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.

Hot moment of N2O emissions in seasonally frozen peatlands

The ISME Journal volume 17, pages 792–802 (2023)Cite this article

Subjects

Abstract

Since the start of the Anthropocene, northern seasonally frozen peatlands have been warming at a rate of 0.6 °C per decade, twice that of the Earth’s average rate, thereby triggering increased nitrogen mineralization with subsequent potentially large losses of nitrous oxide (N2O) to the atmosphere. Here we provide evidence that seasonally frozen peatlands are important N2O emission sources in the Northern Hemisphere and the thawing periods are the hot moment of annual N2O emissions. The flux during the hot moment of thawing in spring was 1.20 ± 0.82 mg N2O m−2 d−1, significantly higher than that during the other periods (freezing, −0.12 ± 0.02 mg N2O m−2 d−1; frozen, 0.04 ± 0.04 mg N2O m−2 d−1; thawed, 0.09 ± 0.01 mg N2O m−2 d−1) or observed for other ecosystems at the same latitude in previous studies. The observed emission flux is even higher than those of tropical forests, the World’s largest natural terrestrial N2O source. Furthermore, based on soil incubation with 15N and 18O isotope tracing and differential inhibitors, heterotrophic bacterial and fungal denitrification was revealed as the main source of N2O in peatland profiles (0–200 cm). Metagenomic, metatranscriptomic, and qPCR assays further revealed that seasonally frozen peatlands have high N2O emission potential, but thawing significantly stimulates expression of genes encoding N2O-producing protein complexes (hydroxylamine dehydrogenase (hao) and nitric oxide reductase (nor)), resulting in high N2O emissions during spring. This hot moment converts seasonally frozen peatlands into an important N2O emission source when it is otherwise a sink. Extrapolation of our data to all northern peatland areas reveals that the hot moment emissions could amount to approximately 0.17 Tg of N2O yr−1. However, these N2O emissions are still not routinely included in Earth system models and global IPCC assessments.

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

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Hot moment of N2O emissions in seasonally frozen peatland.
Fig. 2: Rates and contributions of bacterial, fungal denitrification and nitrification to N2O production in the seasonally frozen peatland.
Fig. 3: N2O production- and reduction-related functional gene transcripts identified in seasonally frozen peatland.
Fig. 4: Metabolic reconstruction and features of N2O production- and reduction-related microorganisms identified in seasonally frozen peatland.

Data availability

The metagenomic data and the metatranscriptomic data were deposited in the NCBI Sequence Read Archive under accession numbers SAMN26424243–SAMN26424272 and SRR14251110–SRR14251136, respectively.

References

  1. Loisel JL, Yu ZC, Beilman DW, Camill P, Alm J, Amesbury MJ, et al. A database and synthesis of northern peatland soil properties and Holocene carbon and nitrogen accumulation. Holocene. 2014;24:1028–42. https://doi.org/10.1177/0959683614538073.

    Article  Google Scholar 

  2. Hugelius G, Loisel J, Chadburn S, Jackson RB, Jones M, MacDonald G, et al. Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw. Proc Natl Acad Sci USA. 2020;117:20438–46. https://doi.org/10.1073/pnas.1916387117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Frolking S, Talbot J, Jones MC, Treat CC, Kauffman JB, Tuittila E-S, et al. Peatlands in the Earth’s 21st century climate system. Environ Rev. 2011;19:371–96. https://doi.org/10.1139/a11-014.

    Article  CAS  Google Scholar 

  4. Yu Z, Loisel JL, Brosseau DP, Beilman DW, Hunt SJ. Global peatland dynamics since the Last Glacial Maximum. Geophys Res Lett. 2010;37:13402. https://doi.org/10.1029/2010GL043584.

    Article  CAS  Google Scholar 

  5. Leifeld J, Menichetti L. The underappreciated potential of peatlands in global climate change mitigation strategies. Nat Commun. 2018;9:1–7. https://doi.org/10.1038/s41467-018-03406-6.

    Article  CAS  Google Scholar 

  6. Zhang T, Barry RG, Knowles K, Ling F, Armstong RL. Distribution of seasonally and perennially frozen ground in the Northern Hemisphere. In: ICOP 2003 Permafrost: proceedings of the 8th International Conference on Permafrost. Netherlands: A.A. Balkma Publishers; 2003. 2, p. 1289–94.

  7. Dai LC, Guo XW, Zhang FW, Du Y, Ke X, Li YK, et al. Seasonal dynamics and controls of deep soil water infiltration in the seasonally frozen region of the Qinghai-Tibet Plateau. J Hydrol. 2019;571:740–8. https://doi.org/10.1016/j.jhydrol.2019.02.021.

    Article  Google Scholar 

  8. Åkerman HJ, Johansson M. Thawing permafrost and thicker active layers in sub-arctic Sweden. Permafr Periglac Process. 2008;19:279–92. https://doi.org/10.1002/ppp.626.

    Article  Google Scholar 

  9. Quinton WL, Baltzer J. The active-layer hydrology of a peat plateau with thawing permafrost (Scotty Creek, Canada). Hydrol J. 2013;21:201–20. https://doi.org/10.1007/s10040-012-0935-2.

  10. Swindles GT, Morris PJ, Mullan D, Watson EJ, Turner TE, Roland TP, et al. The long-term fate of permafrost peatlands under rapid climate warming. Sci Rep. 2015;5:17951. https://doi.org/10.1038/srep17951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Marushchak ME, Kerttula J, Diáková K, Faguet A, Gil J, Grosse G, et al. Thawing Yedoma permafrost is a neglected nitrous oxide source. Nat Commun. 2021;12:1–10. https://doi.org/10.1038/s41467-021-27386-2.

    Article  CAS  Google Scholar 

  12. Kou D, Yang GB, Li F, Feng XH, Zhang DY, Zhang QW, et al. Progressive nitrogen limitation across the Tibetan alpine permafrost region. Nat Commun. 2020;11:3331. https://doi.org/10.1038/s41467-020-17169-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Voigt C, Marushchak ME, Abbott BW, Biasi C, Elberling B, Siciliano SD, et al. Nitrous oxide emissions from permafrost-affected soils. Nat Rev Earth Environ. 2020;1:420–34. https://doi.org/10.1038/s43017-020-0063-9.

    Article  CAS  Google Scholar 

  14. Larmola T, Leppänen SM, Tuittila E-S, Aarva M, Merilä P, Fritze H, et al. Methanotrophy induces nitrogen fixation during peatland development. Proc Natl Acad Sci USA. 2014;111:734–9. https://doi.org/10.1073/pnas.131428411.

    Article  CAS  PubMed  Google Scholar 

  15. Kox MAR, van den Elzen E, Lamers LPM, Jetten MSM. Microbial nitrogen fixation and methane oxidation are strongly enhanced by light in Sphagnum mosses. AMB Expr. 2020;10:61. https://doi.org/10.1186/s13568-020-00994-9.

    Article  Google Scholar 

  16. de Jong AEE, in’t Zandt MH, Meisel OH, Jetten MSM, Dean JF, Rasigraf O, et al. Increases in temperature and nutrient availability positively affect methane-cycling microorganisms in Arctic thermokarst lake sediments. Environ Microbiol. 2018;20:4314–27. https://doi.org/10.1111/1462-2920.14345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Voigt C, Marushchak ME, Lamprecht RE, Jackowicz-Korczyński M, Lindgren A, Mastepanov M, et al. Increased nitrous oxide emissions from arctic peatlands after permafrost thaw. Proc Natl Acad Sci USA. 2017;114:6238–43. https://doi.org/10.1073/pnas.1702902114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Repo ME, Susiluoto S, Lind SE, Jokinen S, Elsakov V, Biasi C, et al. Large N2O emissions from cryoturbated peat soil in tundra. Nat Geosci. 2009;2:189–92. https://doi.org/10.1038/NGEO434.

