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The Effects of N Enrichment on Microbial Cycling of Non-CO2 Greenhouse Gases in Soils—a Review and a Meta-analysis

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Abstract

Terrestrial ecosystems are typically nitrogen (N) limited, but recent years have witnessed N enrichment in various soil ecosystems caused by human activities such as fossil fuel combustion and fertilizer application. This enrichment may alter microbial processes in soils in a way that would increase the emissions of methane (CH4) and nitrous oxide (N2O), thereby aggravating global climate change. This review focuses on the effects of N enrichment on methanogens and methanotrophs, which play a central role in the dynamics of CH4 at the global scale. We also address the effects of N enrichment on N2O, which is produced in soils mainly by nitrification and denitrification. Overall, N enrichment inhibits methanogenesis in pure culture experiments, while its effects on CH4 oxidation are more complicated. The majority of previous studies reported that N enrichment, especially NH4+ enrichment, inhibits CH4 oxidation, resulting in higher CH4 emissions from soils. However, both activation and neutral responses have also been reported, particularly in rice paddies and landfill sites, which is well reflected in our meta-analysis. In contrast, N enrichment substantially increases N2O emission by both nitrification and denitrification, which increases proportionally to the amount of N amended. Future studies should address the effects of N enrichment on the active microbes of those functional groups at multiple scales along with parameterization of microbial communities for the application to climate models at the global scale.

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References

  1. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  2. Soong JL, Fuchslueger L, Maranon-Jimenez S, Torn MS, Janssens IA, Penuelas J, Richter A (2020) Microbial carbon limitation: the need for integrating microorganisms into our understanding of ecosystem carbon cycling. Glob Chang Biol 26:1953–1961. https://doi.org/10.1111/gcb.14962

    Article  Google Scholar 

  3. Kanakidou M, Myriokefalitakis S, Daskalakis N, Fanourgakis G, Nenes A, Baker AR, Tsigaridis K, Mihalopoulos N (2016) Past, present, and future atmospheric nitrogen deposition. J Atmos Sci 73:2039–2047. https://doi.org/10.1175/jas-d-15-0278.1

    Article  CAS  Google Scholar 

  4. Dijkstra FA, Blumenthal D, Morgan JA, Pendall E, Carrillo Y, Follett RF (2010) Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland. New Phytol 187:426–437. https://doi.org/10.1111/j.1469-8137.2010.03293.x

    Article  CAS  Google Scholar 

  5. Butler SM, Melillo JM, Johnson JE, Mohan J, Steudler PA, Lux H, Burrows E, Smith RM, Vario CL, Scott L, Hill TD, Aponte N, Bowles F (2012) Soil warming alters nitrogen cycling in a New England forest: implications for ecosystem function and structure. Oecologia 168:819–828. https://doi.org/10.1007/s00442-011-2133-7

    Article  CAS  Google Scholar 

  6. Schleppi P, Korner C, Klein T (2019) Increased nitrogen availability in the soil under mature Picea abies trees exposed to elevated CO2 concentrations. Front Forests Glob Chang 2. https://doi.org/10.3389/ffgc.2019.00059

  7. Sinha E, Michalak AM, Balaji V (2017) Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357:405–408. https://doi.org/10.1126/science.aan2409

    Article  CAS  Google Scholar 

  8. Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  9. Tian H, Chen G, Lu C, Xu X, Ren W, Zhang B, Banger K, Tao B, Pan S, Liu M (2015) Global methane and nitrous oxide emissions from terrestrial ecosystems due to multiple environmental changes. Ecosyst Health Sustain 1:1–20

    Article  Google Scholar 

  10. Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque JF, Langenfelds RL, Le Quere C, Naik V, O’Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, van der Werf GR, Voulgarakis A, van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823. https://doi.org/10.1038/ngeo1955

    Article  CAS  Google Scholar 

  11. Toet S, Ineson P, Peacock S, Ashmore M (2011) Elevated ozone reduces methane emissions from peatland mesocosms. Glob Chang Biol 17:288–296. https://doi.org/10.1111/j.1365-2486.2010.02267.x

    Article  Google Scholar 

  12. Knief C (2015) Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.01346

  13. Dutaur L, Verchot LV (2007) A global inventory of the soil CH4 sink. Glob Biogeochem Cycle 21

  14. Le Mer J, Roger P (2001) Production, oxidation, emission and consumption of methane by soils: a review. Eur J Soil Biol 37:25–50. https://doi.org/10.1016/s1164-5563(01)01067-6

    Article  Google Scholar 

  15. Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol 69:5483–5491. https://doi.org/10.1128/aem.69.9.5483-5491.2003

    Article  CAS  Google Scholar 

  16. Eller G, Kanel LK, Kruger M (2005) Cooccurrence of aerobic and anaerobic methane oxidation in the water column of lake plusssee. Appl Environ Microbiol 71:8925–8928. https://doi.org/10.1128/aem.71.12.8925-8928.2005

