Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria

Nature volume 461, pages 976–979 (2009)Cite this article

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Schleper, C., Jurgens, G. & Jonuscheit, M. Genomic studies of uncultivated archaea. Nature Rev. Microbiol. 3, 479–488 (2005)

    Article  CAS  Google Scholar 

  2. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005)

    Article  ADS  CAS  Google Scholar 

  3. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005)

    Article  ADS  Google Scholar 

  4. de la Torre, J. R., Walker, C. B., Ingalls, A. E., Könneke, M. & Stahl, D. A. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10, 810–818 (2008)

    Article  CAS  Google Scholar 

  5. Wuchter, C. et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317–12322 (2006)

    Article  ADS  CAS  Google Scholar 

  6. Hatzenpichler, R. et al. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl Acad. Sci. USA 105, 2134–2139 (2008)

    Article  ADS  CAS  Google Scholar 

  7. Mincer, T. J. et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9, 1162–1175 (2007)

    Article  CAS  Google Scholar 

  8. Prosser, J. I. & Nicol, G. W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931–2941 (2008)

    Article  CAS  Google Scholar 

  9. Hashimoto, L. K., Kaplan, W. A., Wofsy, S. C. & McElroy, M. B. Transformations of fixed nitrogen and N2O in the Cariaco Trench. Deep-Sea Res. 30, 575–590 (1983)

    Article  ADS  CAS  Google Scholar 

  10. Olson, R. J. 15N tracer studies of the primary nitrite maximum. J. Mar. Res. 39, 203–226 (1981)

    CAS  Google Scholar 

  11. Yool, A., Martin, A. P., Fernandez, C. & Clark, D. R. The significance of nitrification for oceanic new production. Nature 447, 999–1002 (2007)

    Article  ADS  CAS  Google Scholar 

  12. Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008)

    Article  ADS  CAS  Google Scholar 

  13. Prosser, J. I. in Advances in Microbial Physiology (eds Rose, A. H. & Tempest, D. W.) 125–181 (Academic, 1989)

    Google Scholar 

  14. Ward, B. B. in Nitrification (ed. Prosser, J. I.) 157–184 (IRL Press, 1986)

    Google Scholar 

  15. Bollmann, A., Bär-Gilissen, M.-J. & Laanbroek, H. J. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 68, 4751–4757 (2002)

    Article  CAS  Google Scholar 

  16. Agogué, H., Brink, M., Dinasquet, J. & Herndl, G. J. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456, 788–791 (2008)

    Article  ADS  Google Scholar 

  17. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)

    Article  ADS  CAS  Google Scholar 

  18. Kirchman, D. L., Elifantz, H., Dittel, A. I., Malmstrom, R. R. & Cottrell, M. T. Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean. Limnol. Oceanogr. 52, 495–507 (2007)

    Article  ADS  CAS  Google Scholar 

  19. Laanbroek, H. J. & Woldendorp, J. W. in Advances in Microbial Ecology (ed. Jones, J. G.) 275–304 (Plenum, 1995)

    Book  Google Scholar 

  20. Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006)

    Article  ADS  CAS  Google Scholar 

  21. Stark, J. M. & Firestone, M. K. Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol. Biochem. 28, 1307–1317 (1996)

    Article  CAS  Google Scholar 

  22. Ward, B. B., Talbot, M. C. & Perry, M. J. Contributions of phytoplankton and nitrifying bacteria to ammonium and nitrite dynamics in coastal waters. Cont. Shelf Res. 3, 383–398 (1984)

    Article  ADS  Google Scholar 

  23. Karl, D. M., Knauer, G. A., Martin, J. H. & Ward, B. B. Bacterial chemolithotrophy in the ocean is associated with sinking particles. Nature 309, 54–56 (1984)

    Article  ADS  CAS  Google Scholar 

  24. Phillips, C. J., Smith, Z., Embley, T. M. & Prosser, J. I. Phylogenetic differences between particle-associated and planktonic ammonia-oxidizing bacteria of the β subdivision of the class Proteobacteria in the northwestern Mediterranean Sea. Appl. Environ. Microbiol. 65, 779–786 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Freitag, T. E., Chang, L. & Prosser, J. I. Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient. Environ. Microbiol. 8, 684–696 (2006)

    Article  CAS  Google Scholar 

  26. Button, D. K., Robertson, B. R., Lepp, P. W. & Schmidt, T. M. A small, dilute-cytoplasm, high-affinity, novel bacterium isolated by extinction culture and having kinetic constants compatible with growth at ambient concentrations of dissolved nutrients in seawater. Appl. Environ. Microbiol. 64, 4467–4476 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Button, D. K. Nutrient uptake by microorganisms according to kinetic parameters from theory as related to cytoarchitecture. Microbiol. Mol. Biol. Rev. 62, 636–645 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Kirchman, D. L. The uptake of inorganic nutrients by heterotrophic bacteria. Microb. Ecol. 28, 255–271 (1994)

    Article  CAS  Google Scholar 

  29. Eppley, R. W., Rogers, J. N. & McCarthy, J. J. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14, 912–920 (1969)

    Article  ADS  CAS  Google Scholar 

  30. Ouverney, C. C. & Fuhrman, J. A. Marine planktonic archaea take up amino acids. Appl. Environ. Microbiol. 66, 4829–4833 (2000)

    Article  CAS  Google Scholar 

  31. Berube, P. M., Samudrala, R. & Stahl, D. A. Transcription of all amoC copies is associated with recovery of Nitrosomonas europaea from ammonia starvation. J. Bacteriol. 189, 3935–3944 (2007)