    Article  CAS  Google Scholar 

  19. Elberling B, Christiansen HH, Hansen BU. High nitrous oxide production from thawing permafrost. Nat Geosci. 2010;3:332–5. https://doi.org/10.1038/NGEO803.

    Article  CAS  Google Scholar 

  20. Wang JY, Song CC, Hou AX, Miao YQ, Yang GS, Zhang J. Effects of freezing-thawing cycle on peatland active organic carbon fractions and enzyme activities in the Da Xing’anling Mountains, Northeast China. Environ Earth Sci. 2014;72:1853–60. https://doi.org/10.1007/s12665-014-3094-z.

    Article  CAS  Google Scholar 

  21. Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Pean C, Berger S, et al., editors. and Intergovernmental Panel on Climate Change (IPCC). IPCC, 2021: Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Open Access. UK, Cambridge: Cambridge University Press; 2021. pp. 2391. https://doi.org/10.1017/9781009157896.

  22. Koven CD, Lawrence DM, Riley WJ. Permafrost carbon climate feedback is sensitive to deep soil carbon decomposability but not deep soil nitrogen dynamics. Proc Natl Acad Sci USA. 2015;112:3752–7. https://doi.org/10.1073/pnas.1415123112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chen LY, Liu L, Mao C, Qin SQ, Wang J, Liu FT, et al. Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency. Nat Commun. 2018;9:1–11. https://doi.org/10.1038/s41467-018-06232-y.

    Article  CAS  Google Scholar 

  24. Salmon VG, Soucy P, Mauritz M, Celis G, Natali SM, Mack MC, et al. Nitrogen availability increases in a tundra ecosystem during five years of experimental permafrost thaw. Glob Change Biol. 2016;22:1927–41. https://doi.org/10.1111/gcb.13204.

    Article  Google Scholar 

  25. Finger RA, Turetsky MR, Kielland K, Ruess RW, Mack MC, Euskirchen ES. Effects of permafrost thaw on nitrogen availability and plant-soil interactions in a boreal Alaskan lowland. J Ecol. 2016;104:1542–54. https://doi.org/10.1111/1365-2745.12639.

    Article  Google Scholar 

  26. Mao C, Kou D, Qin S, Yang YH. Permafrost nitrogen status and its determinants on the Tibetan Plateau. Glob Change Biol. 2020;26:5290–302. https://doi.org/10.1111/gcb.15205.

    Article  Google Scholar 

  27. Congreves KA, Wagner-Riddle C, Si BC, Clough TJ. Nitrous oxide emissions and biogeochemical responses to soil freezing-thawing and drying-wetting. Soil Biol Biochem. 2018;117:5–15. https://doi.org/10.1016/j.soilbio.2017.10.040.

    Article  CAS  Google Scholar 

  28. Frostegård Å, Vick SHW, Lim NYN, Bakken LR, Shapleigh JP. Linking meta-omics to the kinetics of denitrification intermediates reveals pH-dependent causes of N2O emissions and nitrite accumulation in soil. ISME J. 2022;16:26–37. https://doi.org/10.1038/s41396-021-01045-2.

    Article  CAS  PubMed  Google Scholar 

  29. van den Heuvel RN, van der Biezen E, Jetten MS, Hefting MM. Denitrification at pH 4 by a soil-derived Rhodanobacter-dominated community. Environ Microbiol. 2010;12:3264–71. https://doi.org/10.1111/j.1462-2920.2010.02301.x.

    Article  CAS  PubMed  Google Scholar 

  30. Hénault C, Bourennane H, Ayzac A, Ratié C, Saby NPA, Cohan J, et al. Management of soil pH promotes nitrous oxide reduction and thus mitigates soil emissions of this greenhouse gas. Sci Rep. 2019;9:20182 https://doi.org/10.1038/s41598-019-56694-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Jonasson S, Michelsen A, Schmidt IK. Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes. Appl Soil Ecol. 1999;11:135–46. https://doi.org/10.1016/S0929-1393(98)00145-0.

    Article  Google Scholar 

  32. Zhu GB, Wang SY, Wang WD, Wang Y, Zhou LL, Jiang B, et al. Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nat Geosci. 2013;6:103–7. https://doi.org/10.1038/NGEO1683.

    Article  CAS  Google Scholar 

  33. Chen LY, Liang JY, Qin SQ, Liu L, Fang K, Xu YP, et al. Determinants of carbon release from the active layer and permafrost deposits on the Tibetan Plateau. Nat Commun. 2016;7:13046. https://doi.org/10.1038/ncomms13046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ding JZ, Chen LY, Ji CJ, Hugelius G, Li YN, Li L, et al. Decadal soil carbon accumulation across Tibetan permafrost regions. Nat Geosci. 2017;10:420–4. https://doi.org/10.1038/NGEO2945.

    Article  CAS  Google Scholar 

  35. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, et al. Molecular mechanism of anaerobic ammonium oxidation. Nature. 2011;479:127–30. https://doi.org/10.1038/nature10453.

    Article  CAS  PubMed  Google Scholar 

  36. Song CC, Xu XF, Tian HQ, Wang YY. Ecosystem–atmosphere exchange of CH4 and N2O and ecosystem respiration in wetlands in the Sanjiang Plain, Northeastern China. Glob Change Biol. 2009;15:692–705. https://doi.org/10.1111/j.1365-2486.2008.01821.x.

    Article  Google Scholar 

  37. Butterbach-Bahl K, Baggs EM, 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. 2013;368:20130122. https://doi.org/10.1098/rstb.2013.0122.

    Article  CAS  Google Scholar 

  38. Palmer K, Biasi C, Horn MA. Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J. 2012;6:1058–77. https://doi.org/10.1038/ismej.2011.172.

    Article  CAS  PubMed  Google Scholar 

  39. Siciliano SD, Ma WK, Ferguson S, Farrell RE. Nitrifier dominance of Arctic soil nitrous oxide emissions arises due to fungal competition with denitrifiers for nitrate. Soil Biol Biochem. 2009;41:1104–10. https://doi.org/10.1016/j.soilbio.2009.02.024.

    Article  CAS  Google Scholar 

  40. Kool DM, Wrage N, Zechmeister-Boltenstern S, Pfeffer M, Brus D, Oenema O, et al. Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labelling method. Eur J Soil Sci. 2010;61:759–72. https://doi.org/10.1111/j.1365-2389.2010.01270.x.

    Article  CAS  Google Scholar 

  41. Kool DM, Dolfing J, Wrage N, Groenigen JWV. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem. 2011;43:174–8. https://doi.org/10.1016/j.soilbio.2010.09.030.

    Article  CAS  Google Scholar 

  42. Zhu X, Burger M, Doane TA, Horwath WR. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc Natl Acad Sci USA. 2013;110:6328–33. https://doi.org/10.1073/pnas.1219993110.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Chen HH, Mothapo NV, Shi W. The significant contribution of fungi to soil N2O production across diverse ecosystems. Appl Soil Ecol. 2014;73:70–77. https://doi.org/10.1016/j.apsoil.2013.08.011.

    Article  Google Scholar 

  44. Aldossari N, Ishii A. Fungal denitrification revisited-Recent advancements and future opportunities. Soil Biol Biochem. 2021;157:108250. https://doi.org/10.1016/j.soilbio.2021.108250.

