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:

Hotspots of anaerobic ammonium oxidation at land–freshwater interfaces

Abstract

For decades, the conversion of organic nitrogen to dinitrogen gas by heterotrophic bacteria, termed heterotrophic denitrification, was assumed to be the main pathway of nitrogen loss in natural ecosystems. Recently, however, autotrophic bacteria have been shown to oxidize ammonium in the absence of oxygen, yielding dinitrogen gas. This process, termed anammox, accounts for over 50% of nitrogen loss in marine ecosystems1,2,3,4,5. However, the significance of anammox in freshwater ecosystems has remained uncertain6,7. Here, we report the occurrence of anammox hotspots at land–freshwater interfaces of lake riparian zones in North China, using molecular and isotopic tracing technologies. Laboratory incubations measuring anammox activity at substrate concentrations no more than 10% of those observed in situ yielded some of the highest potential activities reported for natural environments to date. Potential rates of anammox peaked in sediments sampled from the interface between land and water, as did the abundance of annamox bacteria. Scaling our findings up to the entire lake system, we estimate that interfacial anammox hotspots account for the loss of 103 g Nm−2 yr−1 from this lake region, and around one fifth of the nitrogen lost from the land–water interface.

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

Access options

Buy this article

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

Figure 1: Spatiotemporal distribution of anammox bacterial abundance and activity in the surface (above) and subsurface (centre) sediments/soils from a riparian zone of Baiyangdian Lake.
Figure 2: Biogeographical distribution of anammox bacterial abundance and activities in waterward sediments and interface sediments of Baiyangdian Lake.
Figure 3: Comparative fluxes of nitrous oxide (N2O) in waterward sediments and land–freshwater interface sediments over four seasons.

Similar content being viewed by others

References

  1. Kuypers, M. M. M. et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611 (2003).

    Article  Google Scholar 

  2. Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B. & Acuña-González, J. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608 (2003).

    Article  Google Scholar 

  3. Kuypers, M. M. M. et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl Acad. Sci. USA 102, 6478–6483 (2005).

    Article  Google Scholar 

  4. Arrigo, K. R. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2005).

    Article  Google Scholar 

  5. Lam, P. et al. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl Acad. Sci. USA 102, 6478–6483 (2007).

    Google Scholar 

  6. Zhu, G., Jetten, M. S. M., Kuschk, P., Ettwig, K. & Yin, C. Potential roles of anaerobic ammonia and methane oxidation in the nitrogen cycle of freshwater wetland ecosystems. Appl. Microbiol. Biotechnol. 86, 1043–1055 (2010).

    Article  Google Scholar 

  7. Humbert, S. et al. Molecular detection of anammox bacteria in terrestrial ecosystems: Distribution and diversity. ISME J. 4, 450–454 (2010).

    Article  Google Scholar 

  8. McClain, M. E. et al. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6, 301–312 (2003).

    Article  Google Scholar 

  9. Naiman, R. J. & Décamps, H. The ecology of interfaces: Riparian zones. Annu. Rev. Ecol. Syst. 28, 621–658 (1997).

    Article  Google Scholar 

  10. Wang, Y. et al. Spatial distribution of archaeal and bacterial ammonia oxidizers in the littoral buffer zone of a nitrogen-rich lake. J. Environ. Sci. 24, 790–799 (2012).

    Article  Google Scholar 

  11. Wang, W. D., Wang, D. L. & Yin, C. Q. A field study on the hydrochemistry of land/inland water ecotones with reed domination. Acta Hydroch. Hydrob. 30, 117–127 (2002).

    Article  Google Scholar 

  12. Hefting, M. M., Bobbink, R. & Janssens, M. P. Spatial variation in denitrification and N(2)O emission in relation to nitrate removal efficiency in a n-stressed riparian buffer zone. Ecosystems 9, 550–563 (2006).

    Article  Google Scholar 

  13. Zhu, G. et al. Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J. 5, 1905–1912 (2011).

    Article  Google Scholar 

  14. Meyer, R. L., Risgaard-Petersen, N. & Allen, D. E. Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl. Environ. Microbiol. 71, 6142–6149 (2005).

    Article  Google Scholar 

  15. Trimmer, M., Nicholls, J. C., Morley, N., Davies, C. A. & Aldridge, J. Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment. Appl. Environ. Microbiol. 71, 1923–1930 (2005).