    Article  CAS  Google Scholar 

  32. Rotthauwe, J.-H., Witzel, K. P. & Liesack, W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704–4712 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Stickland, J. D. H. & Parsons, T. R. A Practical Handbook of Seawater Analysis (Fisheries Research Board of Canada, 1972)

    Google Scholar 

  34. Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A. & Peterson, B. J. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56, 1801–1809 (1999)

    Article  CAS  Google Scholar 

  35. Lunau, M., Lemke, A., Walther, K., Martens-Habbena, W. & Simon, M. An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy. Environ. Microbiol. 7, 961–968 (2005)

    Article  Google Scholar 

  36. Gundersen, J. K., Ramsing, N. B. & Glud, R. N. Predicting the signal of O2 microsensors from physical dimensions, temperature, salinity, and O2 concentration. Limnol. Oceanogr. 43, 1932–1937 (1998)

    Article  ADS  CAS  Google Scholar 

  37. Suzuki, I., Dular, U. & Kwok, S. C. Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J. Bacteriol. 120, 556–558 (1974)

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Ward, B. B. Kinetic studies on ammonia and methane oxidation by Nitrosococcus oceanus . Arch. Microbiol. 147, 126–133 (1987)

    Article  CAS  Google Scholar 

  39. Bollmann, A., Schmidt, I., Saunders, A. M. & Nicolaisen, M. H. Influence of starvation on potential ammonia-oxidizing activity and amoA mRNA levels of Nitrosospira briensis . Appl. Environ. Microbiol. 71, 1276–1282 (2005)

    Article  CAS  Google Scholar 

  40. Button, D. K. Kinetics of nutrient-limited transport and microbial growth. Microbiol. Rev. 49, 270–297 (1985)

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Eppley, R. W. & Renger, E. H. Nitrogen assimilation of an oceanic diatom in nitrogen-limited continuous culture. J. Phycol. 10, 15–23 (1974)

    CAS  Google Scholar 

  42. Glover, H. E. The relationship between inorganic nitrogen oxidation and organic-carbon production in batch and chemostat cultures of marine nitrifying bacteria. Arch. Microbiol. 142, 45–50 (1985)

    Article  CAS  Google Scholar 

  43. Jiang, Q. Q. & Bakken, L. R. Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol. Ecol. 30, 171–186 (1999)

    Article  CAS  Google Scholar 

  44. Keen, G. A. & Prosser, J. I. Steady state and transient growth of autotrophic nitrifying bacteria. Arch. Microbiol. 147, 73–79 (1987)

    Article  CAS  Google Scholar 

  45. Loureiro, S. et al. The significance of organic nutrients in the nutrition of Pseudo-nitzschia delicatissima (Bacillariophyceae). J. Plankt. Res. 31, 399–410 (2009)

    Article  CAS  Google Scholar 

  46. Reay, D. S., Nedwell, D. B., Priddle, J. & Ellis-Evans, J. C. Temperature dependence of inorganic nitrogen uptake: reduced affinity for nitrate at suboptimal temperatures in both algae and bacteria. Appl. Environ. Microbiol. 65, 2577–2584 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Stehr, G., Böttcher, B., Dittberner, P., Rath, G. & Koops, H. P. The ammonia-oxidizing nitrifying population of the River Elbe estuary. FEMS Microbiol. Ecol. 17, 177–186 (1995)

    Article  CAS  Google Scholar 

  48. Suwa, Y., Imamura, Y., Suzuki, T., Tashiro, T. & Urushigawa, Y. Ammonia-oxidizing bacteria with different sensitivities to (NH4)2SO4 in activated sludges. Wat. Res. 28, 1523–1532 (1994)

    Article  CAS  Google Scholar 

  49. Ward, B. B. Kinetics of ammonia oxidation by a marine nitrifying bacterium: methane as a substrate analogue. Microb. Ecol. 19, 211–225 (1990)

    Article  CAS  Google Scholar 

  50. Watson, S. W. Characteristics of a marine nitrifying bacterium, Nitrosocystis oceanus sp. N. Limnol. Oceanogr. 10, R274–R289 (1965)

    Article  ADS  Google Scholar 

  51. Clegg, S. L. & Whitfield, M. A chemical model of seawater including dissolved ammonia and the stoichiometric dissociation constant of ammonia in estuarine water and seawater from -2 to 40°C. Geochim. Cosmochim. Acta 59, 2403–2421 (1995)

    Article  ADS  CAS  Google Scholar 

  52. Lee, S. & Fuhrman, J. A. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 53, 1298–1303 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Simon, M. & Azam, F. Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989)

    Article  ADS  CAS  Google Scholar 

Download references

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.

Author information

Author notes

  1. Paul M. Berube & José R. de la Torre

    Present address: Present addresses: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA (P.M.B.); Department of Biology, San Francisco State University, San Francisco, California 94132, USA (J.R.T).,

Authors and Affiliations

  1. Department of Civil & Environmental Engineering, University of Washington, Seattle, Washington 98105, USA,

    Willm Martens-Habbena, Paul M. Berube, Hidetoshi Urakawa, José R. de la Torre & David A. Stahl

Authors
  1. Willm Martens-Habbena
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul M. Berube
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hidetoshi Urakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José R. de la Torre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David A. Stahl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

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

Supplementary information

Supplementary Information

This file contains Supplementary Notes 1-3. Supplementary References, and Supplementary Figures 1-3 with Legends. (PDF 619 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08465

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing