Research ArticleENVIRONMENTAL STUDIES

Adaptability as the key to success for the ubiquitous marine nitrite oxidizer Nitrococcus

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Science Advances  01 Nov 2017:
Vol. 3, no. 11, e1700807
DOI: 10.1126/sciadv.1700807
  • Fig. 1 Occurrence and distribution of Nitrococcus in a marine OMZ and the global oceans.

    (A) Water column chemistry and nitrogen cycling rates in the Namibian OMZ. Left: Vertical distribution of oxygen, NO2, NH4+, and NO3 at station 2. Middle: Nitrite oxidation rates, N2O production rates, and cellular abundance of Nitrococcus and Nitrospina. Right: Rates of ammonia oxidation, nitrate reduction, and anammox measured with 15N-labeling experiments. Error bars show SDs derived from linear regression analyses. (B) Worldwide distribution of Nitrococcus mobilis and Nitrococcus-like phylotypes in the oceans. Combined abundance of all four phylotypes in different metagenomic data sets is denoted in orange (MG-RAST), turquoise (OSD), and blue (Tara Oceans). Circle size indicates percentage of 16S rRNA gene reads relative to all bacterial and archaeal 16S rRNA gene reads within each sample.

  • Fig. 2 Cell metabolic cartoon based on the annotation of the N. mobilis Nb-231 genome.

    ETF, electron-transport flavoprotein; hmp, NO dioxygenase; HYD, hydrogenase; NirBD, assimilatory nitrite reductase; NirK, copper-containing nitrite reductase (NO-forming); NXR, nitrite oxidoreductase; sNOR, NO reductase; PHB, polyhydroxybuterate; poly-P, polyphosphates; SOR, sulfite dehydrogenase; SQR, sulfide/quinone oxidoreductase; PPP, pentose phosphate pathway; TRAP, tripartite ATP-independent periplasmic transporter (TRAP-T); TRK, K+ transporter; RND, resistance-nodulation-division; ATPase, adenosine triphosphatase; ABC, ATP-binding cassette. Enzyme complexes of the electron transport chain are labeled by Roman numerals. Red and orange diamonds represent cytochrome c proteins and quinones, respectively. The legend indicates transport protein classifications.

  • Fig. 3 Denitrifying potential of Nitrococcus mobilis Nb-231.

    (A) Anaerobic nitrogen dissimilation under (left) organoheterotrophic conditions (500 μM 15NO3, 250 μM acetate, and 250 μM formate, anoxic) and (right) without the addition of electron donor (200 μM 15NO2, anoxic). See the main text for more details. Error bars indicate SD of three biological replicates. (B) FISH-SIMS analyses of single Nitrococcus cells in Namibian OMZ bottom water samples (1.20 m above seafloor), incubated with (top) 13C-labeled dissolved organic matter (DOM) or (bottom) 13C-labeled bicarbonate under hypoxic conditions. Left: Nitrococcus cells (green) targeted by CARD-FISH among other microbial cells (blue). Middle: 32S/12C of the corresponding cells. Right: 13C/12C ratio. Scale bars, 1 μm.

  • Fig. 4 Sulfide oxidation potential of N. mobilis Nb-231.

    (A) Oxygen consumption in the presence (diamonds; mean of three replicates) and absence (triangles; single measurement) of Na2S. Only one measurement every 2 min is shown. The arrow indicates the time point of substrate addition. (B) Sulfide consumption by N. mobilis Nb-231 (diamonds) and abiotic control (triangles). The curves represent the mean of three biological replicates, and error bars indicate the SD of three technical replicates.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/11/e1700807/DC1

    Supplementary Text

    fig. S1. Abundance of Nitrococcus-affiliated cells in the Namibian OMZ based on CARD-FISH counts.

    fig. S2. 16S rRNA gene-based phylogenetic tree visualizing the relation of four Nitrococcus phylotypes.

    fig. S3. Phylogenetic analysis of NxrA.

    fig. S4. Incubation experiments with N. mobilis Nb-231.

    fig. S5. Phylogenetic analysis of the sNOR.

    fig. S6. Selection of Tara Oceans, MG-RAST, and OSD samples that were mapped to the N. mobilis Nb-231 genome.

    fig. S7. Effect of reduced O2 and enhanced IO3 concentrations on nitrite oxidation rates.

    table S1. Percent identity of 16S rRNA genes between N .mobilis and the newly identified Nitrococcus-like phylotype 1.

    table S2. List of marine environmental metagenomes that contain at least one of the four Nitrococcus phylotypes.

    table S3. List of marine amplicon sequencing data sets that contain at least one of the four Nitrococcus phylotypes.

    table S4. N. mobilis strain Nb-231 proteins with predicted functions in key metabolic pathways.

    table S5. 13C enrichment of single Nitrococcus cells from the Namibian OMZ.

    table S6. Composition of marine NOB medium used to grow N. mobilis.

    table S7. Functional genes associated with Nitrococcus spp. in selected Tara Oceans metagenomes.

    table S8. Summary of stations, sampling depths, and 15N incubation experiments conducted.

    table S9. NOB specific 16S rRNA-targeted oligonucleotide probes.

    table S10. Substrate amendments for N. mobilis Nb-231 incubation experiments.

    References (6476)

  • Supplementary Materials

    This PDF file includes:

    • Supplementary Text
    • fig. S1. Abundance of Nitrococcus-affiliated cells in the Namibian OMZ based on CARD-FISH counts.
    • fig. S2. 16S rRNA gene-based phylogenetic tree visualizing the relation of four Nitrococcus phylotypes.
    • fig. S3. Phylogenetic analysis of NxrA.
    • fig. S4. Incubation experiments with N. mobilis Nb-231.
    • fig. S5. Phylogenetic analysis of the sNOR.
    • fig. S6. Selection of Tara Oceans, MG-RAST, and OSD samples that were mapped to the N. mobilis Nb-231 genome.
    • fig. S7. Effect of reduced O2 and enhanced IO3 concentrations on nitrite oxidation rates.
    • References (64–76)

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    Other Supplementary Material for this manuscript includes the following:

    • table S1 (Microsof Excel format). Percent identity of 16S rRNA genes between N .mobilis and the newly identified Nitrococcus-like phylotype 1.
    • table S2 (Microsof Excel format). List of marine environmental metagenomes that contain at least one of the four Nitrococcus phylotypes.
    • table S3 (Microsof Excel format). List of marine amplicon sequencing data sets that contain at least one of the four Nitrococcus phylotypes.
    • table S4 (Microsof word format). N. mobilis strain Nb-231 proteins with predicted functions in key metabolic pathways.
    • table S5 (Microsof Excel format). 13C enrichment of single Nitrococcus cells from the Namibian OMZ.
    • table S6 (Microsof Excel format). Composition of marine NOB medium used to grow N. mobilis.
    • table S7 (Microsof Excel format). Functional genes associated with Nitrococcus spp. in selected Tara Oceans metagenomes.
    • table S8 (Microsof Excel format). Summary of stations, sampling depths, and 15N incubation experiments conducted.
    • table S9 (Microsof Excel format). NOB specific 16S rRNA-targeted oligonucleotide probes.
    • table S10 (Microsof Excel format). Substrate amendments for N. mobilis Nb-231 incubation experiments.

    Download Tables S1 to S10

    Files in this Data Supplement: