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Nitrous oxide emissions from permafrost-affected soils

Nature Reviews Earth & Environment volume 1, pages 420–434 (2020)Cite this article

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Abstract

Soils are sources of the potent greenhouse gas nitrous oxide (N2O) globally, but emissions from permafrost-affected soils have been considered negligible owing to nitrogen (N) limitation. Recent measurements of N2O emissions have challenged this view, showing that vegetated soils in permafrost regions are often small but evident sources of N2O during the growing season (~30 μg N2O–N m−2 day−1). Moreover, barren or sparsely vegetated soils, common in harsh climates, can serve as substantial sources of N2O (~455 μg N2O–N m−2 day−1), demonstrating the importance of permafrost-affected soils in Earth’s N2O budget. In this Review, we discuss N2O fluxes from subarctic, Arctic, Antarctic and alpine permafrost regions, including areas that likely serve as sources (such as peatlands) and as sinks (wetlands, dry upland soils), and estimate global permafrost-affected soil N2O emissions from previously published fluxes. We outline the below-ground N cycle in permafrost regions and examine the environmental conditions influencing N2O dynamics. Climate-change-related impacts on permafrost ecosystems and how these impacts could alter N2O fluxes are reviewed, and an outlook on the major questions and research needs to better constrain the global impact of permafrost N2O emissions is provided.

Key points

  • Published studies suggest that permafrost-affected soils are a source of nitrous oxide (N2O).

  • Compared with measurements of carbon dioxide and methane fluxes, measurements of N2O fluxes in permafrost regions are sparse and lacking during the non-growing season, making the magnitude of N2O fluxes across the vast permafrost regions uncertain.

  • Permafrost-affected soils store large amounts of nitrogen, but only a fraction is in bioavailable form. Strong plant–microorganism competition causes a general nitrogen limitation in permafrost-affected soils, often preventing N2O production and release.

  • Plant-regulatory effects on the size of the soil N pool are important, and N2O-emission hotspots occur in barren ground features, especially permafrost peatlands.

  • Climate warming and associated permafrost thaw, and other disturbances, could turn permafrost regions into a globally relevant source of N2O, creating a non-carbon permafrost feedback to the global climate system.

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Fig. 1: Map of locations with published N2O flux measurements in permafrost regions.
Fig. 2: Permafrost-affected soil biogeochemistry.
Fig. 3: N2O dynamics across the permafrost landscape.
Fig. 4: N2O fluxes under various environmental conditions.
Fig. 5: Idealized N2O fluxes during perturbations.

References

  1. Gruber, S. Derivation and analysis of a high-resolution estimate of global permafrost zonation. Cryosphere 6, 221–233 (2012).

    Google Scholar 

  2. Hugelius, G. et al. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593 (2014).

    Google Scholar 

  3. Jobbágy, E. G. & Jackson, R. B. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 10, 423–436 (2000).

    Google Scholar 

  4. Batjes, N. H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil. Sci. 47, 151–163 (1996).

    Google Scholar 

  5. Post, W. M., Emmanuel, W. R., Zinke, P. J. & Stangenberger, A. G. Soil carbon pools and world life zones. Nature 298, 156–159 (1982).

    Google Scholar 

  6. Harris, S. A. et al. Glossary of Permafrost and Related Ground-ice Terms (National Research Council Canada, 1988).

  7. Kou, D. et al. Spatially-explicit estimate of soil nitrogen stock and its implication for land model across Tibetan alpine permafrost region. Sci. Total. Environ. 650, 1795–1804 (2019).

    Google Scholar 

  8. Harden, J. W. et al. Field information links permafrost carbon to physical vulnerabilities of thawing. Geophys. Res. Lett. 39, L15704 (2012).

    Google Scholar 

  9. Schädel, C. et al. Circumpolar assessment of permafrost C quality and its vulnerability over time using long-term incubation data. Glob. Change Biol. 20, 641–652 (2014).

    Google Scholar 

  10. Kirtman, B. et al. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker, T. F. et al.) 953–1028 (Cambridge Univ. Press, 2013).

  11. Pepin, N. et al. Elevation-dependent warming in mountain regions of the world. Nat. Clim. Change 5, 424–430 (2015).

    Google Scholar 

  12. IPCC in IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds Pörtner H.-O. et al.) in press (IPCC, 2019).

  13. McGuire, A. D. et al. Dependence of the evolution of carbon dynamics in the northern permafrost region on the trajectory of climate change. Proc. Natl Acad. Sci. USA 115, 3882–3887 (2018).

    Google Scholar 

  14. Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).

    Google Scholar 

  15. Schaefer, K., Lantuit, H., Romanovsky, V. E., Schuur, E. A. G. & Witt, R. The impact of the permafrost carbon feedback on global climate. Environ. Res. Lett. 9, 085003 (2014).

    Google Scholar 

  16. Butterbach-Bahl, K., Baggs, E. M., Dannenmann, M., Kiese, R. & Zechmeister-Boltenstern, S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos. Trans. R. Soc. B Biol. Sci. 368, 20130122 (2013). An overview of the current state of knowledge, level of process understanding and new research advances related to soil N 2O fluxes.

