Skip to main content

Thank you for visiting 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.

Warming stimulates sediment denitrification at the expense of anaerobic ammonium oxidation


Temperature is one of the fundamental environmental variables governing microbially mediated denitrification and anaerobic ammonium oxidation (anammox) in sediments. The GHG nitrous oxide (N2O) is produced during denitrification, but not by anammox, and knowledge of how these pathways respond to global warming remains limited. Here, we show that warming directly stimulates denitrification-derived N2O production and that the warming response for N2O production is slightly higher than the response for denitrification in subtropical sediments. Moreover, denitrification had a higher optimal temperature than anammox. Integrating our data into a global compilation indicates that denitrifiers are more thermotolerant, whereas anammox bacteria are relatively psychrotolerant. Crucially, recent summer temperatures in low-latitude sediments have exceeded the optimal temperature of anammox, implying that further warming may suppress anammox and direct more of the nitrogen flow towards denitrification and associated N2O production, leading to a positive climate feedback at low latitudes.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Temperature responses of sedimentary denitrification, anammox and related N2O production potential rates.
Fig. 2: Temperature responses of the relative contribution of anammox to total gas (N2 + N2O) production (ra%).
Fig. 3: Variation of Q10 values for denitrification-related gas production and Nr-removal processes from both seasons.
Fig. 4: Compiled literature values for denitrification and anammox in subtropical, temperate and polar sediments globally.
Fig. 5: The projected increase of sedimentary denitrification and associated N2O production in coastal environments.

Data availability

The data that support the findings of this study can be requested from the corresponding author upon request.


  1. 1.

    Battye, W., Aneja, V. P. & Schlesinger, W. H. Is nitrogen the next carbon? Earth’s Future 5, 894–904 (2017).

    Google Scholar 

  2. 2.

    Rockstrom, J. A safe operating space for humanity. Nature 461, 472–475 (2009).

    Google Scholar 

  3. 3.

    Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).

    CAS  Google Scholar 

  4. 4.

    Galloway, J. N. et al. The nitrogen cascade. Bioscience 53, 341–356 (2003).

    Google Scholar 

  5. 5.

    Field, C. B. & Barros, V. R. Added value from IPCC approval sessions. Science 350, 36 (2015).

    CAS  Google Scholar 

  6. 6.

    Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).

    Google Scholar 

  7. 7.

    Magozzi, S. & Calosi, P. Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Glob. Change Biol. 21, 181–194 (2015).

    Google Scholar 

  8. 8.

    Allison, S. D. & Treseder, K. K. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob. Change Biol. 14, 2898–2909 (2008).

    Google Scholar 

  9. 9.

    Gudasz, C. et al. Temperature-controlled organic carbon mineralization in lake sediments. Nature 466, 478–481 (2010).

    CAS  Google Scholar 

  10. 10.

    Duan, S. W. & Kaushal, S. S. Warming increases carbon and nutrient fluxes from sediments in streams across land use. Biogeosciences 10, 1193–1207 (2013).

    Google Scholar 

  11. 11.

    Seitzinger, S. et al. Denitrification across landscapes and waterscapes: a synthesis. Ecol. Appl. 16, 2064–2090 (2006).

    CAS  Google Scholar 

  12. 12.

    Kuypers, M. M. M., Marchant, H. K. & Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 16, 263–276 (2018).

    CAS  Google Scholar 

  13. 13.

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

    CAS  Google Scholar 

  14. 14.

    Peng, X. et al. Long‐term fertilization alters the relative importance of nitrate reduction pathways in salt marsh sediments. J. Geophys. Res. Biogeosci. 121, 2082–2095 (2016).

    CAS  Google Scholar 

  15. 15.

    Koriyama, M., Koga, A., Seguchi, M. & Ishitani, T. Factors controlling denitrification of mudflat sediments in Ariake Bay, Japan. Environ. Monit. Assess. 188, 1–14 (2016).

    CAS  Google Scholar 

  16. 16.

    Devol, A. H. Denitrification, anammox, and N2 production in marine sediments. Annu. Rev. Mar. Sci. 7, 403–423 (2015).

