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Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle

Nature volume 549, pages 269272 (14 September 2017) | Download Citation

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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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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Affiliations

  1. Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network Chemistry meets Microbiology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

    • K. Dimitri Kits
    • , Christopher J. Sedlacek
    • , Ping Han
    • , Petra Pjevac
    • , Anne Daebeler
    • , Stefano Romano
    • , Holger Daims
    •  & Michael Wagner
  2. Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky Ave. 33, Bld 2, 119071 Moscow, Russia

    • Elena V. Lebedeva
    •  & Alexandr Bulaev
  3. Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, Fredrik Bajers Vej 7H, 9220 Aalborg, Denmark

    • Mads Albertsen
  4. Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Building, Edmonton, Alberta T6G 2E9, Canada

    • Lisa Y. Stein

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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Holger Daims.

Reviewer Information Nature thanks M. Kuypers, A. Schramm and M. Strous for their contribution to the peer review of this work.

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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.

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https://doi.org/10.1038/nature23679

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