    Google Scholar 

  17. Myhre, G. et al. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Vol. 423 (eds Stocker, T. F. et al.) 659–740 (Cambridge Univ. Press, 2013).

  18. Ravishankara, A., Daniel, J. S. & Portmann, R. W. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125 (2009).

    Google Scholar 

  19. Voigt, C. et al. Increased nitrous oxide emissions from Arctic peatlands after permafrost thaw. Proc. Natl Acad. Sci. USA 114, 6238–6243 (2017). Showed a direct release of N 2O from thawing permafrost peatland mesocosms for the first time.

    Google Scholar 

  20. Turetsky, M. R. et al. Permafrost collapse is accelerating carbon release. Nature 569, 32–34 (2019).

    Google Scholar 

  21. Parmentier, F.-J., Sonnentag, O., Mauritz, M., Virkkala, A. M. & Schuur, E. A. G. Is the northern permafrost zone a source or a sink for carbon? Eos https://doi.org/10.1029/2019EO130507 (2019).

    Article  Google Scholar 

  22. Olefeldt, D., Turetsky, M. R., Crill, P. M. & McGuire, A. D. Environmental and physical controls on northern terrestrial methane emissions across permafrost zones. Glob. Change Biol. 19, 589–603 (2013).

    Google Scholar 

  23. Nadelhoffer, K. J., Giblin, A. E., Shaver, G. R. & Laundre, J. A. Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72, 242–253 (1991).

    Google Scholar 

  24. Bernhardt, E. S. et al. Control points in ecosystems: moving beyond the hot spot hot moment concept. Ecosystems 20, 665–682 (2017).

    Google Scholar 

  25. Abbott, B. W. & Jones, J. B. Permafrost collapse alters soil carbon stocks, respiration, CH4, and N2O in upland tundra. Glob. Change Biol. 21, 4570–4587 (2015). Observation of elevated N 2O concentrations in thermokarst erosion features.

    Google Scholar 

  26. Thompson, R. L. et al. Acceleration of global N2O emissions seen from two decades of atmospheric inversion. Nat. Clim. Change 9, 993–998 (2019).

    Google Scholar 

  27. Tian, H. et al. The global N2O Model Intercomparison Project. Bull. Am. Meteorol. Soc. 99, 1231–1251 (2018).

    Google Scholar 

  28. Bobbink, R. et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30–59 (2010).

    Google Scholar 

  29. Stewart, K. J., Grogan, P., Coxson, D. S. & Siciliano, S. D. Topography as a key factor driving atmospheric nitrogen exchanges in arctic terrestrial ecosystems. Soil Biol. Biochem. 70, 96–112 (2014). A review of environmental controls on N cycling in the Arctic.

    Google Scholar 

  30. Hobara, S. et al. Nitrogen fixation in surface soils and vegetation in an Arctic tundra watershed: a key source of atmospheric nitrogen. Arct. Antarct. Alp. Res. 38, 363–372 (2006).

    Google Scholar 

  31. Diáková, K. et al. Variation in N2 fixation in subarctic tundra in relation to landscape position and nitrogen pools and fluxes. Arct. Antarct. Alp. Res. 48, 111–125 (2016).

    Google Scholar 

  32. Frolking, S. et al. Peatlands in the Earth’s 21st century climate system. Environ. Rev. 19, 371–396 (2011).

    Google Scholar 

  33. Beermann, F. et al. Permafrost thaw and liberation of inorganic nitrogen in eastern Siberia. Permafr. Periglac. Process. 28, 605–618 (2017).

    Google Scholar 

  34. Keuper, F. et al. A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands. Glob. Change Biol. 18, 1998–2007 (2012). Showed high mineralization rates and biologically relevant release of mineral nitrogen from thawing permafrost peat.

    Google Scholar 

  35. Bjorkman, A. D. et al. Plant functional trait change across a warming tundra biome. Nature 562, 57–62 (2018).

    Google Scholar 

  36. Chen, D. et al. Assessment of past, present and future environmental changes on the Tibetan Plateau. Chin. Sci. Bull. 60, 3025–3035 (2015).

    Google Scholar 

  37. Olefeldt, D. et al. Circumpolar distribution and carbon storage of thermokarst landscapes. Nat. Commun. 7, 13043 (2016).

    Google Scholar 

  38. Biskaborn, B. K. et al. Permafrost is warming at a global scale. Nat. Commun. 10, 264 (2019).

    Google Scholar 

  39. Liljedahl, A. K. et al. Pan-Arctic ice-wedge degradation in warming permafrost and its influence on tundra hydrology. Nat. Geosci. 9, 312–319 (2016).

    Google Scholar 

  40. Rocha, A. V. et al. The footprint of Alaskan tundra fires during the past half-century: implications for surface properties and radiative forcing. Environ. Res. Lett. 7, 044039 (2012).

    Google Scholar 

  41. Phoenix, G. K. & Bjerke, J. W. Arctic browning: extreme events and trends reversing arctic greening. Glob. Change Biol. 22, 2960–2962 (2016).

    Google Scholar 

  42. Shaver, G. R. et al. Global change and the carbon balance of arctic ecosystems: carbon/nutrient interactions should act as major constraints on changes in global terrestrial carbon cycling. BioScience 42, 433–441 (1992).

