

    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.

  • Data Set S1 

    Genomes used in the study and their associated metadata. Download Data Set S1, XLSX file, 0.1 MB.

    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.

Additional Files

  • Figures
  • Tables
  • Supplemental Material
  • Supplementary Data

    Supplementary Data

    Files in this Data Supplement:

    • Figure sf1, PDF - Figure sf1, PDF
    • Figure sf2, PDF - Figure sf2, PDF
    • Figure sf3, PDF - Figure sf3, PDF
    • Figure sf4, PDF - Figure sf4, PDF
    • Figure sf5, PDF - Figure sf5, PDF
    • Figure sf6, PDF - Figure sf6, PDF
    • Figure sf7, PDF - Figure sf7, PDF
    • Figure sf8, PDF - Figure sf8, PDF
    • Dataset sd1, XLSX - Dataset sd1, XLSX
    • Dataset sd2, XLSX - Dataset sd2, XLSX
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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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