    Article  CAS  Google Scholar 

  17. Nunoura T, Inagaki F, Delwiche ME, Colwell FS, Takai K (2008) Subseafloor microbial communities in methane hydrate-bearing sediment at two distinct locations (ODP Leg204) in the Cascadia Margin. Microbes Environ 23:317–325. https://doi.org/10.1264/jsme2.ME08514

    Article  Google Scholar 

  18. Kozlowski JA, Price J, Stein LY (2014) Revision of N2O-producing pathways in the ammonia-oxidizing bacterium Nitrosomonas europaea ATCC 19718. Appl Environ Microbiol 80:4930–4935. https://doi.org/10.1128/aem.01061-14

    Article  Google Scholar 

  19. Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732. https://doi.org/10.1016/s0038-0717(01)00096-7

    Article  CAS  Google Scholar 

  20. Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–1146. https://doi.org/10.1038/ismej.2013.220

    Article  CAS  Google Scholar 

  21. Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY (2016) Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J 10:1836–1845. https://doi.org/10.1038/ismej.2016.2

    Article  CAS  Google Scholar 

  22. Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45. https://doi.org/10.1111/j.1747-0765.2007.00195.x

    Article  CAS  Google Scholar 

  23. Braker G, Zhou JZ, Wu LY, Devol AH, Tiedje JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific northwest marine sediment communities. Appl Environ Microbiol 66:2096–2104. https://doi.org/10.1128/aem.66.5.2096-2104.2000

    Article  CAS  Google Scholar 

  24. Lu CQ, Tian HQ (2013) Net greenhouse gas balance in response to nitrogen enrichment: perspectives from a coupled biogeochemical model. Glob Chang Biol 19:571–588. https://doi.org/10.1111/gcb.12049

    Article  Google Scholar 

  25. Song XZ, Peng CH, Ciais P, Li Q, Xiang WH, Xiao WF, Zhou GM, Deng L (2020) Nitrogen addition increased CO2 uptake more than non-CO2 greenhouse gases emissions in a Moso bamboo forest. Sci Adv 6. https://doi.org/10.1126/sciadv.aaw5790

  26. Liu LL, Greaver TL (2009) A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecol Lett 12:1103–1117. https://doi.org/10.1111/j.1461-0248.2009.01351.x

    Article  CAS  Google Scholar 

  27. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x

    Article  Google Scholar 

  28. Bell TH, Klironomos JN, Henry HAL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J 74:820–828. https://doi.org/10.2136/sssaj2009.0036

    Article  CAS  Google Scholar 

  29. Wang C, Liu DW, Bai E (2018) Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol Biochem 120:126–133. https://doi.org/10.1016/j.soilbio.2018.02.003

    Article  CAS  Google Scholar 

  30. Lu M, Zhou XH, Luo YQ, Yang YH, Fang CM, Chen JK, Li B (2011) Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agric Ecosyst Environ 140:234–244. https://doi.org/10.1016/j.agee.2010.12.010

    Article  CAS  Google Scholar 

  31. Zhang TA, Chen HYH, Ruan HH (2018) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825. https://doi.org/10.1038/s41396-018-0096-y

    Article  CAS  Google Scholar 

  32. Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms-a review. Soil Biol Biochem 75:54–63. https://doi.org/10.1016/j.soilbio.2014.03.023

    Article  CAS  Google Scholar 

  33. Bodelier PLE, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol Ecol 47:265–277. https://doi.org/10.1016/s0168-6496(03)00304-0

    Article  CAS  Google Scholar 

  34. Adamsen APS, King GM (1993) Methane consumption in temperate and subarctic forest soils: rates, vertical zonation, and responses to water and nitrogen. Appl Environ Microbiol 59:485–490. https://doi.org/10.1128/aem.59.2.485-490.1993

    Article  CAS  Google Scholar 

  35. Mochizuki Y, Koba K, Yoh M (2012) Strong inhibitory effect of nitrate on atmospheric methane oxidation in forest soils. Soil Biol Biochem 50:164–166. https://doi.org/10.1016/j.soilbio.2012.03.013

    Article  CAS  Google Scholar 

  36. Jang I, Lee S, Zoh KD, Kang H (2011) Methane concentrations and methanotrophic community structure influence the response of soil methane oxidation to nitrogen content in a temperate forest. Soil Biol Biochem 43:620–627. https://doi.org/10.1016/j.soilbio.2010.11.032

    Article  CAS  Google Scholar 

  37. Shrestha M, Shrestha PM, Frenzel P, Conrad R (2010) Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. ISME J 4:1545–1556. https://doi.org/10.1038/ismej.2010.89

