Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils

Nature Geoscience volume 2, pages621–624(2009)Cite this article

Abstract

The oxidation of ammonia to nitrate, nitrification, is a key process in the nitrogen cycle. Ammonia-oxidizing archaea are present in large numbers in the ocean1,2,3 and soils4,5,6, suggesting a potential role for archaea, in addition to bacteria, in the global nitrogen cycle7,8. However, the importance of archaea to nitrification in agricultural soils is not well understood4. Here, we examine the contribution of ammonia-oxidizing archaea and bacteria to nitrification in six grassland soils in New Zealand using a quantitative polymerase chain reaction. We show that although ammonia-oxidizing archaea are present in large numbers in these soils, neither their abundance nor their activity increased with the application of an ammonia substrate, suggesting that their abundance was not related to the rate of nitrification. In contrast, the number of ammonia-oxidizing bacteria increased 3.2–10.4-fold and their activity increased 177-fold, in response to ammonia additions. Indeed, we find a significant relationship between the abundance of ammonia-oxidizing bacteria and the rate of nitrification. We suggest that nitrification is driven by bacteria rather than archaea in these nitrogen-rich grassland soils.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

Rent or Buy

All prices are NET prices.

Figure 1: AOA and AOB amoA gene copy numbers in the six soils in the control treatments at the start of the incubation experiment.
Figure 2: Dynamics of AOB and AOA populations and nitrification rate in the Waikato soil in the incubation study.
Figure 3: Relationships between the amount of NO3−–N produced and ammonia oxidizer populations from the incubation study.
Figure 4: RNA copy numbers of the AOB and AOA populations in the WK soil as affected by applications of cow urine-N and DCD after 49 days of incubation.

References

  1. 1

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

    Article  Google Scholar 

  2. 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  Google Scholar 

  3. 3

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

    Article  Google Scholar 

  4. 4

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

    Article  Google Scholar 

  5. 5

    He, J. Z. et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364–2374 (2007).

    Article  Google Scholar 

  6. 6

    Schauss, K. et al. Dynamics of functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ. Microbiol. 11, 446–456 (2009).

    Article  Google Scholar 

  7. 7

    Nicol, G. W. & Schleper, C. Ammonia-oxidising Crenarchaeota: Important players in the nitrogen cycle? Trends Microbiol. 14, 207–212 (2006).

    Article  Google Scholar 

  8. 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  Google Scholar 

  9. 9

    Francis, C. A., Beman, J. M. & Kuypers, M. M. New processes and players in the nitrogen cycle: The microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19–27 (2007).

    Article  Google Scholar 

  10. 10

    Di, H. J. & Cameron, K. C. The use of a nitrification inhibitor, dicyandiamide (DCD), to reduce nitrate leaching from cow urine patches in a grazed dairy pasture under irrigation. Soil Use Manag. 18, 395–403 (2002).

    Article  Google Scholar 

  11. 11

    Di, H. J. & Cameron, K. C. Mitigation of nitrous oxide emissions in spray-irrigated grazed grassland by treating the soil with dicyandiamide, a nitrification inhibitor. Soil Use Manag. 19, 284–290 (2003).

    Article  Google Scholar 

  12. 12

    Amberger, A. Research on dicyandiamide as a nitrification inhibitor and future outlook. Commun. Soil Sci. Plant Anal. 20, 1933–1955 (1989).

    Article  Google Scholar 

  13. 13

    Shen, J. P., Zhang, L. M., Zhu, Y. G., Zhang, J. B. & He, J. Z. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol. 10, 1601–1611 (2008).

    Article  Google Scholar 

  14. 14

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

    Article  Google Scholar 

  15. 15

    Valentine, D. L. Adaptation to energy stress dictate the ecology and evolution of the Archaea. Nature Rev. Microbiol. 5, 316–323 (2007).

    Article  Google Scholar 

  16. 16

    Mahmood, S. & Prosser, J. I. The influence of synthetic sheep urine on ammonia oxidizing bacterial communities in grassland soil. FEMS Microbiol. Ecol. 56, 444–454 (2006).

    Google Scholar 

  17. 17

    Stephen, J. R., McCaig, A. E., Smith, Z., Prosser, J. I. & Embley, T. M. Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 62, 4147–4154 (1996).

    Google Scholar 

  18. 18

    Kowalchuk, G., Stienstra, A., Heilig, G., Stephen, J. & Woldendorp, J. Changes in the community structure of ammonia-oxidizing bacteria during secondary secession of calcareous grasslands. Environ. Microbiol. 2, 99–110 (2000).

    Article  Google Scholar 

  19. 19

    Horz, H. P., Barbrook, A., Field, C. B. & Bohannan, B. J. M. Ammonia-oxidizing bacteria respond to multifactorial global change. Proc. Natl Acad. Sci. USA 101, 15136–15141 (2004).

    Article  Google Scholar 

  20. 20

    Di, H. J., Cameron, K. C. & Sherlock, R. R. Comparison of the effectiveness of a nitrification inhibitor, dicyandiamide (DCD), in reducing nitrous oxide emissions in four different soils under different climatic and management conditions. Soil Use Manag. 23, 1–9 (2007).

    Article  Google Scholar 

  21. 21

    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).

    Google Scholar 

Download references

Acknowledgements

We would like to thank the New Zealand Foundation for Research, Science and Technology (FRST) for funding, R. Monaghan, S. Ledgard and M. Sheppard of AgResearch and B. Thorrold and D. Waugh of Dairy NZ for assistance with soil sampling, and E. Gerard and S. Brock of AgResearch and J. Lei, S. Moore, C. Barlow and T. Hendry of Lincoln University for technical support.

Author information

Affiliations

  1. Centre for Soil and Environmental Quality, PO Box 84, Lincoln University, Lincoln 7647, Canterbury, New Zealand

    H. J. Di & K. C. Cameron

  2. Research Centre for Eco-Environmental Sciences, Chinese Academy of Sciences, 18 Shuangqing Road, Beijing 100085, China

    J. P. Shen & J. Z. He

  3. Faculty of Agriculture and Life Sciences, PO Box 84, Lincoln University, Lincoln 7647, Canterbury, New Zealand

    C. S. Winefield

  4. AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch 8140, New Zealand

    M. O’Callaghan

  5. AgResearch Ltd, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand

    S. Bowatte

Authors
  1. H. J. Di
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. C. Cameron
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. P. Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. S. Winefield
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. O’Callaghan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Bowatte
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Z. He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The project was conceived and led by H.J.D. and K.C.C. The manuscript was written by H.J.D., assisted by the co-authors. J.P.S., C.S.W., M.O., S.B. and J.Z.H. contributed to the sample analysis.

Corresponding authors

Correspondence to H. J. Di or J. Z. He.

Supplementary information

Supplementary Information

Supplementary Information (PDF 423 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Di, H., Cameron, K., Shen, J. et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geosci 2, 621–624 (2009). https://doi.org/10.1038/ngeo613

Download citation

Further reading

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