    Google Scholar 

  43. Buckeridge, K. M., Zufelt, E., Chu, H. & Grogan, P. Soil nitrogen cycling rates in low arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330, 407–421 (2010).

    Google Scholar 

  44. Kicklighter, D. W., Melillo, J. M., Monier, E., Sokolov, A. P. & Zhuang, Q. Future nitrogen availability and its effect on carbon sequestration in Northern Eurasia. Nat. Commun. 10, 3024 (2019).

    Google Scholar 

  45. Wild, B. et al. Amino acid production exceeds plant nitrogen demand in Siberian tundra. Environ. Res. Lett. 13, 034002 (2018).

    Google Scholar 

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

    Google Scholar 

  47. Palmer, K., Biasi, C. & Horn, M. A. Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J. 6, 1058–1077 (2012).

    Google Scholar 

  48. Siciliano, S. D., Ma, W. K., Ferguson, S. & Farrell, R. E. Nitrifier dominance of Arctic soil nitrous oxide emissions arises due to fungal competition with denitrifiers for nitrate. Soil Biol. Biochem. 41, 1104–1110 (2009).

    Google Scholar 

  49. Zhu, R. et al. Stable isotope natural abundance of nitrous oxide emitted from Antarctic tundra soils: effects of sea animal excrement depositions. Rapid Commun. Mass Spectrom. 22, 3570–3578 (2008).

    Google Scholar 

  50. Chen, Y. et al. Linkage of plant and abiotic properties to the abundance and activity of N-cycling microbial communities in Tibetan permafrost-affected regions. Plant Soil 434, 453–466 (2019).

    Google Scholar 

  51. Ma, W. K. et al. Assessing the potential of ammonia oxidizing bacteria to produce nitrous oxide in soils of a high arctic lowland ecosystem on Devon Island, Canada. Soil Biol. Biochem. 39, 2001–2013 (2007).

    Google Scholar 

  52. Pérez, T. in Stable Isotopes and Biosphere–Atmosphere Interactions: Processes and Biological Controls (eds Flanagan, L. B., Ehleringer, J. R. & Pataki, D. E.) 69–84 (Elsevier, 2005).

  53. Martikainen, P. J., Nykänen, H., Crill, P. & Silvola, J. Effect of a lowered water table on nitrous oxide fluxes from northern peatlands. Nature 366, 51–53 (1993).

    Google Scholar 

  54. Yang, G. et al. Magnitude and pathways of increased nitrous oxide emissions from uplands following permafrost thaw. Environ. Sci. Technol. 52, 9162–9169 (2018).

    Google Scholar 

  55. Palmer, K. & Horn, M. A. Actinobacterial nitrate reducers and proteobacterial denitrifiers are abundant in N2O-metabolizing palsa peat. Appl. Environ. Microbiol. 78, 5584–5596 (2012).

    Google Scholar 

  56. Regina, K., Nykänen, H., Silvola, J. & Martikainen, P. J. Fluxes of nitrous oxide from boreal peatlands as affected by peatland type, water table level and nitrification capacity. Biogeochemistry 35, 401–418 (1996).

    Google Scholar 

  57. Regina, K., Silvola, J. & Martikainen, P. J. Short-term effects of changing water table on N2O fluxes from peat monoliths from natural and drained boreal peatlands. Glob. Change Biol. 5, 183–189 (1999).

    Google Scholar 

  58. Marushchak, M. E. et al. Hot spots for nitrous oxide emissions found in different types of permafrost peatlands. Glob. Change Biol. 17, 2601–2614 (2011).

    Google Scholar 

  59. Goldberg, S. D., Knorr, K. H., Blodau, C., Lischeid, G. & Gebauer, G. Impact of altering the water table height of an acidic fen on N2O and NO fluxes and soil concentrations. Glob. Change Biol. 16, 220–233 (2010).

    Google Scholar 

  60. Gil, J., Pérez, T., Boering, K., Martikainen, P. J. & Biasi, C. Mechanisms responsible for high N2O emissions from subarctic permafrost peatlands studied via stable isotope techniques. Glob. Biogeochem. Cycles 31, 172–189 (2017). Identified mechanisms governing high emissions in Arctic N 2O hotspots using stable isotopes.

    Google Scholar 

  61. Stewart, K. J., Brummell, M. E., Coxson, D. S. & Siciliano, S. D. How is nitrogen fixation in the high arctic linked to greenhouse gas emissions? Plant Soil 362, 215–229 (2013).

    Google Scholar 

  62. Müller, C., Stevens, R., Laughlin, R. & Jäger, H.-J. Microbial processes and the site of N2O production in a temperate grassland soil. Soil Biol. Biochem. 36, 453–461 (2004).

    Google Scholar 

  63. Minke, M., Donner, N., Karpov, N., de Klerk, P. & Joosten, H. Patterns in vegetation composition, surface height and thaw depth in polygon mires in the Yakutian Arctic (NE Siberia): a microtopographical characterisation of the active layer. Permafr. Periglac. Process. 20, 357–368 (2009).

    Google Scholar 

  64. Keiluweit, M., Gee, K., Denney, A. & Fendorf, S. Anoxic microsites in upland soils dominantly controlled by clay content. Soil Biol. Biochem. 118, 42–50 (2018).