    Article  CAS  Google Scholar 

  38. Bodelier PLE, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421–424. https://doi.org/10.1038/35000193

    Article  CAS  Google Scholar 

  39. Kravchenko IK (2002) Methane oxidation in boreal peat soils treated with various nitrogen compounds. Plant Soil 242:157–162. https://doi.org/10.1023/a:1019614613381

    Article  CAS  Google Scholar 

  40. Mohanty S, Kollah B, Chaudhary RS, Singh AB, Singh M (2015) Methane uptake in tropical soybean-wheat agroecosystem under different fertilizer regimes. Environ Earth Sci 74:5049–5061. https://doi.org/10.1007/s12665-015-4603-4

    Article  CAS  Google Scholar 

  41. Walkiewicz A, Brzezinska M (2019) Interactive effects of nitrate and oxygen on methane oxidation in three different soils. Soil Biol Biochem 133:116–118. https://doi.org/10.1016/j.soilbio.2019.03.001

    Article  CAS  Google Scholar 

  42. Nyerges G, Han SK, Stein LY (2010) Effects of ammonium and nitrite on growth and competitive fitness of cultivated methanotrophic bacteria. Appl Environ Microbiol 76:5648–5651. https://doi.org/10.1128/aem.00747-10

    Article  CAS  Google Scholar 

  43. Tays C, Guarnieri MT, Sauvageau D, Stein LY (2018) Combined effects of carbon and nitrogen source to optimize growth of proteobacterial methanotrophs. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02239

  44. O’Neill J, Wilkinson J (1977) Oxidation of ammonia by methane-oxidizing bacteria and the effects of ammonia on methane oxidation. Microbiology 100:407–412

    Google Scholar 

  45. Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monomoxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208. https://doi.org/10.1016/0378-1097(95)00311-r

    Article  CAS  Google Scholar 

  46. King GM, Schnell S (1994) Ammonium and nitrite inhibition of methane oxidation by Methylobacter albus BG8 and Methylosinus trichosporium OB3b at low methane concentrations. Appl Environ Microbiol 60:3508–3513. https://doi.org/10.1128/aem.60.10.3508-3513.1994

    Article  CAS  Google Scholar 

  47. Knief C, Dunfield PF (2005) Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7:1307–1317. https://doi.org/10.1111/j.1462-2920.2005.00814.x

    Article  CAS  Google Scholar 

  48. Lee SW, Im J, DiSpirito AA, Bodrossy L, Barcelona MJ, Semrau JD (2009) Effect of nutrient and selective inhibitor amendments on methane oxidation, nitrous oxide production, and key gene presence and expression in landfill cover soils: characterization of the role of methanotrophs, nitrifiers, and denitrifiers. Appl Microbiol Biotechnol 85:389–403. https://doi.org/10.1007/s00253-009-2238-7

    Article  CAS  Google Scholar 

  49. He D, Zhang LY, Dumont MG, He JS, Ren LJ, Chu HY (2019) The response of methanotrophs to additions of either ammonium, nitrate or urea in alpine swamp meadow soil as revealed by stable isotope probing. FEMS Microbiol Ecol 95. https://doi.org/10.1093/femsec/fiz077

  50. Graham DW, Chaudhary JA, Hanson RS, Arnold RG (1993) Factors affecting competition between type I and type II methanotrophs in two organisms, continuous-flow reactors. Microb Ecol 25:1–17

    Article  CAS  Google Scholar 

  51. Mohanty SR, Bodelier PLE, Floris V, Conrad R (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72:1346–1354. https://doi.org/10.1128/aem.72.2.1346-1354.2006

    Article  CAS  Google Scholar 

  52. Noll M, Frenzel P, Conrad R (2008) Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiol Ecol 65:125–132. https://doi.org/10.1111/j.1574-6941.2008.00497.x

    Article  CAS  Google Scholar 

  53. Ho A, de Roy K, Thas O, De Neve J, Hoefman S, Vandamme P, Heylen K, Boon N (2014) The more, the merrier: heterotroph richness stimulates methanotrophic activity. ISME J 8:1945–1948. https://doi.org/10.1038/ismej.2014.74

    Article  Google Scholar 

  54. Krause SMB, Johnson T, Karunaratne YS, Fu YF, Beck DAC, Chistoserdova L, Lidstrom ME (2017) Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions. Proc Natl Acad Sci U S A 114:358–363. https://doi.org/10.1073/pnas.1619871114

    Article  CAS  Google Scholar 

  55. Veraart AJ, Garbeva P, van Beersum F, Ho A, Hordijk CA, Meima-Franke M, Zweers AJ, Bodelier PLE (2018) Living apart together-bacterial volatiles influence methanotrophic growth and activity. ISME J 12:1163–1166. https://doi.org/10.1038/s41396-018-0055-7

    Article  CAS  Google Scholar 

  56. Klüber HD, Conrad R (1998) Effects of nitrate, nitrite, NO and N2O on methanogenesis and other redox processes in anoxic rice field soil. FEMS Microbiol Ecol 25:301–318

    Article  Google Scholar 

  57. Clarens M, Bernet N, Delgenes JP, Moletta R (1998) Effects of nitrogen oxides and denitrification by Pseudomonas stutzeri on acetotrophic methanogenesis by Methanosarcina mazei. FEMS Microbiol Ecol 25:271–276. https://doi.org/10.1016/s0168-6496(98)00008-7

    Article  CAS  Google Scholar 

  58. Roy R, Conrad R (1999) Effect of methanogenic precursors (acetate, hydrogen, propionate) on the suppression of methane production by nitrate in anoxic rice field soil. FEMS Microbiol Ecol 28:49–61. https://doi.org/10.1016/s0168-6496(98)00092-0

    Article  CAS  Google Scholar 

  59. Gulledge J, Schimel JP (1998) Low-concentration kinetics of atmospheric CH4 oxidation in soil and mechanism of NH4+ inhibition. Appl Environ Microbiol 64:4291–4298

    Article  CAS  Google Scholar 

  60. Crill PM, Martikainen PJ, Nykanen H, Silvola J (1994) Tmperature and N fertilization effects on methane oxidation in a drained peatland soil. Soil Biol Biochem 26:1331–1339. https://doi.org/10.1016/0038-0717(94)90214-3

    Article  CAS  Google Scholar 

  61. Bollag J-M, Czlonkowski S (1973) Inhibition of methane formation in soil by various nitrogen-containing compounds. Soil Biol Biochem 5:673–678

    Article  CAS  Google Scholar 

  62. Balderston W, Payne W (1976) Inhibition of methanogenesis in salt marsh sediments and whole-cell suspensions of methanogenic bacteria by nitrogen oxides. Appl Environ Microbiol 32:264–269

    Article  CAS  Google Scholar 

  63. Kim SY, Veraart AJ, Meima-Franke M, Bodelier PLE (2015) Combined effects of carbon, nitrogen and phosphorus on CH4 production and denitrification in wetland sediments. Geoderma 259:354–361. https://doi.org/10.1016/j.geoderma.2015.03.015

    Article  CAS  Google Scholar 

  64. Scholten JCM, van Bodegom PM, Vogelaar J, van Ittersum A, Hordijk K, Roelofsen W, Stams AJM (2002) Effect of sulfate and nitrate on acetate conversion by anaerobic microorganisms in a freshwater sediment. FEMS Microbiol Ecol 42:375–385. https://doi.org/10.1111/j.1574-6941.2002.tb01027.x

    Article  CAS  Google Scholar 

  65. Keller JK, Bauers AK, Bridgham SD, Kellogg LE, Iversen CM (2006) Nutrient control of microbial carbon cycling along an ombrotrophic-minerotrophic peatland gradient. J Geophys Res Biogeosci 111. https://doi.org/10.1029/2005jg000152

  66. Eriksson T, Öquist MG, Nilsson MB (2010) Production and oxidation of methane in a boreal mire after a decade of increased temperature and nitrogen and sulfur deposition. Glob Chang Biol 16:2130–2144. https://doi.org/10.1111/j.1365-2486.2009.02097.x

    Article  Google Scholar 

  67. Juutinen S, Moore TR, Bubier JL, Arnkil S, Humphreys E, Marincak B, Roy C, Larmola T (2018) Long-term nutrient addition increased CH4 emission from a bog through direct and indirect effects. Sci Rep 8:11. https://doi.org/10.1038/s41598-018-22210-2

    Article  CAS  Google Scholar 

  68. de Jong AEE, Guererro-Cruz S, van Diggelen JMH, Vaksmaa A, Lamers LPM, Jetten MSM, Smolders AJP, Rasigraf O (2020) Changes in microbial community composition, activity, and greenhouse gas production upon inundation of drained iron-rich peat soils. Soil Biol Biochem 149. https://doi.org/10.1016/j.soilbio.2020.107862

  69. Philben M, Zheng JQ, Bill M, Heikoop JM, Perkins G, Yang ZM, Wullschleger SD, Graham DE, Gu BH (2019) Stimulation of anaerobic organic matter decomposition by subsurface organic N addition in tundra soils. Soil Biol Biochem 130:195–204. https://doi.org/10.1016/j.soilbio.2018.12.009

    Article  CAS  Google Scholar 

  70. Lee C, Beauchemin KA (2014) A review of feeding supplementary nitrate to ruminant animals: nitrate toxicity, methane emissions, and production performance. Can J Anim Sci 94:557–570. https://doi.org/10.4141/cjas-2014-069

    Article  CAS  Google Scholar 

  71. Yang CJ, Rooke JA, Cabeza I, Wallace RJ (2016) Nitrate and inhibition of ruminal methanogenesis: microbial ecology, obstacles, and opportunities for lowering methane emissions from ruminant livestock. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00132

