Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria

Abstract

The discovery of ammonia oxidation by mesophilic and thermophilic Crenarchaeota and the widespread distribution of these organisms in marine and terrestrial environments indicated an important role for them in the global nitrogen cycle1,2,3,4,5,6,7. However, very little is known about their physiology or their contribution to nitrification8. Here we report oligotrophic ammonia oxidation kinetics and cellular characteristics of the mesophilic crenarchaeon ‘Candidatus Nitrosopumilus maritimus’ strain SCM1. Unlike characterized ammonia-oxidizing bacteria, SCM1 is adapted to life under extreme nutrient limitation, sustaining high specific oxidation rates at ammonium concentrations found in open oceans. Its half-saturation constant (Km = 133 nM total ammonium) and substrate threshold (≤10 nM) closely resemble kinetics of in situ nitrification in marine systems9,10 and directly link ammonia-oxidizing Archaea to oligotrophic nitrification. The remarkably high specific affinity for reduced nitrogen (68,700 l per g cells per h) of SCM1 suggests that Nitrosopumilus-like ammonia-oxidizing Archaea could successfully compete with heterotrophic bacterioplankton and phytoplankton. Together these findings support the hypothesis that nitrification is more prevalent in the marine nitrogen cycle than accounted for in current biogeochemical models11.

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Figure 1: Growth of SCM1 in ammonium-limited artificial sea water batch culture.
Figure 2: Ammonia oxidation kinetics of SCM1.
Figure 3: High-affinity ammonia oxidation by AOA dominates in oligotrophic environments.

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Acknowledgements

We thank A. M. Gee for technical assistance and C. B. Walker, K. C. Costa, S. Flagan, D. K. Button, M. G. Klotz, L. Bakken, S. Sandfest, M. Könneke, K. L. Hillesland and L. H. Larsen for discussions. This work was supported by NSF award MCB-0604448 to D.A.S. and J.R.T. and by NSF award OCE-0623174 to A. E. Ingalls, D.A.S. and A. H. Devol.

Author Contributions W.M.-H., J.R.T. and D.A.S. designed research; W.M.-H., P.M.B. and H.U. performed research; W.M.-H., J.R.T. and D.A.S. analysed the data; and W.M.-H. and D.A.S. wrote the paper.

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Correspondence to Willm Martens-Habbena or David A. Stahl.

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Martens-Habbena, W., Berube, P., Urakawa, H. et al. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976–979 (2009). https://doi.org/10.1038/nature08465

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