    Google Scholar 

  65. Stewart, K. J., Lamb, E. G., Coxson, D. S. & Siciliano, S. D. Bryophyte-cyanobacterial associations as a key factor in N2-fixation across the Canadian Arctic. Plant Soil 344, 335–346 (2011).

    Google Scholar 

  66. Chapin, D. M. & Bledsoe, C. S. in Arctic Ecosystems in a Changing Climate (eds Chapin, F. S. et al.) 301–319 (Academic, 1992).

  67. Sullivan, B. W. et al. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc. Natl Acad. Sci. USA 111, 8101–8106 (2014).

    Google Scholar 

  68. Stewart, K. J., Coxson, D. & Grogan, P. Nitrogen inputs by associative cyanobacteria across a low arctic tundra landscape. Arct. Antarct. Alp. Res. 43, 267–278 (2011).

    Google Scholar 

  69. Zielke, M., Solheim, B., Spjelkavik, S. & Olsen, R. A. Nitrogen fixation in the high arctic: role of vegetation and environmental conditions. Arct. Antarct. Alp. Res. 37, 372–378 (2005).

    Google Scholar 

  70. Letendre, A.-C., Coxson, D. S. & Stewart, K. J. Restoration of ecosystem function by soil surface inoculation with biocrust in mesic and xeric alpine ecosystems. Ecol. Restor. 37, 101–112 (2019).

    Google Scholar 

  71. Convey, P. & Smith, R. I. L. in Plants and Climate Change. Tasks for Vegetation Science Vol. 41 (eds Rozema, J., Aerts, R. & Cornelissen, H.) 1–12 (Springer, 2005).

  72. Repo, M. E. et al. Large N2O emissions from cryoturbated peat soil in tundra. Nat. Geosci. 2, 189–192 (2009). The first discovery of high N 2O emitting surfaces, barren permafrost peatlands, in the Russian Arctic.

    Google Scholar 

  73. Elberling, B., Christiansen, H. H. & Hansen, B. U. High nitrous oxide production from thawing permafrost. Nat. Geosci. 3, 332–335 (2010). A mesocosms study showing high N 2O production potential in thawing permafrost after rewetting with nitrogen-rich meltwater.

    Google Scholar 

  74. Walker, D. A. et al. The circumpolar Arctic vegetation map. J. Veg. Sci. 16, 267–282 (2005).

    Google Scholar 

  75. Seppälä, M. Surface abrasion of palsas by wind action in Finnish Lapland. Geomorphology 52, 141–148 (2003).

    Google Scholar 

  76. Brummell, M. E., Farrell, R. E. & Siciliano, S. D. Greenhouse gas soil production and surface fluxes at a high arctic polar oasis. Soil Biol. Biochem. 52, 1–12 (2012).

    Google Scholar 

  77. Virtanen, T. & Ek, M. The fragmented nature of tundra landscape. Int. J. Appl. Earth Obs. Geoinf. 27, 4–12 (2014).

    Google Scholar 

  78. Treat, C. C. et al. Tundra landscape heterogeneity, not interannual variability, controls the decadal regional carbon balance in the Western Russian Arctic. Glob. Change Biol. 24, 5188–5204 (2018).

    Google Scholar 

  79. Lamb, E. G. et al. A High Arctic soil ecosystem resists long-term environmental manipulations. Glob. Change Biol. 17, 3187–3194 (2011).

    Google Scholar 

  80. Gregorich, E. G. et al. Emission of CO2, CH4 and N2O from lakeshore soils in an Antarctic dry valley. Soil Biol. Biochem. 38, 3120–3129 (2006).

    Google Scholar 

  81. Cao, Y., Ke, X., Guo, X., Cao, G. & Du, Y. Nitrous oxide emission rates over 10 years in an alpine meadow on the Tibetan Plateau. Pol. J. Environ. Stud. 27, 1353–1358 (2018).

    Google Scholar 

  82. Dinsmore, K. J. et al. Growing season CH4 and N2O fluxes from a subarctic landscape in northern Finland; from chamber to landscape scale. Biogeosciences 14, 799–815 (2017).

    Google Scholar 

  83. Kato, T., Hirota, M., Tang, Y. & Wada, E. Spatial variability of CH4 and N2O fluxes in alpine ecosystems on the Qinghai–Tibetan Plateau. Atmos. Environ. 45, 5632–5639 (2011).

    Google Scholar 

  84. Jiang, C., Yu, G., Fang, H., Cao, G. & Li, Y. Short-term effect of increasing nitrogen deposition on CO2, CH4 and N2O fluxes in an alpine meadow on the Qinghai-Tibetan Plateau, China. Atmos. Environ. 44, 2920–2926 (2010).

    Google Scholar 

  85. Werner, C., Butterbach-Bahl, K., Haas, E., Hickler, T. & Kiese, R. A global inventory of N2O emissions from tropical rainforest soils using a detailed biogeochemical model. Glob. Biogeochem. Cycles 21, GB3010 (2007).

    Google Scholar 

  86. Maljanen, M. et al. Greenhouse gas balances of managed peatlands in the Nordic countries–present knowledge and gaps. Biogeosciences 7, 2711–2738 (2010).