    Google Scholar 

  17. 17.

    Engström, P., Penton, C. R. & Devola, A. H. Anaerobic ammonium oxidation in deep‐sea sediments off the Washington margin. Limnol. Oceanogr. 54, 1643–1652 (2009).

    Google Scholar 

  18. 18.

    Trimmer, M. & Nicholls, J. C. Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol. Oceanogr. 54, 577–589 (2009).

    CAS  Google Scholar 

  19. 19.

    Brin, L. D., Giblin, A. E. & Rich, J. J. Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnol. Oceanogr. 59, 851–860 (2014).

    CAS  Google Scholar 

  20. 20.

    Crowe, S. A., Canfield, D. E., Mucci, A., Sundby, B. & Maranger, R. Anammox, denitrification and fixed-nitrogen removal in sediments from the Lower St. Lawrence Estuary. Biogeosciences 9, 4309–4321 (2012).

    CAS  Google Scholar 

  21. 21.

    Tan, E., Hsu, T.-C., Huang, X., Lin, H.-J. & Kao, S.-J. Nitrogen transformations and removal efficiency enhancement of a constructed wetland in subtropical Taiwan. Sci. Total Environ. 601–602, 1378–1388 (2017).

    Google Scholar 

  22. 22.

    Canion, A. et al. Temperature response of denitrification and anammox reveals the adaptation of microbial communities to in situ temperatures in permeable marine sediments that span 50° in latitude. Biogeosciences 11, 309–320 (2014).

    Google Scholar 

  23. 23.

    Rich, J. J., Dale, O. R., Song, B. & Ward, B. B. Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb. Ecol. 55, 311–320 (2008).

    CAS  Google Scholar 

  24. 24.

    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).

    Google Scholar 

  25. 25.

    McTigue, N. D., Gardner, W. S., Dunton, K. H. & Hardison, A. K. Biotic and abiotic controls on co-occurring nitrogen cycling processes in shallow Arctic shelf sediments. Nat. Commun. 7, 13145 (2016).

    CAS  Google Scholar 

  26. 26.

    Brin, L. D., Giblin, A. E. & Rich, J. J. Similar temperature responses suggest future climate warming will not alter partitioning between denitrification and anammox in temperate marine sediments. Glob. Change Biol. 23, 331–340 (2017).

    Google Scholar 

  27. 27.

    Canion, A. et al. Temperature response of denitrification and anaerobic ammonium oxidation rates and microbial community structure in Arctic fjord sediments. Environ. Microbiol. 16, 3331–3344 (2014).

    CAS  Google Scholar 

  28. 28.

    Dalsgaard, T. & Thamdrup, B. Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl. Environ. Microbiol. 68, 3802–3808 (2002).

    CAS  Google Scholar 

  29. 29.

    Rysgaard, S., Glud, R. N., Risgaard-Petersen, N. & Dalsgaard, T. Denitrification and anammox activity in Arctic marine sediments. Limnol. Oceanogr. 49, 1493–1502 (2004).

    CAS  Google Scholar 

  30. 30.

    Myrstener, M., Jonsson, A. & Bergstrom, A. K. The effects of temperature and resource availability on denitrification and relative N2O production in boreal lake sediments. J. Environ. Sci. 47, 82–90 (2016).

    Google Scholar 

  31. 31.

    Smith, K. A., Thomson, P. E., Clayton, H., Mctaggart, I. P. & Conen, F. Effects of temperature, water content and nitrogen fertilisation on emissions of nitrous oxide by soils. Atmos. Environ. 32, 3301–3309 (1998).

    CAS  Google Scholar 

  32. 32.

    Parkin, T. B. & Kaspar, T. C. Nitrous oxide emissions from corn–soybean systems in the midwest. J. Environ. Qual. 35, 1496 (2006).

    CAS  Google Scholar 

  33. 33.

    Kawagoshi, Y., Fujisaki, K., Tomoshige, Y., Yamashiro, K. & Wei, Q. Temperature effect on nitrogen removal performance and bacterial community in culture of marine anammox bacteria derived from sea-based waste disposal site. J. Biosci. Bioeng. 113, 515–520 (2012).