  72. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Wang JT, Singh BK (2017) Identity of biocrust species and microbial communities drive the response of soil multifunctionality to simulated global change. Soil Biol Biochem 107:208–217. https://doi.org/10.1016/j.soilbio.2016.12.003

    Article  CAS  Google Scholar 

  73. Chen K, Lin Y (1992) Inhibitory effect of ionic nitrogen oxides on methanogenesis of methanol in methanogenic sludge. Proceeding of Asia-Pacific Biochemical Engineering Conference. Springer-Verlage, Tokyo, Japan, pp 839–841

    Google Scholar 

  74. Hirano S, Matsumoto N, Morita M, Sasaki K, Ohmura N (2013) Electrochemical control of redox potential affects methanogenesis of the hydrogenotrophic methanogen Methanothermobacter thermautotrophicus. Lett Appl Microbiol 56:315–321. https://doi.org/10.1111/lam.12059

    Article  CAS  Google Scholar 

  75. Wang H, Fotidis IA, Angelidaki I (2015) Ammonia effect on hydrogenotrophic methanogens and syntrophic acetate-oxidizing bacteria. FEMS Microbiol Ecol 91. https://doi.org/10.1093/femsec/fiv130

  76. Sprott GD, Patel GB (1986) Ammina toxicity in pure cultures of methanogenic bacteria. Syst Appl Microbiol 7:358–363

    Article  CAS  Google Scholar 

  77. Yin QD, Gu MQ, Wu GX (2020) Inhibition mitigation of methanogenesis processes by conductive materials: a critical review. Bioresour Technol 317. https://doi.org/10.1016/j.biortech.2020.123977

  78. Tugtas AE, Pavlostathis SG (2007) Inhibitory effects of nitrogen oxides on a mixed methanogenic culture. Biotechnol Bioeng 96:444–455. https://doi.org/10.1002/bit.21105

    Article  CAS  Google Scholar 

  79. Banihani Q, Sierra-Alvarez R, Field JA (2009) Nitrate and nitrite inhibition of methanogenesis during denitrification in granular biofilms and digested domestic sludges. Biodegradation 20:801–812. https://doi.org/10.1007/s10532-009-9268-9

    Article  CAS  Google Scholar 

  80. Bao Q, Huang Y, Wang F, Nie S, Nicol GW, Yao H, Ding L (2016) Effect of nitrogen fertilizer and/or rice straw amendment on methanogenic archaeal communities and methane production from a rice paddy soil. Appl Microbiol Biotechnol 100:5989–5998

    Article  CAS  Google Scholar 

  81. Donlon BA, Razoflores E, Field JA, Lettinga G (1995) Toxicity of N-substituted aromatics to acetoclastic methanogenic acitivy in granular sludge. Appl Environ Microbiol 61:3889–3893. https://doi.org/10.1128/aem.61.11.3889-3893.1995

    Article  CAS  Google Scholar 

  82. Schimel J (2000) Rice, microbes and methane. Nature 403:375–377. https://doi.org/10.1038/35000325

    Article  CAS  Google Scholar 

  83. Berendse F, Van Breemen N, Rydin H, Buttler A, Heijmans M, Hoosbeek MR, Lee JA, Mitchell E, Saarinen T, Vasander H, Wallen B (2001) Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Glob Chang Biol 7:591–598. https://doi.org/10.1046/j.1365-2486.2001.00433.x

    Article  Google Scholar 

  84. Aulakh MS, Wassmann R, Rennenberg H (2002) Methane transport capacity of twenty-two rice cultivars from five major Asian rice-growing countries. Agric Ecosyst Environ 91:59–71. https://doi.org/10.1016/s0167-8809(01)00260-2

    Article  CAS  Google Scholar 

  85. Saarnio S, Wittenmayer L, Merbach W (2004) Rhizospheric exudation of Eriophorum vaginatum L.-potential link to methanogenesis. Plant Soil 267:343–355. https://doi.org/10.1007/s11104-005-0140-3

    Article  CAS  Google Scholar 

  86. Joabsson A, Christensen TR, Wallen B (1999) Influence of vascular plant photosynthetic rate on CH4 emission from peat monoliths from southern boreal Sweden. Polar Res 18:215–220. https://doi.org/10.1111/j.1751-8369.1999.tb00296.x

    Article  Google Scholar 

  87. Cai ZC, Xing GX, Yan XY, Xu H, Tsuruta H, Yagi K, Minami K (1997) Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilisers and water management. Plant Soil 196:7–14. https://doi.org/10.1023/a:1004263405020

    Article  CAS  Google Scholar 

  88. Schimel JP, Gulledge J (1998) Microbial community structure and global trace gases. Glob Chang Biol 4:745–758. https://doi.org/10.1046/j.1365-2486.1998.00195.x