    Google Scholar 

  87. Maljanen, M. et al. Nitrous oxide production in boreal soils with variable organic matter content at low temperature-snow manipulation experiment. Biogeosciences 6, 2461–2473 (2009).

    Google Scholar 

  88. Potter, C. S., Matson, P. A., Vitousek, P. M. & Davidson, E. A. Process modeling of controls on nitrogen trace gas emissions from soils worldwide. J. Geophys. Res. Atmos. 101, 1361–1377 (1996).

    Google Scholar 

  89. Ciais, P. et al. in Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker, T. F. et al.) 465–570 (Cambridge Univ. Press, 2013).

  90. Kortelainen, P. et al. Lakes as nitrous oxide sources in the boreal landscape. Glob. Change Biol. 26, 1432–1445 (2020).

    Google Scholar 

  91. Priscu, J. C. The biogeochemistry of nitrous oxide in permanently ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Glob. Change Biol. 3, 301–315 (1997).

    Google Scholar 

  92. Kato, T., Toyoda, S., Yoshida, N., Tang, Y. & Wada, E. Isotopomer and isotopologue signatures of N2O produced in alpine ecosystems on the Qinghai–Tibetan Plateau. Rapid Commun. Mass Spectrom. 27, 1517–1526 (2013).

    Google Scholar 

  93. Du, Y. et al. Nitrous oxide emissions from two alpine meadows in the Qinghai–Tibetan Plateau. Plant Soil 311, 245–254 (2008).

    Google Scholar 

  94. Wagner-Riddle, C. et al. Globally important nitrous oxide emissions from croplands induced by freeze–thaw cycles. Nat. Geosci. 10, 279–283 (2017). Showed the important contribution of freeze–thaw cycles to annual N 2O emissions from (non-permafrost) croplands.

    Google Scholar 

  95. Voigt, C. et al. Warming of subarctic tundra increases emissions of all three important greenhouse gases - carbon dioxide, methane, and nitrous oxide. Glob. Change Biol. 23, 3121–3138 (2017).

    Google Scholar 

  96. Mu, C. C. et al. Permafrost collapse shifts alpine tundra to a carbon source but reduces N2O and CH4 release on the northern Qinghai-Tibetan Plateau. Geophys. Res. Lett. 44, 8945–8952 (2017).

    Google Scholar 

  97. Paré, M. C. & Bedard-Haughn, A. Landscape-scale N mineralization and greenhouse gas emissions in Canadian Cryosols. Geoderma 189, 469–479 (2012).

    Google Scholar 

  98. Stewart, K. J., Brummell, M. E., Farrell, R. E. & Siciliano, S. D. N2O flux from plant-soil systems in polar deserts switch between sources and sinks under different light conditions. Soil Biol. Biochem. 48, 69–77 (2012).

    Google Scholar 

  99. Brummell, M. E., Farrell, R. E., Hardy, S. P. & Siciliano, S. D. Greenhouse gas production and consumption in High Arctic deserts. Soil Biol. Biochem. 68, 158–165 (2014).

    Google Scholar 

  100. Bao, T. et al. Potential effects of ultraviolet radiation reduction on tundra nitrous oxide and methane fluxes in maritime Antarctica. Sci. Rep. 8, 3716 (2018).

    Google Scholar 

  101. Treat, C. C., Bloom, A. A. & Marushchak, M. E. Nongrowing season methane emissions – a significant component of annual emissions across northern ecosystems. Glob. Change Biol. 24, 3331–3343 (2018).

    Google Scholar 

  102. Natali, S. M. et al. Large loss of CO2 in winter observed across the northern permafrost region. Nat. Clim. Change 9, 852–857 (2019).

    Google Scholar 

  103. Du, Y., Guo, X., Cao, G. & Li, Y. Increased nitrous oxide emissions resulting from nitrogen addition and increased precipitation in an alpine meadow ecosystem. Pol. J. Environ. Stud. 25, 447–451 (2016).

    Google Scholar 

  104. Du, Y. et al. Simulation and prediction of nitrous oxide emission by the water and nitrogen management model on the Tibetan plateau. Biochem. Syst. Ecol. 65, 49–56 (2016).

    Google Scholar 

  105. Wang, H. et al. Molecular mechanisms of water table lowering and nitrogen deposition in affecting greenhouse gas emissions from a Tibetan alpine wetland. Glob. Change Biol. 23, 815–829 (2017).

    Google Scholar 

  106. Chang, R., Wang, G., Yang, Y. & Chen, X. Experimental warming increased soil nitrogen sink in the Tibetan permafrost. J. Geophys. Res. Biogeosci. 122, 1870–1879 (2017).

    Google Scholar 

  107. Chen, X. et al. Effects of warming and nitrogen fertilization on GHG flux in the permafrost region of an alpine meadow. Atmos. Environ. 157, 111–124 (2017).

    Google Scholar 

  108. Morishita, T. et al. CH4 and N2O dynamics of a Larix gmelinii forest in a continuous permafrost region of central Siberia during the growing season. Polar Sci. 8, 156–165 (2014).

    Google Scholar 

  109. Takakai, F. et al. CH4 and N2O emissions from a forest-alas ecosystem in the permafrost taiga forest region, eastern Siberia, Russia. J. Geophys. Res. Biogeosci. 113, G02002 (2008).

    Google Scholar 

  110. Williams, M. W., Brooks, P. D. & Seastedt, T. Nitrogen and carbon soil dynamics in response to climate change in a high-elevation ecosystem in the Rocky Mountains, USA. Arct. Alp. Res. 30, 26–30 (1998).

    Google Scholar 

  111. Pei, Z.-Y., Ouyang, H., Zhou, C.-P. & Xu, X.-L. N2O exchange within a soil and atmosphere profile in alpine grasslands on the Qinghai-Xizang plateau. Acta Bot. Sin. Engl. Ed. 46, 20–28 (2004).

    Google Scholar 

  112. Zona, D. et al. Cold season emissions dominate the Arctic tundra methane budget. Proc. Natl Acad. Sci. USA 113, 40–45 (2016).

    Google Scholar 

  113. Zhang, T., Wang, G., Yang, Y., Mao, T. & Chen, X. Non-growing season soil CO2 flux and its contribution to annual soil CO2 emissions in two typical grasslands in the permafrost region of the Qinghai-Tibet Plateau. Eur. J. Soil Biol. 71, 45–52 (2015).

    Google Scholar 

  114. Hénault, C., Grossel, A., Mary, B., Roussel, M. & Léonard, J. Nitrous oxide emission by agricultural soils: a review of spatial and temporal variability for mitigation. Pedosphere 22, 426–433 (2012).

    Google Scholar 

  115. Pärn, J. et al. Nitrogen-rich organic soils under warm well-drained conditions are global nitrous oxide emission hotspots. Nat. Commun. 9, 1135 (2018). A global field survey identifying the main drivers of N 2O emissions in (non-permafrost) soils.

    Google Scholar 

  116. Malone, E. T. et al. Decline in ecosystem δ13C and mid-successional nitrogen loss in a two-century postglacial chronosequence. Ecosystems 21, 1659–1675 (2018).

    Google Scholar 

  117. Gao, W. et al. Emissions of nitrous oxide from continuous permafrost region in the Daxing’an Mountains, Northeast China. Atmos. Environ. 198, 34–45 (2019).

    Google Scholar 

  118. Yan, Y. et al. Nitrogen deposition induced significant increase of N2O emissions in an dry alpine meadow on the central Qinghai–Tibetan Plateau. Agric. Ecosyst. Environ. 265, 45–53 (2018).

    Google Scholar 

  119. Lin, X. et al. Fluxes of CO2, CH4, and N2O in an alpine meadow affected by yak excreta on the Qinghai-Tibetan plateau during summer grazing periods. Soil Biol. Biochem. 41, 718–725 (2009).

    Google Scholar 

  120. Li, Y. et al. Seasonal changes of CO2, CH4 and N2O fluxes in different types of alpine grassland in the Qinghai-Tibetan Plateau of China. Soil Biol. Biochem. 80, 306–314 (2015).

    Google Scholar 

  121. Wilcox, E. J. et al. Tundra shrub expansion may amplify permafrost thaw by advancing snowmelt timing. Arct. Sci. 5, 202–217 (2019).

    Google Scholar 

  122. Abbott, B. W., Jones, J. B., Godsey, S. E., Larouche, J. R. & Bowden, W. B. Patterns and persistence of hydrologic carbon and nutrient export from collapsing upland permafrost. Biogeosciences 12, 3725–3740 (2015).

    Google Scholar 

  123. Buckeridge, K. M., Cen, Y.-P., Layzell, D. B. & Grogan, P. Soil biogeochemistry during the early spring in low arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability. Biogeochemistry 99, 127–141 (2010).

    Google Scholar 

  124. Kielland, K. Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383 (1994).

    Google Scholar 

  125. Bardgett, R. D., van der Wal, R., Jónsdóttir, I. S., Quirk, H. & Dutton, S. Temporal variability in plant and soil nitrogen pools in a high-Arctic ecosystem. Soil Biol. Biochem. 39, 2129–2137 (2007).

    Google Scholar 

  126. Shurpali, N. J. et al. Neglecting diurnal variations leads to uncertainties in terrestrial nitrous oxide emissions. Sci. Rep. 6, 25739 (2016).

    Google Scholar 

  127. Köster, E. et al. Carbon dioxide, methane and nitrous oxide fluxes from a fire chronosequence in subarctic boreal forests of Canada. Sci. Total. Environ. 601, 895–905 (2017).

    Google Scholar 

  128. Chen, Q., Zhu, R., Wang, Q. & Xu, H. Methane and nitrous oxide fluxes from four tundra ecotopes in Ny-Ålesund of the high Arctic. J. Environ. Sci. 26, 1403–1410 (2014).

    Google Scholar 

  129. Zhu, R., Chen, Q., Ding, W. & Xu, H. Impact of seabird activity on nitrous oxide and methane fluxes from High Arctic tundra in Svalbard, Norway. J. Geophys. Res. Biogeosci. 117, G04015 (2012).

    Google Scholar 

  130. Zhu, R., Ma, D. & Xu, H. Summertime N2O, CH4 and CO2 exchanges from a tundra marsh and an upland tundra in maritime Antarctica. Atmos. Environ. 83, 269–281 (2014).

