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Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle

Abstract

Nitrification, the oxidation of ammonia (NH3) via nitrite (NO2) to nitrate (NO3), is a key process of the biogeochemical nitrogen cycle. For decades, ammonia and nitrite oxidation were thought to be separately catalysed by ammonia-oxidizing bacteria (AOB) and archaea (AOA), and by nitrite-oxidizing bacteria (NOB). The recent discovery of complete ammonia oxidizers (comammox) in the NOB genus Nitrospira1,2, which alone convert ammonia to nitrate, raised questions about the ecological niches in which comammox Nitrospira successfully compete with canonical nitrifiers. Here we isolate a pure culture of a comammox bacterium, Nitrospira inopinata, and show that it is adapted to slow growth in oligotrophic and dynamic habitats on the basis of a high affinity for ammonia, low maximum rate of ammonia oxidation, high growth yield compared to canonical nitrifiers, and genomic potential for alternative metabolisms. The nitrification kinetics of four AOA from soil and hot springs were determined for comparison. Their surprisingly poor substrate affinities and lower growth yields reveal that, in contrast to earlier assumptions, AOA are not necessarily the most competitive ammonia oxidizers present in strongly oligotrophic environments and that N. inopinata has the highest substrate affinity of all analysed ammonia oxidizer isolates except the marine AOA Nitrosopumilus maritimus SCM1 (ref. 3). These results suggest a role for comammox organisms in nitrification under oligotrophic and dynamic conditions.

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Figure 1: Ammonia oxidation kinetics of N. inopinata and three ammonia-oxidizing Thaumarchaeota.
Figure 2: Nitrite oxidation kinetics of N. inopinata.
Figure 3: Comparison of the affinities for NH3 and NO2 between the comammox organism N. inopinata and canonical ammonia- and nitrite-oxidizing microbes.
Figure 4: Influence of total ammonium concentration on the rate of ammonia oxidation by N. inopinata, N. gargensis and Nitrosospira spp. as described by ammonia oxidation kinetics.

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Acknowledgements

We thank A. Mueller for assistance with the cultivation of AOA strain 5A, M. Palatinszky for assistance with the cultivation of N. uzonensis, J. Vierheilig for help with molecular analyses and the cultivation of N. inopinata, and D. Gruber, N. Cyran, A. Klocker and S. A. Eichorst for assistance with sample preparation for electron microscopy. K.D.K., C.J.S., P.H., S.R. and M.W. were supported by the European Research Council Advanced Grant project NITRICARE 294343 (to M.W.). P.P. and H.D. were supported by the Austrian Science Fund (FWF) project P27319-B21, and A.D. and H.D. were supported by FWF project P25231-B21. K.D.K. and L.Y.S. were supported by the Natural Sciences and Engineering Research Council of Canada (RGPIN-2014-03745). M.A. was supported by research grant 15510 from the VILLUM FONDEN.

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H.D. and M.W. designed this study and wrote the manuscript with the help of all authors. K.D.K. and C.J.S. performed the kinetic and yield experiments. E.V.L. and A.B. purified N. inopinata. P.H., E.V.L. and A.B. enriched the N. uzonensis-related AOA strain 5A. A.D. and S.R. performed electron microscopy of N. inopinata. P.P. and L.Y.S. helped with data interpretation. M.A. performed purity checks of N. inopinata and AOA strain 5A by Illumina sequencing and bioinformatics analyses.

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Correspondence to Holger Daims.

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Extended data figures and tables

Extended Data Figure 1 Binning of the metagenome scaffolds from nitrifier cultures.

Circles represent scaffolds, scaled by the square root of their length. Only scaffolds ≥5 kbp are shown. Clusters of similarly coloured circles represent potential genome bins. a, Sequence-composition-independent binning of the scaffolds from the N. inopinata isolate. The previous enrichment culture ENR6, which contained N. inopinata and only one contaminating betaproteobacterial organism1, was used for comparison in differential coverage binning. The lack of scaffolds from the betaproteobacterium (coverage = 0) shows the absence of this organism in the pure culture of N. inopinata. To further confirm that no trace amounts of the betaproteobacterium were left in the pure culture, the trimmed sequence reads were also mapped to the ENR6 metagenomic assembly that contained the contaminant1. None of 5.8 million reads mapped to the betaproteobacterium, whereas 99.8% of reads mapped to the closed genome of N. inopinata. Purity of the N. inopinata culture was also confirmed by fluorescence in situ hybridization, quantitative PCR targeting the amoA gene of N. inopinata and the soxB gene of the betaproteobacterium1, and the absence of growth in an organic medium. b, Binning of the scaffolds from the ‘Ca. N. uzonensis’-related enrichment culture 5A based on coverage and the G+C content of DNA. Aside from the ‘Ca. N. uzonensis’-related AOA strain 5A (99.93% 16S rRNA sequence identity), the culture contained an alphaproteobacterium at low abundance. Since the genome coverage of strain 5A was 1,512× and that of the alphaproteobacterium was 8×, the relative abundance of strain 5A in the enrichment culture was 99.5%.

Extended Data Figure 2 Morphology and completely nitrifying activity of the N. inopinata isolate.

a, Scanning electron micrograph of spiral-shaped N. inopinata cells. The cells had a diameter of 0.2 to 0.3 μm and length of 0.7 to 1.7 μm. The scale bar represents 2 μm. b, Near-stoichiometric oxidation of 1 mM ammonium to nitrate with transient accumulation of nitrite. Data points show means, error bars show 1 s.d. of n = 3 biological replicates. If not visible, error bars are smaller than symbols. Source data

Extended Data Figure 3 Temperature optima of the ammonia-oxidizing activity of N. inopinata and N. gargensis.

a, Ammonia oxidation by N. inopinata over a temperature range from 30 to 50 °C. Since the optimum for activity was at 37 °C, kinetic analyses of N. inopinata were performed at this temperature. b, Ammonia oxidation by N. gargensis over a temperature range from 37 to 50 °C. Since the optimum for activity was at 46 °C, kinetic analyses of N. gargensis were performed at this temperature. Data points in a and b show means, error bars show 1 s.e.m. of n = 3 biological replicates. If not visible, error bars are smaller than symbols. Source data

Extended Data Figure 4 Ammonia oxidation kinetics of N. inopinata.

Apparent half-saturation constants (Km(app)) and maximum oxidation rates (Vmax) for total ammonium were determined by fitting the data to the Michaelis–Menten kinetic equation. The red curve indicates the best fit of the data. Standard errors of the estimates based on nonlinear regression are reported. See Methods for details of experiments and calculations. a, b, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption and discrete slopes over many substrate concentrations. Results for two biological replicates are shown here; a third biological replicate is shown in Fig. 1a. ce, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption in single-trace measurements. Results for three biological replicates are shown.

Extended Data Figure 5 Nitrite oxidation kinetics of N. inopinata.

ac, Nitrite oxidation rates were calculated from microsensor measurements of NO2-dependent O2 consumption and discrete slopes over many substrate concentrations. Results for three biological replicates are shown here; a fourth biological replicate is shown in Fig. 2. Apparent half-saturation constants (Km(app)) and maximum oxidation rates (Vmax) for nitrite were determined by fitting the data to the Michaelis–Menten kinetic equation. The red curve indicates the best fit of the data. Standard errors of the estimates based on nonlinear regression are reported. See Methods for details of experiments and calculations. Single trace measurements to analyse nitrite oxidation were not feasible because of the high Km(app) of N. inopinata for NO2 and the low solubility of O2 in water at 37 °C.

Extended Data Figure 6 Ammonia oxidation kinetics of N. gargensis.

Apparent half-saturation constants (Km(app)) and maximum oxidation rates (Vmax) for total ammonium were determined by fitting the data to the Michaelis–Menten kinetic equation. The red curve indicates the best fit of the data. Standard errors of the estimates based on nonlinear regression are reported. See Methods for details of experiments and calculations. a, b, Total ammonium oxidation rates were calculated from microsensor measurements of NH3 dependent O2 consumption and discrete slopes over many substrate concentrations. Results for two biological replicates are shown here; a third biological replicate is shown in Fig. 1b. c, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption in a single-trace measurement.

Extended Data Figure 7 Ammonia oxidation kinetics of N. viennensis.

Apparent half-saturation constants (Km(app)) and maximum oxidation rates (Vmax) for total ammonium were determined by fitting the data to the Michaelis–Menten kinetic equation. The red curve indicates the best fit of the data. Standard errors of the estimates based on nonlinear regression are reported. See Methods for details of experiments and calculations. a, b, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption and discrete slopes over many substrate concentrations. Results for two biological replicates are shown here; a third biological replicate is shown in Fig. 1c. c, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption in a single-trace measurement.

Extended Data Figure 8 Ammonia oxidation kinetics of ‘Ca. Nitrosotenuis uzonensis’.

Apparent half-saturation constants (Km(app)) and maximum oxidation rates (Vmax) for total ammonium were determined by fitting the data to the Michaelis–Menten kinetic equation. The red curve indicates the best fit of the data. Standard errors of the estimates based on nonlinear regression are reported. See Methods for details of experiments and calculations. a, b, Total ammonium oxidation rates were calculated from microsensor measurements of NH3-dependent O2 consumption and discrete slopes over many substrate concentrations. Results for two biological replicates are shown here; a third biological replicate is shown in Fig. 1d. Single-trace measurements to analyse ammonium oxidation were hampered by the slow rate of ammonium oxidation by ‘Ca. N. uzonensis’.

Extended Data Figure 9 Adaptation of N. inopinata to slow growth under highly oligotrophic conditions.

Data for N. inopinata are depicted in red, for AOA in blue, and for AOB in orange. a, b, Calculated specific affinities (a) and maximum rates of ammonia oxidation (b). Organisms for which parameters were determined in this study are depicted in bold. Remaining values were obtained from the literature3. Values from this study were determined with n = 6 biological replicates for N. inopinata and n = 4 biological replicates each for N. gargensis and N. viennensis. The specific affinity and Vmax of N. inopinata were significantly different from that of N. gargensis (P < 0.0001) and N. viennensis (P = 0.0001). c, Molar growth yield of ammonia-oxidizing microbes expressed as cellular protein formed per mol of NH3 oxidized. Organisms for which parameters were determined in this study are depicted in bold. Remaining values were obtained from the literature (see Methods for references). Values from this study were determined with n = 4 biological replicates each for N. inopinata, N. gargensis and N. viennensis. The mean molar growth yield of N. inopinata was 394.7 μg protein per mol of NH3 oxidized (s.d. = 20.2; n = 4), that of N. gargensis was 298.4 μg protein per mol of NH3 (s.d. = 24.2; n = 4), and that of N. viennensis was 304.3 μg protein per mol of NH3 (s.d. = 17.9; n = 4). The molar growth yield was significantly different between N. inopinata and that of N. gargensis (P = 0.0003) and N. viennensis (P = 0.0004). Source data

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Supplementary Information

This file contains a short formal description of Nitrospira inopinata sp. nov. (as a pure culture of this organism is first described in this manuscript), a Supplementary Discussion of genome-based hypotheses on the niche specialization of Nitrospira inopinata, and Supplementary References. (PDF 221 kb)

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Kits, K., Sedlacek, C., Lebedeva, E. et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549, 269–272 (2017). https://doi.org/10.1038/nature23679

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