    Article  Google Scholar 

  89. Banger K, Tian HQ, Lu CQ (2012) Do nitrogen fertilizers stimulate or inhibit methane emissions from rice fields? Glob Chang Biol 18:3259–3267. https://doi.org/10.1111/j.1365-2486.2012.02762.x

    Article  Google Scholar 

  90. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976-U234. https://doi.org/10.1038/nature08465

    Article  CAS  Google Scholar 

  91. Jung MY, Park SJ, Min D, Kim JS, Rijpstra WIC, Damsté JSS, Kim GJ, Madsen EL, Rhee SK (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal croup I.1a from an agricultural soil. Appl Environ Microbiol 77:8635–8647. https://doi.org/10.1128/aem.05787-11

    Article  CAS  Google Scholar 

  92. Hink L, Gubry-Rangin C, Nicol GW, Prosser JI (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12:1084–1093. https://doi.org/10.1038/s41396-017-0025-5

    Article  CAS  Google Scholar 

  93. Hink L, Lycus P, Gubry-Rangin C, Frostegård Å, Nicol GW, Prosser JI, Bakken LR (2017) Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers. Environ Microbiol 19:4882–4896. https://doi.org/10.1111/1462-2920.13914

    Article  CAS  Google Scholar 

  94. Levičnik-Höfferle Š, Nicol GW, Ausec L, Mandić-Mulec I, Prosser JI (2012) Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol Ecol 80:114–123

    Article  Google Scholar 

  95. Zhou X, Fornara D, Wasson EA, Wang DM, Ren GD, Christie P, Jia ZJ (2015) Effects of 44 years of chronic nitrogen fertilization on the soil nitrifying community of permanent grassland. Soil Biol Biochem 91:76–83. https://doi.org/10.1016/j.soilbio.2015.08.031

    Article  CAS  Google Scholar 

  96. Lu L, Han WY, Zhang JB, Wu YC, Wang BZ, Lin XG, Zhu JG, Cai ZC, Jia ZJ (2012) Nitrification of archaeal ammonia oxidizers in acid soils is supported by hydrolysis of urea. ISME J 6:1978–1984. https://doi.org/10.1038/ismej.2012.45

    Article  CAS  Google Scholar 

  97. Chen H, Yin C, Fan X, Ye M, Peng H, Li T, Zhao Y, Wakelin SA, Chu G, Liang Y (2019) Reduction of N2O emission by biochar and/or 3,4-dimethylpyrazole phosphate (DMPP) is closely linked to soil ammonia oxidizing bacteria and nosZI-N2O reducer populations. Sci Total Environ 694:133658

    Article  CAS  Google Scholar 

  98. Zhou X, Wang SW, Ma ST, Zheng XK, Wang ZY, Lu CH (2020) Effects of commonly used nitrification inhibitors-dicyandiamide (DCD), 3,4-dimethylpyrazole phosphate (DMPP), and nitrapyrin-on soil nitrogen dynamics and nitrifiers in three typical paddy soils. Geoderma 380. https://doi.org/10.1016/j.geoderma.2020.114637

  99. Jung J, Yeom J, Kim J, Han J, Lim HS, Park H, Hyun S, Park W (2011) Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res Microbiol 162:1018–1026. https://doi.org/10.1016/j.resmic.2011.07.007

    Article  CAS  Google Scholar 

  100. Duan R, Long XE, Tang YF, Wen J, Su SM, Bai LY, Liu RL, Zeng XB (2018) Effects of different fertilizer application methods on the community of nitrifiers and denitrifiers in a paddy soil. J Soils Sediments 18:24–38. https://doi.org/10.1007/s11368-017-1738-9

    Article  CAS  Google Scholar 

  101. Yang YD, Nie JW, Wang S, Shi LL, Li ZZ, Zeng ZH, Zang HD (2021) Differentiated responses of nirS- and nirK-type denitrifiers to 30 years of combined inorganic and organic fertilization in a paddy soil. Arch Agron Soil Sci 67:79–92. https://doi.org/10.1080/03650340.2020.1714032

    Article  CAS  Google Scholar 

  102. Wang Y, Ji H, Wang R, Guo S (2019) Responses of nitrification and denitrification to nitrogen and phosphorus fertilization: does the intrinsic soil fertility matter? Plant Soil 440:443–456

    Article  CAS  Google Scholar 

  103. Cui PY, Fan FL, Yin C, Song AL, Huang PR, Tang YJ, Zhu P, Peng C, Li TQ, Wakelin SA, Liang YC (2016) Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biol Biochem 93:131–141. https://doi.org/10.1016/j.soilbio.2015.11.005

    Article  CAS  Google Scholar 

  104. Wang JM, Zhang TH, Li LP, Li JW, Feng YM, Lu Q (2017) The patterns and drivers of bacterial and fungal β-diversity in a typical dryland ecosystem of northwest China. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02126