    Google Scholar 

  131. Kelsey, K. C. et al. Phenological mismatch in coastal western Alaska may increase summer season greenhouse gas uptake. Environ. Res. Lett. 13, 044032 (2018).

    Google Scholar 

  132. Sun, L., Zhu, R., Xie, Z. & Xing, G. Emissions of nitrous oxide and methane from Antarctic tundra: role of penguin dropping deposition. Atmos. Environ. 36, 4977–4982 (2002).

    Google Scholar 

  133. Neff, J. C., Bowman, W. D., Holland, E. A., Fisk, M. C. & Schmidt, S. K. Fluxes of nitrous oxide and methane from nitrogen-amended soils in a Colorado alpine ecosystem. Biogeochemistry 27, 23–33 (1994).

    Google Scholar 

  134. Cui, Q. et al. Effects of warming on N2O fluxes in a boreal peatland of Permafrost region, Northeast China. Sci. Total. Environ. 616–617, 427–434 (2018).

    Google Scholar 

  135. Li, F., Zhu, R., Bao, T., Wang, Q. & Xu, H. Sunlight stimulates methane uptake and nitrous oxide emission from the High Arctic tundra. Sci. Total. Environ. 572, 1150–1160 (2016).

    Google Scholar 

  136. Serreze, M. C. & Francis, J. A. The Arctic amplification debate. Clim. Change 76, 241–264 (2006).

    Google Scholar 

  137. Schaeffer, S. M., Sharp, E., Schimel, J. P. & Welker, J. M. Soil–plant N processes in a High Arctic ecosystem, NW Greenland are altered by long-term experimental warming and higher rainfall. Glob. Change Biol. 19, 3529–3539 (2013).

    Google Scholar 

  138. Rustad, L. E. et al. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001).

    Google Scholar 

  139. Biasi, C. et al. Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307, 191–205 (2008).

    Google Scholar 

  140. Jones, B. M. et al. Recent Arctic tundra fire initiates widespread thermokarst development. Sci. Rep. 5, 15865 (2015).

    Google Scholar 

  141. Helbig, M. et al. The positive net radiative greenhouse gas forcing of increasing methane emissions from a thawing boreal forest-wetland landscape. Glob. Change Biol. 23, 2413–2427 (2017).

    Google Scholar 

  142. Kokelj, S. V. & Jorgenson, M. T. Advances in thermokarst research. Permafr. Periglac. Process. 24, 108–119 (2013).

    Google Scholar 

  143. Lawrence, D. M., Koven, C., Swenson, S. C., Riley, W. & Slater, A. Permafrost thaw and resulting soil moisture changes regulate projected high-latitude CO2 and CH4 emissions. Environ. Res. Lett. 10, 094011 (2015).

    Google Scholar 

  144. Elberling, B. et al. Long-term CO2 production following permafrost thaw. Nat. Clim. Change 3, 890–894 (2013).

    Google Scholar 

  145. Salmon, V. G. et al. Nitrogen availability increases in a tundra ecosystem during five years of experimental permafrost thaw. Glob. Change Biol. 22, 1927–1941 (2016).

    Google Scholar 

  146. Keuper, F. et al. Experimentally increased nutrient availability at the permafrost thaw front selectively enhances biomass production of deep-rooting subarctic peatland species. Glob. Change Biol. 23, 4257–4266 (2017).

    Google Scholar 

  147. Bintanja, R. & Andry, O. Towards a rain-dominated Arctic. Nat. Clim. Change 7, 263–267 (2017).

    Google Scholar 

  148. Peng, J. et al. Global carbon sequestration is highly sensitive to model-based formulations of nitrogen fixation. Glob. Biogeochem. Cycles 34, e2019GB006296 (2020).

    Google Scholar 

  149. Elmendorf, S. C. et al. Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol. Lett. 15, 164–175 (2012).

    Google Scholar 

  150. Chu, H. & Grogan, P. Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape. Plant Soil 329, 411–420 (2010).

    Google Scholar 

  151. Zhang, W. et al. Tundra shrubification and tree-line advance amplify arctic climate warming: results from an individual-based dynamic vegetation model. Environ. Res. Lett. 8, 034023 (2013).

    Google Scholar 

  152. Abbott, B. W. et al. Biomass offsets little or none of permafrost carbon release from soils, streams, and wildfire: an expert assessment. Environ. Res. Lett. 11, 034014 (2016).

    Google Scholar 

  153. Christensen, T. R., Michelsen, A. & Jonasson, S. Exchange of CH4 and N2O in a subarctic heath soil: effects of inorganic N and P and amino acid addition. Soil Biol. Biochem. 31, 637–641 (1999).

    Google Scholar 

  154. Liu, X., Zhang, Q., Li, S., Zhang, L. & Ren, J. Simulated NH4 +-N deposition inhibits CH4 uptake and promotes N2O emission in the meadow Steppe of inner Mongolia, China. Pedosphere 27, 306–317 (2017).

    Google Scholar 

  155. Wang, P. et al. Sea animal activity controls CO2, CH4 and N2O emission hotspots on South Georgia, sub-Antarctica. Soil Biol. Biochem. 132, 174–186 (2019).