    CAS  Google Scholar 

  34. 34.

    Pfenning, K. S. & McMahon, P. B. Effect of nitrate, organic carbon, and temperature on potential denitrification rates in nitrate-rich riverbed sediments. J. Hydrol. 187, 283–295 (1996).

    Google Scholar 

  35. 35.

    Boulêtreau, S., Salvo, E. & Lyautey, E. Temperature dependence of denitrification in phototrophic river biofilms. Sci. Total Environ. 416, 323–328 (2012).

    Google Scholar 

  36. 36.

    Jørgensen, C. J., Ole Stig, J., Bo, E. & Jens, A. Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment. Environ. Sci. Technol. 43, 4851–4857 (2009).

    Google Scholar 

  37. 37.

    Ambus, P. Control of denitrification enzyme activity in a streamside soil. FEMS Microbiol. Lett. 102, 225–234 (1993).

    CAS  Google Scholar 

  38. 38.

    Palacin-Lizarbe, C., Camarero, L. & Catalan, J. Denitrification temperature dependence in remote, cold and N-poor lake sediments. Water Resour. Res. 54, 1161–1173 (2018).

    CAS  Google Scholar 

  39. 39.

    Warneke, S., Schipper, L. A., Bruesewitz, D. A., Mcdonald, I. & Cameron, S. Rates, controls and potential adverse effects of nitrate removal in a denitrification bed. Ecol. Eng. 37, 511–522 (2011).

    Google Scholar 

  40. 40.

    Kuenen, J. G. Extraordinary anaerobic ammonium-oxidizing bacteria. ASM News 67, 456–462 (2001).

    Google Scholar 

  41. 41.

    Strous, M., Kuenen, J. G. & Jetten, M. S. Key physiology of anaerobic ammonium oxidation. Appl. Environ. Microbiol. 65, 3248–3250 (1999).

    CAS  Google Scholar 

  42. 42.

    Morita, R. Y. Psychrophilic bacteria. Bacteriol. Rev. 39, 144–167 (1975).

    CAS  Google Scholar 

  43. 43.

    Isaksen, M. F. & Jorgensen, B. B. Adaptation of psychrophilic and psychrotrophic sulfate-reducing bacteria to permanently cold marine environments. Appl. Environ. Microbiol. 62, 408–414 (1996).

    CAS  Google Scholar 

  44. 44.

    Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).

    CAS  Google Scholar 

  45. 45.

    King, D. & Nedwell, D. B. Changes in the nitrate-reducing community of an anaerobic saltmarsh sediment in response to seasonal selection by temperature. Microbiology 130, 2935–2941 (1984).

    CAS  Google Scholar 

  46. 46.

    Veraart, A. J., de Klein, J. J. & Marten, S. Warming can boost denitrification disproportionately due to altered oxygen dynamics. PLoS ONE 6, e18508 (2011).

    CAS  Google Scholar 

  47. 47.

    Hallin, S. et al. Soil functional operating range linked to microbial biodiversity and community composition using denitrifiers as model guild. PLoS ONE 7, e51962 (2012).

    CAS  Google Scholar 

  48. 48.

    Bestion, E., Schaum, C. E. & Yvon-Durocher, G. Nutrient limitation constrains thermal tolerance in freshwater phytoplankton. Limnol. Oceanogr. Lett. 3, 436–443 (2018).

    Google Scholar 

  49. 49.

    Greaver, T. L. et al. Key ecological responses to nitrogen are altered by climate change. Nat. Clim. Change 6, 836–843 (2016).

    CAS  Google Scholar 

  50. 50.

    Xue, K. et al. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. Nat. Clim. Change 6, 595–600 (2016).

    CAS  Google Scholar 

  51. 51.

    Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2, 106–110 (2011).

    Google Scholar 

  52. 52.

    Tscherko, D., Kandeler, E. & Jones, T. H. Effect of temperature on below-ground N-dynamics in a weedy model ecosystem at ambient and elevated atmospheric CO2 levels. Soil Biol. Biochem. 33, 491–501 (2001).