  105. Grave RA, Nicoloso RD, Cassol PC, da Silva MLB, Mezzari MP, Aita C, Wuaden CR (2018) Determining the effects of tillage and nitrogen sources on soil N2O emission. Soil Tillage Res 175:1–12. https://doi.org/10.1016/j.still.2017.08.011

    Article  Google Scholar 

  106. Senbayram M, Well R, Bol R, Chadwick DR, Jones DL, Wu D (2018) Interaction of straw amendment and soil NO3- content controls fungal denitrification and denitrification product stoichiometry in a sandy soil. Soil Biol Biochem 126:204–212. https://doi.org/10.1016/j.soilbio.2018.09.005

    Article  CAS  Google Scholar 

  107. Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychol Bull 86:638

    Article  Google Scholar 

  108. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miler HL (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  109. Benbi DK (2013) Greenhouse gas emissions from agricultural soils: sources and mitigation potential. J Crop Improv 27:752–772

    Article  CAS  Google Scholar 

  110. Shcherbak I, Millar N, Robertson GP (2014) Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A 111:9199–9204. https://doi.org/10.1073/pnas.1322434111

    Article  CAS  Google Scholar 

  111. Sun BF, Zhao H, LÜ YZ, Lu F, Wang XK, (2016) The effects of nitrogen fertilizer application on methane and nitrous oxide emission/uptake in Chinese croplands. J Integr Agric 15:440–450. https://doi.org/10.1016/s2095-3119(15)61063-2

    Article  CAS  Google Scholar 

  112. Wang YJ, Guo JH, Vogt RD, Mulder J, Wang JG, Zhang XS (2018) Soil pH as the chief modifier for regional nitrous oxide emissions: new evidence and implications for global estimates and mitigation. Glob Chang Biol 24:E617–E626. https://doi.org/10.1111/gcb.13966

    Article  Google Scholar 

  113. Shi XZ, Hu HW, Zhu-Barker X, Hayden H, Wang JT, Suter H, Chen DL, He JZ (2017) Nitrifier-induced denitrification is an important source of soil nitrous oxide and can be inhibited by a nitrification inhibitor 3,4-dimethylpyrazole phosphate. Environ Microbiol 19:4851–4865. https://doi.org/10.1111/1462-2920.13872

    Article  CAS  Google Scholar 

  114. Prosser JI, Hink L, Gubry-Rangin C, Nicol GW (2020) Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Glob Chang Biol 26:103–118. https://doi.org/10.1111/gcb.14877

    Article  Google Scholar 

  115. Jung MY, Well R, Min D, Giesemann A, Park SJ, Kim JG, Kim SJ, Rhee SK (2014) Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. ISME J 8:1115–1125. https://doi.org/10.1038/ismej.2013.205

    Article  CAS  Google Scholar 

  116. Shen TL, Stieglmeier M, Dai JL, Urich T, Schleper C (2013) Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol Lett 344:121–129. https://doi.org/10.1111/1574-6968.12164

    Article  CAS  Google Scholar 

  117. Šimek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354. https://doi.org/10.1046/j.1365-2389.2002.00461.x

    Article  Google Scholar 

  118. Raut N, Dörsch P, Sitaula BK, Bakken LR (2012) Soil acidification by intensified crop production in South Asia results in higher N2O/(N2+N2O) product ratios of denitrification. Soil Biol Biochem 55:104–112. https://doi.org/10.1016/j.soilbio.2012.06.011

    Article  CAS  Google Scholar 

  119. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531. https://doi.org/10.1016/j.tim.2012.08.001

    Article  CAS  Google Scholar 

  120. Huang XR, Zhao J, Su J, Jia ZJ, Shi XL, Wright AL, Zhu-Barker X, Jiang XJ (2018) Neutrophilic bacteria are responsible for autotrophic ammonia oxidation in an acidic forest soil. Soil Biol Biochem 119:83–89. https://doi.org/10.1016/j.soilbio.2018.01.016

    Article  CAS  Google Scholar 

  121. Wu YC, Lu L, Wang BZ, Lin XG, Zhu JG, Cai ZC, Yan XY, Jia ZJ (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75:1431–1439. https://doi.org/10.2136/sssaj2010.0434

    Article  CAS  Google Scholar 

  122. Moreno-García B, Guillén M, Quílez D (2020) Greenhouse gas emissions as affected by fertilization type (pig slurry vs. mineral) and soil management in mediterranean rice systems. Agronomy-Basel 10. https://doi.org/10.3390/agronomy10040493

  123. Win AT, Toyota K, Win KT, Motobayashi T, Ookawa T, Hirasawa T, Chen DJ, Lu J (2014) Effect of biogas slurry application on CH4 and N2O emissions, Cu and Zn uptakes by whole crop rice in a paddy field in Japan. Soil Sci Plant Nutr 60:411–422. https://doi.org/10.1080/00380768.2014.899886

