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Research Article | Applied and Environmental Science

Genome-Enabled Insights into the Ecophysiology of the Comammox Bacterium “Candidatus Nitrospira nitrosa”

Pamela Y. Camejo, Jorge Santo Domingo, Katherine D. McMahon, Daniel R. Noguera
Zarath M. Summers, Editor
Pamela Y. Camejo
a Department of Civil and Environmental Engineering, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Jorge Santo Domingo
b Environmental Protection Agency, Cincinnati, Ohio, USA
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Katherine D. McMahon
a Department of Civil and Environmental Engineering, University of Wisconsin—Madison, Madison, Wisconsin, USA
c Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
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  • ORCID record for Katherine D. McMahon
Daniel R. Noguera
a Department of Civil and Environmental Engineering, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Zarath M. Summers
ExxonMobil Research and Engineering
Roles: Editor
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DOI: 10.1128/mSystems.00059-17
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  • FIG 1
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    FIG 1

    Nutrient profiles of nitrogenous compounds (A), phosphorus and acetate (B), and oxygen concentration (C) in a regular cycle of the lab-scale SBR during stage 1. Dotted lines separate operational conditions within cycle. ANO, anoxic; AER, microaerobic; SET, settling.

  • FIG 2
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    FIG 2

    Comparison of the genome-wide average nucleotide identities and alignment percentages of Nitrospira-like genomes. The heat map shows the average nucleotide identity (red upper section of matrix) and the percentage of the two genomes that aligned (yellow lower section).

  • FIG 3
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    FIG 3

    RAxML phylogenetic tree of a concatenated alignment of 37 marker genes (nucleotide sequence) from a data set with the root placed on the branch leading to Nitrobacter winogradskyi. The numbers at the nodes of both trees show support values derived from 100 RAxML bootstrap replicates.

  • FIG 4
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    FIG 4

    (A) Normalized frequency of metagenomic reads mapping to the genome of comammox organisms, AOA, AOB, NOB, and anammox-related organisms in samples from stages 1 and 2 of the lab-scale SBR. (B) Relative abundance of reads mapping to genomes of Nitrospira-related bacteria in stage 1 sample, including the draft genomes retrieved in this study.

  • FIG 5
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    FIG 5

    Genomic differences between Nitrospira sp. UW-LDO-01 and “Ca. Nitrospira nitrosa.” (A) Venn diagram of ortholog clusters shared between the two draft genomes; (B) distribution of SEED functional categories in the fraction of orthologs shared by the two genomes; (C) distribution of SEED functional categories in ortholog clusters found in only one of the genomes (genome-specific fraction).

Tables

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  • TABLE 1

    Inventory of transcriptional regulators with implications for adaptive metabolism, from complete and draft genomes of Nitrospira

    Transcriptional regulatorGenePresence or absence of gene in species or strainaFunction
    Comammox organismsNOB
    Nitrospira sp. UW-LDO-01“Ca. Nitrospira nitrosa”“Ca. Nitrospira nitrificans”“Ca. Nitrospira inopinata”Nitrospira sp. Ga0074138Nitrospira sp. UW-LDO-02NitrospiramoscoviensisNitrospiradefluviiNitrospira sp. OL23
    Formate hydrogen lyase transcriptional activator fhlA +++++++++FhlA binds to formate hydrogen
    lyase structural genes (formate dehydrogenase and group 4 hydrogenase complex) to
    activate transcription of their promoters (54).
    Transcriptional activator protein NhaR nhaR +++++++−−NhaR regulates nhaA, a pH-dependent sodium-proton antiporter that responds to alkaline and saline conditions (82). It is also responsible for osmC induction
    (55), required for resistance to organic peroxides and osmotic conditions and for long-term survival in stationary phase (83, 84). NhaR also stimulates transcription of pga, a set of genes responsible for poly-β-1,6-N-acetyl-d- glucosamine (PGA) synthesis (56). PGA is involved in cell-cell adhesion and attachment, which stabilize biofilm formation (85).
    Hydrogen peroxide-inducible gene activator oxyR ++++++−++OxyR is required for the induction of a hydrogen peroxide-inducible regulon in response to elevated levels of hydrogen peroxide (57).
    Chemotaxis regulator CheZ cheZ +++++−+++CheZ is a component of the chemotaxis signal-transduction pathway (86). It controls the phosphorylation of CheY, a protein involved in the cell excitation response. Absence of CheZ results in nonchemotactic cells or long stimulus response latencies, demonstrating its critical importance during response to stimuli (87).
    Fumarate and nitrate reductase regulatory protein fnr +++−−++++Fnr is an oxygen-responsive regulator required for the expression of a number of genes involved in anaerobic metabolism (61, 88, 89), including fumarate reductase, nitrate and nitrite reductase, and cytochrome oxidase genes (90).
    • ↵a Plus and minus signs represent the presence and absence of each gene, respectively.