    CAS  Google Scholar 

  53. 53.

    Cao, W., Huang, Z., Zhai, W., Li, Y. & Hong, H. Isotopic evidence on multiple sources of nitrogen in the northern Jiulong River, Southeast China. Estuar. Coast. Shelf Sci. 163, 37–43 (2015).

    CAS  Google Scholar 

  54. 54.

    Hong, Q., Cai, P., Shi, X., Li, Q. & Wang, G. Solute transport into the Jiulong River estuary via pore water exchange and submarine groundwater discharge: new insights from 224Ra/228Th disequilibrium. Geochim. Cosmochim. Acta 198, 338–359 (2016).

    Google Scholar 

  55. 55.

    Chen, N., Hong, H., Zhang, L. & Cao, W. Nitrogen sources and exports in an agricultural watershed in Southeast China. Biogeochemistry 87, 169–179 (2008).

    CAS  Google Scholar 

  56. 56.

    Yan, X. et al. Distribution, fluxes and decadal changes of nutrients in the Jiulong River Estuary, Southwest Taiwan Strait. Chin. Sci. Bull. 57, 2307–2318 (2012).

    CAS  Google Scholar 

  57. 57.

    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).

    CAS  Google Scholar 

  58. 58.

    Tan, E. et al. Organic matter decomposition sustains sedimentary nitrogen loss in the Pearl River Estuary, China. Sci. Total Environ. 648, 508–517 (2019).

    CAS  Google Scholar 

  59. 59.

    Kao, S. J., Liu, K. K., Hsu, S. C., Chang, Y. P. & Dai, M. H. North Pacific-wide spreading of isotopically heavy nitrogen during the last deglaciation: evidence from the western Pacific. Biogeosciences 5, 1641–1650 (2008).

    CAS  Google Scholar 

  60. 60.

    Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal. Chem. 61, 2715–2718 (1989).

    CAS  Google Scholar 

  61. 61.

    Zheng, Z. Z. et al. Effects of temperature and particles on nitrification in a eutrophic coastal bay in southern China. J. Geophys. Res. 122, 2325–2337 (2017).

    CAS  Google Scholar 

  62. 62.

    Hsu, T. C. & Kao, S. J. Simultaneous measurement of sedimentary N2 and N2O production and a modified 15N isotope pairing technique. Biogeosciences 10, 7847–7862 (2013).

    Google Scholar 

  63. 63.

    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Google Scholar 

  64. 64.

    Perkins, D. M. et al. Consistent temperature dependence of respiration across ecosystems contrasting in thermal history. Glob. Change Biol. 18, 1300–1311 (2012).

    Google Scholar 

Download references


This study was supported by the National Natural Science Foundation of China (NSFC no. 91851209, 41721005, 41561164019 and 41806092). This is State Key Laboratory of Marine Environment Science contribution no. melpublication2019349. J.J.M. was supported by the Netherlands Earth System Science Center. Special acknowledgment to intensive field and laboratory work by J. C. Xu.

Author information




E.T. and S.-j.K. conceived the study and designed the experiment; E.T., W.Z., M.D. and L.T. performed the experiment and measured the samples; E.T., M.D., T.-C.H., L.T. and S.-j.K. analysed the data; E.T., Z.Z., X.Y., T.-C.H., J.J.M., T.W.T. and S.-j.K. contributed to the discussion of the results and wrote the manuscript.

Corresponding author

Correspondence to Shuh-ji Kao.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Climate Change thanks Rachel Horak, Jeremy Rich and Mark Trimmer for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary results, discussion, Figs. 1–8, Tables 1–8 and references.

Reporting Summary

Source data

Source Data Fig. 1

Numerical data.

Source Data Fig. 2

Numerical data.

Source Data Fig. 3

Numerical data.

Source Data Fig. 4

Numerical data.

Source Data Fig. 5

Numerical data.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tan, E., Zou, W., Zheng, Z. et al. Warming stimulates sediment denitrification at the expense of anaerobic ammonium oxidation. Nat. Clim. Chang. 10, 349–355 (2020).

Download citation


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