    Article  CAS  Google Scholar 

  45. Xu XZ, Xu Y, Chen SC, Xu SG, Zhang HW. Soil loss and conservation in the black soil region of Northeast China: a retrospective study. Environ Sci Policy. 2010;13:793–800. https://doi.org/10.1016/j.envsci.2010.07.004.

    Article  CAS  Google Scholar 

  46. Li H, Pei JB, Wang JK, Li SY, Gao GW. Organic carbon density and storage of the major black soil regions in Northeast China. J Soil Sci Plant Nut. 2013;13:883–93. https://doi.org/10.4067/S0718-95162013005000070.

    Article  CAS  Google Scholar 

  47. Wang BW, Zhao XL, Wang X, Zhang ZX, Yi L, Hu SG. Spatial and temporal variability of soil erosion in the black soil region of Northeast China from 2000 to 2015. Environ Monit Assess. 2020;192:1–14. https://doi.org/10.1007/s10661-020-08298-y.

    Article  CAS  Google Scholar 

  48. Ma X, Yin C, Wen B, Wang M, Wang G, Wang D, et al. The carbon reserves and emissions of peatlands in China, estimation of organic carbon reserves of peatlands in China. Beijing: Chinese Forestry Press; 2013.

  49. Wang M, Wang SZ, Cao YW, Jiang M, Wang GD, Dong YM. The effects of hummock-hollow microtopography on soil organic carbon stocks and soil labile organic carbon fractions in a sedge peatland in Changbai Mountain, China. Catena. 2021;201:105204. https://doi.org/10.1016/j.catena.2021.105204.

    Article  CAS  Google Scholar 

  50. Yang W, Zhao H, Chen XL, Yin SL, Cheng XL, An SQ. Consequences of short-term C4 plant Spartina alterniflora invasions for soil organic carbon dynamics in a coastal wetland of Eastern China. Ecol Eng. 2013;61:50–57. https://doi.org/10.1016/j.ecoleng.2013.09.056.

    Article  Google Scholar 

  51. Zhu GB, Wang SY, Wang C, Zhou LG, Zhao SY, Li YX, et al. Resuscitation of anammox bacteria after >10,000 years of dormancy. ISME J. 2019;13:1098–109. https://doi.org/10.1038/s41396-018-0316-5.

    Article  CAS  PubMed  Google Scholar 

  52. Zhao SY, Wang XM, Pan HW, Wang SY, Zhu GB. High N2O reduction potential by denitrification in the nearshore site of a riparian zone. Sci Total Environ. 2022;813:152458. https://doi.org/10.1016/j.scitotenv.2021.152458.

    Article  CAS  PubMed  Google Scholar 

  53. Reck M, Tomasch J, Deng ZL, Jarek M, Husemann P, Wagner-Döbler I, et al. Stool metatranscriptomics: a technical guideline for mRNA stabilisation and isolation. BMC Genomics. 2015;16:494. https://doi.org/10.1186/s12864-015-1694-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wang XM, Wang SY, Jiang YY, Zhou JM, Han C, Zhu GB. Comammox bacterial abundance, activity, and contribution in agricultural rhizosphere soils. Sci Total Environ. 2020;727:138563. https://doi.org/10.1016/j.scitotenv.2020.138563.

    Article  CAS  PubMed  Google Scholar 

  55. He BS, Zhu RR, Yang HD, Lu QQ, Wang WW, Song L, et al. Assessing the impact of data preprocessing on analyzing next generation sequencing data. Front Bioeng Biotechnol. 2020;8:817. https://doi.org/10.3389/fbioe.2020.00817.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Sun X, Kop LFM, Lau MCY, Frank J, Jayakumar A, Lücker S, et al. Uncultured Nitrospina-like species are major nitrite oxidizing bacteria in oxygen minimum zones. ISME J. 2019;13:2391–402. https://doi.org/10.1038/s41396-019-0443-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512. https://doi.org/10.1038/nprot.2013.084.

