Skip to main content
Log in

Growth and N2O production of Nitrosocosmicus clade in agricultural soil when responding to high ammonium inputs

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

In recent years, some ammonia-oxidizing archaea (AOA) species from the Nitrosocosmicus clade have been suggested to be ammonium tolerant, with ability close to many ammonia-oxidizing bacteria (AOB) species. However, the Nitrosocosmicus clade growth and contribution to N2O production in agricultural soil when responding to high ammonium inputs are still unknown.

Methods

Based on three microcosms, the effects of ammonium inputs on the abundance of Nitrosocosmicus clade in AOA community, the Nitrosocosmicus clade growth, and contribution to N2O production were investigated. Based on batch cultivation of Candidatus Nitrosocosmicus agrestis (Ca. N. agrestis) and the microcosm with extra addition of Ca. N. agrestis, AOA contribution to N2O production was studied.

Results

High ammonium inputs benefited the abundance increase of Nitrosocosmicus clade, with relative abundance increased from 2.6 to 9.1–15.5% of the AOA community in DNA samples, and from 1.4 to 15.1–47.5% in RNA samples. High ammonium inputs promoted the growth of Nitrosocosmicus clade, with number accounting for 16.9–22.9% of the total AOA but 48.5–74.2% of the increased AOA. High ammonium inputs also activated the expression of Nitrosocosmicus clade amoA gene. Due to the presence of Nitrosocosmicus clade, high ammonium inputs increased the contribution of AOA to N2O production; in the presence of Ca. N. agrestis, the contribution of AOA to N2O production is comparable to AOB when responding to high ammonium inputs.

Conclusion

The Nitrosocosmicus clade in agricultural soils is likely ammonium tolerant; its growth and contribution to N2O production could be favored by high ammonium inputs.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Data will be made available on request.

References

  • Aliyu G, Luo J, Di HJ, Lindsey S, Liu D, Yuan J, Chen Z, Lin Y, He T, Zaman M, Ding W (2019) Nitrous oxide emissions from China’s croplands based on regional and crop-specific emission factors deviate from IPCC 2006 estimates. Sci Total Environ 669:547–558

    Article  CAS  Google Scholar 

  • Bedard C, Knowles R (1989) Physiology biochemistry and specific inhibitors of CH4, NH4+ and CO oxidation by methanotrophs and nitrifiers. Microbiol Mol Biol R 53:68–84

    CAS  Google Scholar 

  • Bello MO, Aigle A, Meng Y, Prosser JI, Gubry-Rangin C (2021) Preferential temperature and ammonia concentration for in-situ growth of Candidatus Nitrosocosmicus ammonia oxidising archaea. Soil Biol Biochem 162:108405

    Article  CAS  Google Scholar 

  • Berger SA, Krompass D, Stamatakis A (2011) Performance accuracy and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol 60:291–302

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Deppe M, Well R, Giesemann A, Spott O, Flessa H (2017) Soil N2O fluxes and related processes in laboratory incubations simulating ammonium fertilizer depots. Soil Biol Biochem 104:68–80

    Article  CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688

    Article  CAS  Google Scholar 

  • Fu QL, Xi RZ, Zhu J, Hu HQ, Xing ZQ, Zuo JC (2020) The relative contribution of ammonia oxidizing bacteria and archaea to N2O emission from two paddy soils with different fertilizer N sources: a microcosm study. Geoderma 375:114486

    Article  CAS  Google Scholar 

  • Gubry-Rangin C, Kratsch C, Williams TA, McHardy AC, Embley TM, Prosser JI, Macqueen DJ (2015) Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. Proc Natl Acad Sci USA 112:9370–9375

    Article  CAS  Google Scholar 

  • Hergoualc’h K, Mueller N, Bernoux M, Kasimir A, van der Weerden TJ, Ogle SM (2021) Improved accuracy and reduced uncertainty in greenhouse gas inventories by refining the IPCC emission factor for direct N2O emissions from nitrogen inputs to managed soils. Global Change Biol 27:6536-6550

  • 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

    Article  CAS  Google Scholar 

  • Hink L, Nicol GW, Prosser JI (2017a) Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol 19:4829–4837

    Article  CAS  Google Scholar 

  • Hink L, Lycus P, Gubry-Rangin C, Frostegard A, Nicol GW, Prosser JI, Bakken LR (2017b) Kinetics of NH3-oxidation NO-turnover N2O-production and electron flow during oxygen depletionin model bacterial and archaeal ammonia oxidisers. Environ Microbiol 19:4882–4896

    Article  CAS  Google Scholar 

  • IPCC. Climate change 2021: the physical science basis. Cambridge: Cambridge University Press 2021.

  • ISO/TS 14256–1:2003 (2003). Soil quality-determination of nitrate nitrite and ammonium in field moist soils by extraction with potassium chloride solution. Geneva: International Organisation for Standardisation

  • Jung MY, Kim JG, Sinninghe Damste JS, Rijpstra WI, Madsen EL, Kim SJ, Hong H, Si OJ, Kerou M, Schleper C, Rhee SK (2016) A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment. Env Microbiol Rep 8:983–992

    Article  CAS  Google Scholar 

  • Jung MY, Park SJ, Min D, Kin JS, Rijpstra WI, 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 and Environ Microb. 77:8635-8647

  • Lehtovirta-Morley L E, Ross J, Hink L, Weber E B, Gubry-Rangin C, Thion C, Prosser J I, Nicol G W (2016) Isolation of “Candidatus Nitrosocosmicus franklandus” a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonium concentration. FEMS Microbiol Ecol. 92: fiw057

  • Liang D, Robertson GP (2021) Nitrification is a minor source of nitrous oxide (N2O) in an agricultural landscape and declines with increasing management intensity. Global Change Biol 27:5599–5613

    Article  CAS  Google Scholar 

  • Liu H, Hu H, Huang X, Ge T, Li Yongfu Zhu Z, Liu X, Tan W, Jia Z, Di H, Xu J, Yong Li (2021a) Canonical ammonia oxidizers rather than comammox Nitrospira dominated autotrophic nitrification during the mineralization of organic substances in two paddy soils. Soil Biol Biochem 156:108192

    Article  CAS  Google Scholar 

  • Liu L, Li S, Han J, Lin W, Luo J (2019) A two-step strategy for the rapid enrichment of Nitrosocosmicus-like ammonia-oxidizing thaumarchaea. Front Microbiol 10:875

    Article  Google Scholar 

  • Liu L, Liu M, Jiang Y, Lin W, Luo J (2021b) Production and excretion of polyamines to tolerate high ammonium a case study on soil ammonia-oxidizing archaeon “Candidatus Nitrosocosmicus agrestis”. mSystems. 6: e01003–20

  • McCarty GW (1999) Modes of action of nitrification inhibitors. Biol and Fert Soils 29:1–9

    Article  CAS  Google Scholar 

  • Meinhardt KA, Stopnisek N, Pannu MW, Strand SE, Fransen SC, Casciotti KL, Stahl DA (2018) Ammonia-oxidizing bacteria are the primary N2O producers in an ammonia-oxidizing archaea dominated alkaline agricultural soil. Environ Microbiol 20:2195–2206

    Article  CAS  Google Scholar 

  • Prather MJ, Hsu J, DeLuca NM, Jackman CH, Oman LD, Douglass AR, Fleming EL, Strahan SE, Steenrod SD, Sovde OA, Isaksen IS, Froidevaux L, Funke B (2015) Measuring and modeling the lifetime of nitrous oxide including its variability. J Geophys Res 120:5693–5705

    Article  CAS  Google Scholar 

  • Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Change 2:410–416

    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 and Environ Microb 63:4704–4712

    Article  CAS  Google Scholar 

  • Sauder LA, Albertsen M, Engel K, Schwarz J, Nielsen PH, Wagner M, Neufeld JD (2017) Cultivation and characterization of Candidatus Nitrosocosmicus exaquare an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J 11:1142–1157

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source platform-independent community-supported software for describing and comparing microbial communities. Appl and Environ Microb 75:7537–7541

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shepherd A, Yan X, Nayak D, Newbold J, Moran D, Dhanoa MS, Goulding K, Smith P, Cardenas LM (2015) Disaggregated N2O emission factors in China based on cropping parameters create a robust approach to the IPCC Tier 2 methodology. Atmos Environ 122:272–281

    Article  CAS  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  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  Google Scholar 

  • Tan C, Yin C, Li W, Fan X, Jiang Y, Liang Y (2022) Comammox Nitrospira play a minor role in N2O emissions from an alkaline arable soil. Soil Biol Biochem 171:108720

    Article  CAS  Google Scholar 

  • Tian H, Xu R, Canadell JG, Thompson RL, Winiwarter W, Suntharalingam P, Davidson EA, Ciais P, Jackson RB, Janssens-Maenhout G, Prather MJ, Regnier P, Pan N, Pan S, Peters GP, Shi H, Tubiello FN, Zaehle S, Zhou F, Arneth A, Battaglia G, Berthet S, Bopp L, Bouwman AF, Buitenhuis ET, Chang J, Chipperfield MP, Dangal SRS, Dlugokencky E, Elkins JW, Eyre BD, Fu B, Hall B, Ito A, Joos F, Krummel PB, Landolfi A, Laruelle GG, Lauerwald R, Li W, Lienert S, Maavara T, MacLeod M, Millet DB, Olin S, Patra PK, Prinn RG, Raymond PA, Ruiz DJ, van der Werf GR, Vuichard N, Wang J, Weiss RF, Wells KC, Wilson C, Yang J, Yao Y (2020) A comprehensive quantification of global nitrous oxide sources and sinks. Nature 586:248–256

    Article  CAS  Google Scholar 

  • Tian H, Yang J, Xu R, Lu C, Canadell JG, Davidson EA, Jackson RB, Arneth A, Chang J, Ciais P, Gerber S, Ito A, Joos F, Lienert S, Messina P, Olin S, Pan S, Peng C, Saikawa E, Thompson RL, Vuichard N, Winiwarter W, Zaehle S, Zhang B (2019) Global soil nitrous oxide emissions since the preindustrial era estimated by an ensemble of terrestrial biosphere models: magnitude attribution and uncertainty. Global Change Biol 25:640–659

    Article  Google Scholar 

  • Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    Article  CAS  Google Scholar 

  • Wang MZ, Wang SY, Long X, Zhuang LJ, Zhao X, Jia ZJ, Zhu GB (2019) High contribution of ammonia-oxidizing archaea (AOA) to ammonia oxidation related to a potential active AOA species in various arable land soils. J Soil Sediment 19:1077–1087

    Article  CAS  Google Scholar 

  • Wang Q, Zhang LM, Shen JP, Du S, Han LL, He JZ (2016) 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 and Fert of Soils 52:1163–1171

    Article  CAS  Google Scholar 

  • Winiwarter W, Höglund-Isaksson L, Klimont Z, Schöpp W, Amann M (2018) Technical opportunities to reduce global anthropogenic emissions of nitrous oxide. Environ Res Lett 13:014011

    Article  Google Scholar 

  • Wrage-Mönnig N, Horn MA, Well R, Müller C, Velthof G, Oenema O (2018) The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biol Biochem 123:A3–A16

    Article  Google Scholar 

  • Yang L, Zhu G, Ju X, Liu R (2021) How nitrification-related N2O is associated with soil ammonia oxidizers in two contrasting soils in China? Sci Total Environ 770:143212

    Article  CAS  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  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (41977034 and 91951118), the Guangdong Basic and Applied Basic Research Foundation (No. 2021A1515010565), and the Fundamental Research Funds for the Central Universities (no. 2022ZYGXZR040).

Author information

Authors and Affiliations

Authors

Contributions

YJ, JW, WL, and JL proposed the study and designed the experiment. YJ, JW, and ML conducted microcosmic studies, laboratory measurements, and analyzed the data. YZ and QW helped with laboratory measurements. YJ and JL wrote the manuscript. WL and JL revised the manuscript.

Corresponding authors

Correspondence to Weitie Lin or Jianfei Luo.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Yuan Ge

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 500 KB)

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

Jiang, Y., Wu, J., Liu, M. et al. Growth and N2O production of Nitrosocosmicus clade in agricultural soil when responding to high ammonium inputs. J Soils Sediments 23, 3458–3471 (2023). https://doi.org/10.1007/s11368-023-03547-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-023-03547-2

Keywords

Navigation