Supplemental Material

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  • TABLE S1

    Metrics of the two Nitrospira genomes assembled in this study after each genome refinement step. Download TABLE S1, DOCX file, 0.05 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • FIG S1

    Neighbor-joining phylogenetic tree based on full-length nucleotide sequences of homologs to amoA in the genome of ammonia-oxidizing prokaryotes, methane-oxidizing bacteria, and comammox. amoA sequences identified in other nitrifying prokaryotes through HMM profiling are highlighted in bold and named as the operational day of the sample, contig number in the assembly, and gene position within the contig (start-end). Bootstrap values are shown in the tree branches based on 1,000 bootstrap replicates. The scale bar represents the number of nucleotide substitutions per site. Sequences from Nitrospira sp. strain CG24_A-E belong to the genomes assembled in the work of Palomo et al. (37). Download FIG S1, PDF file, 0.3 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • FIG S2

    Neighbor-joining phylogenetic tree based on full-length nucleotide sequences of homologs to hao in the genome of ammonia-oxidizing bacteria and comammox. hao sequences identified in other nitrifying prokaryotes through HMM profiling are highlighted in bold and named as the operational-day of the sample, contig number in the assembly, and gene position within the contig (start-end). Bootstrap values are shown in the tree branches based on 1,000 bootstrap replicates. The scale bar represents the number of nucleotide substitutions per site. Download FIG S2, PDF file, 0.2 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • FIG S3

    Neighbor-joining phylogenetic tree based on full-length nucleotide sequences of homologs to nxrA in the genome of nitrite-oxidizing bacteria and comammox. nxrA sequences identified in other nitrifying prokaryotes through HMM profiling are highlighted in bold and named as the operational day of the sample, contig number in the assembly, and gene position within the contig (start-end). Bootstrap values are shown in the tree branches based on 1,000 bootstrap replicates. The scale bar represents the number of nucleotide substitutions per site. Download FIG S3, PDF file, 0.2 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • FIG S4

    Normalized metagenomic read coverage of contigs containing amoA (A), hao (B), and nxrA (C) genes, identified using HMM profiling, in samples from stages 1 and 2 of the lab-scale SBR. Sequences not belonging to UW-LDO-01 and UW-LDO-02 are labeled according to the sample day, contig number in the assembly, and position within contig (start-end). Download FIG S4, PDF file, 0.2 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • TABLE S2

    Genomes included in the metagenomic mapping analysis and the number of reads mapping to each of them. The number of mapping reads was also normalized by the number of reads in each metagenome, paired-end read average length, and genome size. Download TABLE S2, DOCX file, 0.1 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • TABLE S3

    Inventory of genes involved in energy-driving processes from complete and draft genomes of Nitrospira. Gray and white rectangles represent the presence and absence of each gene, respectively. Download TABLE S3, DOCX file, 0.1 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

  • DATA SET S1

    Fasta file with contigs from the assembled metagenomic data containing nitrifying genes (amoA, hao, and nxrA). Download DATA SET S1, TXT file, 0.01 MB.

    Copyright © 2017 Camejo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license .

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Genome-Enabled Insights into the Ecophysiology of the Comammox Bacterium “Candidatus Nitrospira nitrosa”
Pamela Y. Camejo, Jorge Santo Domingo, Katherine D. McMahon, Daniel R. Noguera
mSystems Sep 2017, 2 (5) e00059-17; DOI: 10.1128/mSystems.00059-17

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Genome-Enabled Insights into the Ecophysiology of the Comammox Bacterium “Candidatus Nitrospira nitrosa”
Pamela Y. Camejo, Jorge Santo Domingo, Katherine D. McMahon, Daniel R. Noguera
mSystems Sep 2017, 2 (5) e00059-17; DOI: 10.1128/mSystems.00059-17
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    • ABSTRACT
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KEYWORDS

“Ca. Nitrospira nitrosa”
comammox
NOB
Nitrospira
metagenomics

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