Skip to main content
SpringerLink
Log in

Nitrogen fertiliser-induced changes in N2O emissions are attributed more to ammonia-oxidising bacteria rather than archaea as revealed using 1-octyne and acetylene inhibitors in two arable soils

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Nitrification is believed to be one of the major sources of N2O production emitted from soil. Previous studies showed that both ammonia-oxidising bacteria (AOB) and archaea (AOA) can produce N2O via nitrification but their relative contributions are still poorly defined. Here, we used acetylene, an inhibitor of AOB and AOA ammonia monooxygenase (AMO), and 1-octyne, a selective inhibitor that specifically inhibits AOB AMO, to investigate how AOB versus AOA contribute to N2O emissions in two distinct arable soils. Soil amended with ammonium (NH4 +) increased N2O emissions to a greater extent than nitrate (NO3 −), and acetylene had a greater impact on N2O emissions in NH4 +-treated soils than that in NO3 −-amended soils, which indicated that nitrification was the dominant N2O emitting process in these two arable soils. In the alluvial and red soil, the percentage of evolved N2O after application of NH4 + by AOB were 70.5 ~ 78.1 % and 18.7 ~ 19.7 % by AOA, respectively. Quantitative PCR revealed that NH4 + addition stimulated AOB growth, and the growth could be significantly inhibited by acetylene or 1-octyne in the two soils. The stimulation of N2O emissions by NH4 + and the relative suppression by inhibitors paralleled fluctuations in the AOB growth. In addition, cumulative N2O emissions were not correlated with AOA abundance in the two soils. Our results revealed that AOB could contribute more to soil N2O production than AOA in the NH4 +-amended arable soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ai C, Liang GQ, Sun JW, Wang XB, He P, Zhou W (2013) Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biol Biochem 57:30–42

    Article  CAS  Google Scholar 

  • Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388

    Article  CAS  Google Scholar 

  • Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils-what matters for their functioning? Adv Appl Microbiol 75(75):33–70

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516

    Article  CAS  Google Scholar 

  • Chen QH, Qi LY, Bi QF, Dai PB, Sun DS, Sun CL, Liu WJ, Lu LL, Ni WZ, Lin XY (2015) Comparative effects of 3,4-dimethylpyrazole phosphate (DMPP) and dicyandiamide (DCD) on ammonia-oxidizing bacteria and archaea in a vegetable soil. Appl Microbiol Biotechnol 99:477–487

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Wang J, Wang SQ, Zhang JB, Cai ZC (2014) Effects of soil moisture on gross N transformations and N2O emission in aci subtropical forest soils. Bio Fertil Soils 50:1099–1108

    Article  CAS  Google Scholar 

  • Cui PY, Fan FL, Yin C, Li Z, Song AL, Wan Y, Liang YC (2013) Urea- and nitrapyrin-affected N2O emission is coupled mainly with ammonia oxidizing bacteria growth in microcosms of three typical Chinese arable soils. Soil Biol Biochem 66:214–221

    Article  CAS  Google Scholar 

  • Cui PY, Fan FL, Yin C, Song AL, Huang PR, Tang YJ, Zhu P, Peng C, Li T, 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

    Article  CAS  Google Scholar 

  • Dai Y, Di HJ, Cameron KC, He JZ (2013) Effects of nitrogen application rate and a nitrification inhibitor dicyandiamide on ammonia oxidizers and N2O emissions in a grazed pasture soil. Sci Total Environ 465:125–135

    Article  CAS  PubMed  Google Scholar 

  • Davidson EA (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat Geosci 2:659–662

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC (2011) Inhibition of ammonium oxidation by a liquid formulation of 3,4-Dimethylpyrazole phosphate (DMPP) compared with a dicyandiamide (DCD) solution in six new Zealand grazed grassland soils. J Soils Sediments 11:1032–1039

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Sherlock RR, Shen JP, He JZ, Winefield CS (2010) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J Soils Sediments 10:943–954

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Podolyan A, Robinson A (2014) Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil. Soil Biol Biochem 73:59–68

    Article  CAS  Google Scholar 

  • Gӧdde M, Conrad R (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biol Fertil Soils 30:33–40

    Article  Google Scholar 

  • Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574

    Article  CAS  PubMed  Google Scholar 

  • Habteselassie MY, Xu L, Norton JM (2013) Ammonia-oxidizer communities in an agricultural soil treated with contrasting nitrogen sources. Front Microbiol 4:326

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatch D, Trindade H, Cardenas L, Carneiro J, Hawkins J, Scholefield D, Chadwick D (2005) Laboratory study of the effects of two nitrification inhibitors on greenhouse gas emissions from a slurry-treated arable soil: impact of diurnal temperature cycle. Biol Fertil Soils 41:225–232

    Article  CAS  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374

    Article  CAS  PubMed  Google Scholar 

  • Hink L, Nicol GW, Prosser JI (2016) Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol. doi:10.1111/1462-2920.13282

  • Hooper AB, Terry KR (1979) Hydroxylamine oxidoreductase of Nitrosomonas production of nitric-oxide from hydroxylamine. Bioch Et Bioph Act 571:12–20

    Article  CAS  Google Scholar 

  • Hu HW, Zhang LM, Yuan CL, He JZ (2013) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27

    Article  CAS  Google Scholar 

  • Hu HW, Macdonald CA, Trivedi P, Holmes B, Bodrossy L, He JZ, Singh BK (2015) Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. Environ Microbiol 17:444–461

    Article  CAS  PubMed  Google Scholar 

  • Huang T, Gao B, Hu XK, Lu X, Well R, Christie P, Bakken LR, Ju XT (2014a) Ammonia-oxidation as an engine to generate nitrous oxide in an intensively managed calcareous fluvo-aquic soil. Sci Rep 4:3950

    PubMed  PubMed Central  Google Scholar 

  • Huang Y, Li YY, Yao HY (2014b) Nitrate enhances N2O emission more than ammonium in a highly acidic soil. J Soils Sediments 14:146–154

    Article  CAS  Google Scholar 

  • Hynes RK, Knowles R (1978) Inhibition by acetylene of ammonia oxidation in Nitrosomonas-Europaea. FEMS Microbiol Lett 4:319–321

    Article  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  CAS  PubMed  Google Scholar 

  • Jung MY, Park SJ, Min D, Kim JS, Rijpstra WIC, Damste JSS, Kim GJ, Madsen EL, Rhee SK (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural Soil. Appl Environ Microbiol 77:8635–8647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kool DM, Wrage N, Zechmeister-Boltenstern S, Pfeffer M, Brus D, Oenema O, Van Groenigen JW (2010) Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labelling method. Eur J Soil Sci 61:759–772

    Article  CAS  Google Scholar 

  • Kool DM, Dolfing J, Wrage N, Van Groenigen JW (2011) Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem 43:174–178

    Article  CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  PubMed  Google Scholar 

  • Li P, Lang M (2014) Gross nitrogen transformations and related N2O emissions in uncultivated and cultivated black soil. Biol Fertil Soils 50:197–20

    Article  CAS  Google Scholar 

  • Loscher CR, Kock A, Konneke M, LaRoche J, Bange HW, Schmitz RA (2012) Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9:2419–2429

    Article  Google Scholar 

  • Lu XD, Bottomley PJ, Myrold DD (2015) Contributions of ammonia-oxidizing archaea and bacteria to nitrification in Oregon forest soils. Soil Biol Biochem 85:54–62

    Article  CAS  Google Scholar 

  • Lund MB, Smith JM, Francis CA (2012) Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea. ISME J 6:1966–1977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Ma E, Xu H, Yagi K, Cai ZC (2009) Wheat straw management affects CH4 and N2O emissions from rice fields. Soil Biol Biochem 41:1022–1028

    Article  CAS  Google Scholar 

  • Ma L, Shan J, Yan XY (2015) Nitrite behavior accounts for the nitrous oxide peaks following fertilization in a fluvo-aquic soil. Biol Fert soils 51:563–572

    Article  CAS  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  CAS  PubMed  Google Scholar 

  • Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. Methods Enzymol 486:343–368

    Article  CAS  PubMed  Google Scholar 

  • Offre P, Prosser JI, Nicol GW (2009) Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70:99–108

    Article  CAS  PubMed  Google Scholar 

  • Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol Biochem 96:4–15

    Article  CAS  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santoro AE, Buchwald C, McIlvin MR, Casciotti KL (2011) Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282–1285

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214–222

    Article  CAS  PubMed  Google Scholar 

  • Shcherbak I, Millar N, Robertson GP (2014) Global meta-analysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A 111:9199–9204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith KA, Mosier AR, Crutzen PJ, Winiwarter W (2012) The role of N2O derived from crop-based biofuels, and from agriculture in general, in Earth’s climate. Phil Trans R Soc B 367:1169–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein LY (2011) Surveying N2O-producing pathways in bacteria. In: Klotz MG (ed) Methods in enzymology, vol 486. Academic Press, CA, pp 131–152

    Google Scholar 

  • Sterngren AE, Hallin S, Bengtson P (2015) Archaeal ammonia oxidizers dominate in numbers, but bacteria drive gross nitrification in N-amended grassland soil. Front Microbiol 6:1350

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AE, Zeglin LH, Wanzek TA, Myrold DD, Bottomley PJ (2012) Dynamics of ammonia-oxidizing archaea and bacteria populations and contributions to soil nitrification potentials. ISME J 6:2024–2032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AE, Vajrala N, Giguere AT, Gitelman AI, Arp DJ, Myrold DD, Sayavedra-Soto L, Bottomley PJ (2013) Use of aliphatic n-Alkynes to discriminate soil nitrification activities of ammonia-oxidizing thaumarchaea and bacteria. Appl Environ Microbiol 79:6544–6551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AE, Taylor K, Tennigkeit B, Palatinszky M, Stieglmeier M, Myrold DD, Schleper C, Wagner M, Bottomley PJ (2015) Inhibitory effects of C-2 to C-10 1-Alkynes on ammonia oxidation in two Nitrososphaera Species. Appl Environ Microbiol 81:1942–1948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • USDA (1994) Keys to soil taxonomy. United States Department of Agriculture, Soil Conservation Service, 6th edn., p 306

    Google Scholar 

  • Vajrala N, Martens-Habbena W, Sayavedra-Soto LA, Schauer A, Bottomley PJ, Stahl DA, Arp DJ (2013) Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc Natl Acad Sci U S A 110:1006–1011

    Article  CAS  PubMed  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  • Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Burger M, Doane TA, Horwath WR (2013) Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc Natl Acad Sci U S A 110:6328–6333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020200) and by the Natural Science Foundation of China (41322007 and 41371265).

Author information

Authors and Affiliations

  1. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Qing Wang, Li-Mei Zhang, Ju-Pei Shen, Shuai Du, Li-Li Han & Ji-Zheng He

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

    Qing Wang & Shuai Du

  3. Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, 3010, Australia

    Ji-Zheng He

Authors
  1. Qing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li-Mei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ju-Pei Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuai Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li-Li Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ji-Zheng He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li-Mei Zhang or Ji-Zheng He.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Q., Zhang, LM., Shen, JP. et al. Nitrogen fertiliser-induced changes in N2O emissions are attributed more to ammonia-oxidising bacteria rather than archaea as revealed using 1-octyne and acetylene inhibitors in two arable soils. Biol Fertil Soils 52, 1163–1171 (2016). https://doi.org/10.1007/s00374-016-1151-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-016-1151-3

Keywords

Search

Navigation