    Article  CAS  PubMed  Google Scholar 

  58. Fu LM, Niu BF, Zhu ZW, Wu ST, Li WZ. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28:3150–2. https://doi.org/10.1093/bioinformatics/bts565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Peng, Y, Leung HCM, Yiu SM, Chin FYL. IDBA - A practical iterative de bruijn graph De Novo assembler. In: Annual International Conference on Research in Computational Molecular Biology Lisbon. 6044, 426–40 (2010). https://doi.org/10.1007/978-3-642-12683-3_28

  60. Zhu W, Lomsadze A, Borodovsky M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 2010;38:132–132. https://doi.org/10.1093/nar/gkq275.

    Article  CAS  Google Scholar 

  61. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–60. https://doi.org/10.1038/NMETH.1923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Tu QC, Lin L, Cheng L, Deng Y, He ZL. NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics. 2019;35:1040–8. https://doi.org/10.1093/bioinformatics/bty741.

    Article  CAS  PubMed  Google Scholar 

  63. Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-A flexible pipeline for genome-resolved metagenomic data analysis. Microbiome. 2018;6:1–13. https://doi.org/10.1186/s40168-018-0541-1b.

    Article  Google Scholar 

  64. Li D, Liu C, Luo R, Sadakane K, Lam T. MEGAHIT: An Ultra-fast single-node solution for large and complex metagenomics assembly via succinct de bruijn graph. Bioinformatics. 2015;31:1674–6. https://doi.org/10.1093/bioinformatics/btv033.

    Article  CAS  PubMed  Google Scholar 

  65. Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. Peer J. 2019;7:7359. https://doi.org/10.7717/peerj.7359.

    Article  Google Scholar 

  66. Wu Y, Simmons BA, Singer SW. MaxBin 2.0: An Automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7. https://doi.org/10.1093/bioinformatics/btv638.

    Article  CAS  PubMed  Google Scholar 

  67. Alneberg J, Bjarnason BS, de Bruijin I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6. https://doi.org/10.1038/nmeth.3103.

    Article  CAS  PubMed  Google Scholar 

  68. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55. https://doi.org/10.1101/gr.186072.114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004. https://doi.org/10.1038/nbt.4229.

    Article  CAS  PubMed  Google Scholar 

  70. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–9. https://doi.org/10.1038/nmeth.4197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Bastian M. Gephi: an open source software for exploring and manipulating networks. In: Third international AAAI conference on weblogs and social media. 2009, vol 8, p. 361–2. https://doi.org/10.13140/2.1.1341.1520.

  72. Hu H, Chen D, He J. Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev. 2015;39:729–49. https://doi.org/10.1093/femsre/fuv021.

    Article  CAS  PubMed  Google Scholar 

  73. Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;88:1386–94. https://doi.org/10.1890/06-0219.

    Article  PubMed  Google Scholar 

  74. Speth D, in’t Zandt MH, Guerrero-Cruz S, Dutilh BE, Jetten MSM. Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system. Nat Commun. 2016;7:11172. https://doi.org/10.1038/ncomms11172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Pessi, IS, Viitamäki S, Rasimus EE, Delmont TO, Luoto M, Hultman J. Truncated denitrifiers dominate the denitrification pathway in tundra soil metagenomes. bioRxiv. 2020;419267. https://doi.org/10.1101/2020.12.21.419267.

  76. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA. 2011;108:15892–7. https://doi.org/10.1073/pnas.110719610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Peng YZ, Zhu GB. Biological nitrogen removal with nitrification and denitrification via nitrite pathway. Appl Microbiol Biotechnol. 2006;73:15–26. https://doi.org/10.1007/s00253-006-0534-z.

    Article  CAS  PubMed  Google Scholar 

  78. Werner C, Butterbach-Bahl K, Hass E, Hickler T, Kiese R. A global inventory of N2O emissions from tropical rainforest soils using a detailed biogeochemical model. Global Biogeochem Cy. 2007;21:GB3010. https://doi.org/10.1029/2006GB002909.