    Article  Google Scholar 

  16. Zhu, G. et al. Anammox bacterial abundance, biodiversity and activity in a constructed wetland. Environ. Sci. Technol. 45, 9951–9958 (2011).

    Article  Google Scholar 

  17. Strous, M. et al. Missing lithotroph identified as new planctomycete. Nature 400, 446–449 (1999).

    Article  Google Scholar 

  18. Verhamme, D. T., Prosser, J. I. & Nicol, G. W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071 (2011).

    Article  Google Scholar 

  19. Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976–979 (2009).

    Article  Google Scholar 

  20. Teixeira, C., Magalhaes, C., Joye, S. B. & Bordalo, A. A. Potential rates and environmental controls of anaerobic ammonium oxidation in estuarine sediments. Aquat. Microb. Ecol. 66, 23–32 (2012).

    Article  Google Scholar 

  21. Wang, W. & Yin, C. The boundary filtration effect of reed-dominated ecotones under water level fluctuations. Wetlands Ecol. Manage. 16, 65–76 (2008).

    Article  Google Scholar 

  22. Kartal, B. et al. Molecular mechanism of anaerobic ammonium oxidation. Nature 479, 127–130 (2011).

    Article  Google Scholar 

  23. Yin, C. & Lan, Z. The nutrient retention by ecotone wetlands and their modification for Baiyangdian Lake restoration. Wat. Sci. Technol. 32, 159–167 (1995).

    Google Scholar 

  24. Harhangi, H. R. et al. Hydrazine synthase, a unique phylomarker to study the presence and biodiversity of anammox bacteria. Appl. Environ. Microbiol. 78, 752–758 (2012).

    Article  Google Scholar 

  25. Wang, Y. et al. Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiol. Lett. 336, 79–88 (2012).

    Article  Google Scholar 

  26. Risgaard-Petersen, N., Nielsen, L. P., Rysgaard, S., Dalsgaard, T. & Meyer, R. L. Application of the isotope pairing technique in sediments where anammox and denitrification co-exists. Limnol. Oceanogr. Meth. 1, 63–73 (2003).

    Article  Google Scholar 

  27. Thamdrup, B. & Dalsgaard, T. Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl. Environ. Microbiol. 68, 1312–1318 (2002).

    Article  Google Scholar 

  28. Wang, H., Yang, L., Wang, W., Lu, J. & Yin, C. Nitrous oxide (N2O) fluxes and their relationships with water-sediment characteristics in a hyper-eutrophic shallow lake, China. J. Geophys. Res. 112, G01005 (2007).

    Article  Google Scholar 

  29. Kurola, J., Salkinoja-Salonen, M., Aarnio, T., Hultman, J. & Romantschuk, M. Activity, diversity and population size of ammonia-oxidising bacteria in oilcontaminated landfarming soil. FEMS Microbiol. Lett. 250, 33–38 (2005).

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank M. Yang, J. He, Y. Mu and J. Liu for their help, and J. Guo and B. Qu for discussions. This research is financially supported by the National Natural Science Foundation of China (No. 21077119), Knowledge Innovation Program of the Chinese Academy of Sciences (KZCX2-EW-410-01), and special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (12L03ESPC). Moreover, G.Z. gratefully acknowledges the support of the Beijing Nova Program (2011095) and K.C. Wong Education Foundation, Hong Kong. The anammox research of Mike Jetten is supported by ERC Advanced Grant 232937 and the 2012 Spinoza Prize of the Netherlands Organization for Scientific Research (NWO). N.R-P. is funded by the German Max Planck Society and the Danish National Research Foundation.

Author information

Authors and Affiliations

Authors

Contributions

The project was conceived and led by G.Z. and C.Y. S.W., W.W., Y.W., L.Z., B.J. and G.Z. contributed to the sample analysis. G.Z. wrote the paper and all co-authors substantially contributed by commenting upon and revising it.

Corresponding author

Correspondence to Guibing Zhu.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 2042 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhu, G., Wang, S., Wang, W. et al. Hotspots of anaerobic ammonium oxidation at land–freshwater interfaces. Nature Geosci 6, 103–107 (2013). https://doi.org/10.1038/ngeo1683

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo1683

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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