    Google Scholar 

  156. Walker, X. J. et al. Cross-scale controls on carbon emissions from boreal forest megafires. Glob. Change Biol. 24, 4251–4265 (2018).

    Google Scholar 

  157. Young, A. M., Higuera, P. E., Duffy, P. A. & Hu, F. S. Climatic thresholds shape northern high-latitude fire regimes and imply vulnerability to future climate change. Ecography 40, 606–617 (2017).

    Google Scholar 

  158. Jiang, Y. et al. Modeling carbon–nutrient interactions during the early recovery of tundra after fire. Ecol. Appl. 25, 1640–1652 (2015).

    Google Scholar 

  159. Bret-Harte, M. S. et al. The response of Arctic vegetation and soils following an unusually severe tundra fire. Philos. Trans. R. Soc. B Biol. Sci. 368, 20120490 (2013).

    Google Scholar 

  160. Strauss, J. et al. Deep Yedoma permafrost: a synthesis of depositional characteristics and carbon vulnerability. Earth-Sci. Rev. 172, 75–86 (2017).

    Google Scholar 

  161. Wilkerson, J. et al. Permafrost nitrous oxide emissions observed on a landscape scale using the airborne eddy-covariance method. Atmos. Chem. Phys. 19, 4257–4268 (2019). The first study reporting N 2O emissions at the landscape scale over Arctic Alaska using an airborne eddy covariance system.

    Google Scholar 

  162. Obu, J. et al. Northern Hemisphere permafrost map based on TTOP modelling for 2000–2016 at 1 km2 scale. Earth-Sci. Rev. 193, 299–316 (2019).

    Google Scholar 

  163. Zoltai, S. C. & Tarnocai, C. Perennially frozen peatlands in the western Arctic and Subarctic of Canada. Can. J. Earth Sci. 12, 28–43 (1975).

    Google Scholar 

  164. Schreiber, F., Wunderlin, P., Udert, K. M. & Wells, G. F. Nitric oxide and nitrous oxide turnover in natural and engineered microbial communities: biological pathways, chemical reactions, and novel technologies. Front. Microbiol. 3, 372 (2012).

    Google Scholar 

  165. Voigt, C. et al. Nitrous oxide fluxes from permafrost regions. PANGAEA, https://doi.org/10.1594/PANGAEA.919217 (2020).

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Acknowledgements

We wish to acknowledge funding from the Academy of Finland/Russian Foundation for Basic Research project NOCA (decision no. 314630) and the Yedoma-N project (General Research Grant from the Academy of Finland, decision number 287469). C.V. was funded by the Canada Research Chair in Atmospheric Biogeosciences at High Latitudes (awarded to O.S.) and the Global Water Futures project Northern Water Futures. B.E. was supported by the Danish National Research Foundation (Center for Permafrost, CENPERM DNRF100), S.D.S. was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant, the Polar Continental Shelf Program (PCSP) and the International Polar Year (IPY) project CiCAT. Y.Y. was supported by the National Natural Science Foundation of China (31825006, 31988102 and 91837312) and the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0106 and 2019QZKK0302). We are grateful to Evan J. Wilcox for help in preparing Fig. 1 and to the authors of published N2O flux studies for providing additional site-level information that helped to interpret the flux data.

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Authors and Affiliations

  1. Department of Geography, University of Montreal, Montreal, QC, Canada

    Carolina Voigt & Oliver Sonnentag

  2. Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

    Maija E. Marushchak

  3. Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT, USA

    Benjamin W. Abbott

  4. Department of Environmental and Biological Sciences, University of Eastern Finland, Kuopio, Finland

    Christina Biasi & Pertti J. Martikainen

  5. Center for Permafrost (CENPERM), Department of Geosciences and Natural Resource Management, University of Copenhagen, Copenhagen, Denmark

    Bo Elberling

  6. Department of Soil Science, University of Saskatchewan, Saskatoon, SK, Canada

    Steven D. Siciliano & Katherine J. Stewart

  7. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Yuanhe Yang

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Contributions

P.J.M. initiated the study. P.J.M., C.V., M.E.M. and C.B. conducted the literature review. C.V. and P.J.M. wrote an outline of the manuscript, with contributions from M.E.M., C.B., B.W.A., B.E., O.S. and Y.Y. C.V. wrote the first version of the manuscript, after which all co-authors provided input on the manuscript text, figures and discussion of scientific content.

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Correspondence to Carolina Voigt.

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Nature Reviews Earth & Environment thanks Klaus Butterbach-Bahl, Jens Strauss and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Glossary

Permafrost

Ground that remains continuously frozen for at least two consecutive years.

Mesocosm

Intact plant–soil systems in laboratories meant to mimic near-field conditions.

Nitrite reductase

Enzyme catalysing the reduction of nitrite (NO2−) to nitric oxide (NO).

Greening

Increase in ‘greenness’ caused by warming-induced increase in shrub cover and height.

Browning

Decrease in greenness caused by warming and extreme events, wildfires, thermokarst erosion and insect outbreaks.

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Voigt, C., Marushchak, M.E., Abbott, B.W. et al. Nitrous oxide emissions from permafrost-affected soils. Nat Rev Earth Environ 1, 420–434 (2020). https://doi.org/10.1038/s43017-020-0063-9

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