    Article  CAS  Google Scholar 

  79. Harriss RC, Gorham E, Sebacher DI, Bartlett KB, Flebbe PA. Methane flux from northern peatlands. Nature. 1985;315:652–4. https://doi.org/10.1038/315652a0.

    Article  CAS  Google Scholar 

  80. Martikainen P, Nykänen H, Crill P, Silvola J. Effect of a lowered water table on nitrous oxide fluxes from northern peatlands. Nature. 1993;366:51–53. https://doi.org/10.1038/366051a0.

    Article  CAS  Google Scholar 

  81. Liimatainen M, Voigt C, Martikainen PJ, Hytönen J, Regina K, Óskarsson H, et al. Factors controlling nitrous oxide emissions from managed northern peat soils with low carbon to nitrogen ratio. Soil Biol Biochem. 2018;122:186–95. https://doi.org/10.1016/j.soilbio.2018.04.006.

    Article  CAS  Google Scholar 

  82. Tian HQ, Xu RT, Canadell JG, Thompson RL, Winiwarter W, Suntharalingam P, et al. A comprehensive quantification of global nitrous oxide sources and sinks. Nature. 2020;586:248–56. https://doi.org/10.1038/s41586-020-2780-0.

    Article  CAS  PubMed  Google Scholar 

  83. Gil J, Pérez T, Boering K, Martikainen PJ, Biasi C. Mechanisms responsible for high N2O emissions from subarctic permafrost peatlands studied via stable isotope techniques. Global Biogeochem Cy. 2017;31:172–89. https://doi.org/10.1002/2015GB005370.

    Article  CAS  Google Scholar 

  84. Siljanen HMP, Alves RJE, Ronkainen JG, Lamprecht RE, Bhattarai HR, Bagnoud A, et al. Archaeal nitrification is a key driver of high nitrous oxide emissions from arctic peatlands. Soil Biol Biochem. 2019;137:107539. https://doi.org/10.1016/j.soilbio.2019.107539.

    Article  CAS  Google Scholar 

  85. Kozlowski J, Stieglmeier M, Schleper C, Klotz MG, Stein LY. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J. 2016;10:1836–45. https://doi.org/10.1038/ismej.2016.2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Clymo RS, Hayward PM. The ecology of sphagnum. In: Bryophyte Ecology. Springer Netherlands; 1982, p. 229–89. https://doi.org/10.1007/978-94-009-5891-3_8.

  87. Malmer N, Svensson BM, Wallén B. Interactions between sphagnum mosses and field layer vascular plants in the development of peat-forming systems. Folia Geobot Phytotaxonomica. 1994;29:483–96. https://doi.org/10.1007/BF02883146.

    Article  Google Scholar 

  88. Morley N, Baggs EM, Dörsch P, Bakken L. Production of NO, N2O and N2 by extracted soil bacteria, regulation by NO2- and O2 concentrations. FEMS Microbiol Ecol. 2008;65:102–12. https://doi.org/10.1111/j.1574-6941.2008.00495.x.

    Article  CAS  PubMed  Google Scholar 

  89. Senbayram M, Chen R, Budai A, Bakken L, Dittert K. N2O emission and the N2O/(N2O+N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations. Agr Ecosyst Environ. 2012;147:4–12. https://doi.org/10.1016/j.agee.2011.06.022.

    Article  CAS  Google Scholar 

  90. Chen SM, Wang FH, Zhang YM, Qin SP, Wei SC, Wang SQ, et al. Organic carbon availability limiting microbial denitrification in the deep vadose zone. Environ Microbiol. 2018;20:980–92. https://doi.org/10.1111/1462-2920.14027.

    Article  CAS  PubMed  Google Scholar 

  91. Yang GB, Peng YF, Marushchak ME, Chen YL, Wang GQ, Li F, et al. Magnitude and pathways of increased nitrous oxide emissions from uplands following permafrost thaw. Environ Sci Technol. 2018;52:9162–9. https://doi.org/10.1021/acs.est.8b02271.