    Article  CAS  Google Scholar 

  124. Sasada Y, Win KT, Nonaka R, Win AT, Toyota K, Motobayashi T, Hosomi M, Dingjiang C, Lu J (2011) Methane and N2O emissions, nitrate concentrations of drainage water, and zinc and copper uptake by rice fertilized with anaerobically digested cattle or pig slurry. Biol Fertil Soils 47:949–956. https://doi.org/10.1007/s00374-011-0601-1

    Article  CAS  Google Scholar 

  125. Zhang XY, Fang QC, Zhang T, Ma WQ, Velthof GL, Hou Y, Oenema O, Zhang FS (2020) Benefits and trade-offs of replacing synthetic fertilizers by animal manures in crop production in China: a meta-analysis. Glob Chang Biol 26:888–900. https://doi.org/10.1111/gcb.14826

    Article  Google Scholar 

  126. Qin YM, Liu SW, Guo YQ, Liu QH, Zou JW (2010) Methane and nitrous oxide emissions from organic and conventional rice cropping systems in Southeast China. Biol Fertil Soils 46:825–834. https://doi.org/10.1007/s00374-010-0493-5

    Article  CAS  Google Scholar 

  127. Charles A, Rochette P, Whalen JK, Angers DA, Chantigny MH, Bertrand N (2017) Global nitrous oxide emission factors from agricultural soils after addition of organic amendments: a meta-analysis. Agric Ecosyst Environ 236:88–98. https://doi.org/10.1016/j.agee.2016.11.021

    Article  CAS  Google Scholar 

  128. Velthof GL, Kuikman PJ, Oenema O (2003) Nitrous oxide emission from animal manures applied to soil under controlled conditions. Biol Fertil Soils 37:221–230. https://doi.org/10.1007/s00374-003-0589-2

    Article  CAS  Google Scholar 

  129. Yin MY, Gao XP, Tenuta M, Kuang WN, Gui DW, Zeng FJ (2019) Manure application increased denitrifying gene abundance in a drip-irrigated cotton field. PeerJ 7. https://doi.org/10.7717/peerj.7894

  130. Tao R, Wakelin SA, Liang YC, Hu BW, Chu GX (2018) Nitrous oxide emission and denitrifier communities in drip-irrigated calcareous soil as affected by chemical and organic fertilizers. Sci Total Environ 612:739–749. https://doi.org/10.1016/j.scitotenv.2017.08.258

    Article  CAS  Google Scholar 

  131. van der Weerden TJ, Kelliher FM, de Klein CAM (2012) Influence of pore size distribution and soil water content on nitrous oxide emissions. Soil Res 50:125–135. https://doi.org/10.1071/sr11112

    Article  Google Scholar 

  132. Petersen SO, Schjønning P, Thomsen IK, Christensen BT (2008) Nitrous oxide evolution from structurally intact soil as influenced by tillage and soil water content. Soil Biol Biochem 40:967–977. https://doi.org/10.1016/j.soilbio.2007.11.017

    Article  CAS  Google Scholar 

  133. Toma Y, Hatano R (2007) Effect of crop residue C: N ratio on N2O emissions from Gray Lowland soil in Mikasa, Hokkaido, Japan. Soil Sci Plant Nutr 53:198–205. https://doi.org/10.1111/j.1747-0765.2007.00125.x

    Article  CAS  Google Scholar 

  134. Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752. https://doi.org/10.1016/j.orggeochem.2004.09.006

    Article  CAS  Google Scholar 

  135. Dumont MG, Pommerenke B, Casper P (2013) Using stable isotope probing to obtain a targeted metatranscriptome of aerobic methanotrophs in lake sediment. Environ Microbiol Rep 5:757–764. https://doi.org/10.1111/1758-2229.12078

    Article  CAS  Google Scholar 

  136. Ding JJ, Fang FL, Lin W, Qiang XJ, Xu CY, Mao LL, Li QZ, Zhang XM, Li YZ (2019) N2O emissions and source partitioning using stable isotopes under furrow and drip irrigation in vegetable field of North China. Sci Total Environ 665:709–717. https://doi.org/10.1016/j.scitotenv.2019.02.053

    Article  CAS  Google Scholar 

  137. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340. https://doi.org/10.1038/ngeo846

    Article  CAS  Google Scholar 

  138. Jansson JK, Hofmockel KS (2018) The soil microbiome-from metagenomics to metaphenomics. Curr Opin Microbiol 43:162–168. https://doi.org/10.1016/j.mib.2018.01.013

    Article  CAS  Google Scholar 

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Kang, H., Lee, J., Zhou, X. et al. The Effects of N Enrichment on Microbial Cycling of Non-CO2 Greenhouse Gases in Soils—a Review and a Meta-analysis. Microb Ecol 84, 945–957 (2022). https://doi.org/10.1007/s00248-021-01911-8

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