    Article  CAS  PubMed  Google Scholar 

  92. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria, K L, et al. Metagenomic analysis of permafrost microbial community response to thaw. Nature. 2011;480:368–71. https://doi.org/10.1038/nature10576.

    Article  CAS  PubMed  Google Scholar 

  93. Hazard C, Prosser JI, Nicol GW. Use and abuse of potential rates in soil microbiology. Soil Biol Biochem. 2021;157:108242. https://doi.org/10.1016/j.soilbio.2021.108242.

    Article  CAS  Google Scholar 

  94. Monteux S, Keuper F, Fontaine S, Gavazov K, Hallin S, Juhanson J, et al. Carbon and nitrogen cycling in Yedoma permafrost controlled by microbial functional limitations. Nat Geosci. 2020;13:794–8. https://doi.org/10.1038/s41561-020-00662-4.

    Article  CAS  Google Scholar 

  95. Turetsky M, Wieder K, Halsey L, Vitt D. Current disturbance and the diminishing peatland carbon sink. Geophys Res Lett. 2002;29:11 https://doi.org/10.1029/2001GL014000.

    Article  Google Scholar 

  96. Cui Q, Song C, Wang X, Shi F, Yu X, Tan W. Effects of warming on N2O fluxes in a boreal peatland of Permafrost region, Northeast China. Sci Total Environ. 2018;616-617:427–34. https://doi.org/10.1016/j.scitotenv.2017.10.246.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Mr. Dachun Zhu, Mr. Bangrui Lan, Mr. Longbin Yu, Mr. Shiguang Liu, Mr. Yuantao Wang, Mr. Libo Sun, and Miss. Gawhar Armanbek for sampling peatland soil cores in Antu. This research was financially supported by the National Natural Science Foundation of China (Nos. 91851204 and 92251304), Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2017BT01Z176), National Key R&D Program (2016YFA0602303), and special fund from the State Key Joint Laboratory of Environment Simulation and Pollution Control (Research Center for Eco-environmental Sciences, Chinese Academy of Sciences) (18Z02ESPCR). The author GZ gratefully acknowledges the Program of the Youth Innovation Promotion Association of Chinese Academy of Sciences.

Author information

Authors and Affiliations

  1. Key Laboratory of Drinking Water Science and Technology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085, Beijing, China

    Xiaomin Wang, Shanyun Wang & Guibing Zhu

  2. University of Chinese Academy of Sciences, 100049, Beijing, China

    Xiaomin Wang & Guibing Zhu

  3. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, 100093, Beijing, China

    Yuanhe Yang

  4. Schiller Institute for Integrated Science and Society, Department of Earth and Environmental Sciences, Boston College, Boston, Chestnut Hill, MA 02467, USA

    Hanqin Tian

  5. Department of Microbiology, Radboud University Nijmegen, Nijmegen, The Netherlands

    Mike S. M. Jetten

  6. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China

    Changchun Song

Authors
  1. Xiaomin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shanyun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuanhe Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hanqin Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mike S. M. Jetten
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Changchun Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guibing Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GZ designed the project. XW, GZ, and SW contributed to sample analysis. XW and GZ wrote the manuscript with contributions from SW, YY, HT, MSMJ, and CS. All authors discussed and interpreted the results and contributed to the manuscript. All authors discussed and commented on the manuscript. Correspondence and requests for materials should be addressed to GZ. (gbzhu@rcees.ac.cn).

Corresponding author

Correspondence to Guibing Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Wang, S., Yang, Y. et al. Hot moment of N2O emissions in seasonally frozen peatlands. ISME J 17, 792–802 (2023). https://doi.org/10.1038/s41396-023-01389-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-023-01389-x

Search

Advanced search

Quick links