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Contrasting response of nitrification capacity in three agricultural soils to N addition during short-term incubation

  • SOILS, SEC 5 • SOIL AND LANDSCAPE ECOLOGY • RESEARCH ARTICLE
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Abstract

Purpose

Human disturbance is a major culprit driving imbalances in the biological transformation of nitrogen from the nonreactive to the reactive pool and is therefore one of the greatest concerns for nitrogen (N) cycling. The objective of this study was to compare potential nitrification rates and the abundance of ammonia oxidizers responsible for nitrification, with the amendment of external N in different agricultural soils.

Materials and methods

Three typical Chinese agricultural soils, QiYang (QY) acid soil, ShenYang (SY) neutral soil, and FengQiu (FQ) alkaline soil, were amended with 0, 20, 150, and 300 μg NH4 +-N g−1 soil and incubated for 40 days. The abundance of ammonia oxidizing bacteria (AOB) and archaea (AOA) at the end of incubation in the soil microcosms was determined using the real-time PCR.

Results and discussion

There was a significant decrease in ammonium concentration in the QY soil from the highest to the lowest N-loading treatments, while no significant difference in ammonium concentrations was detected among the different N-loading treatments for the SY and FQ soils. A significantly higher potential nitrification rate (PNR) was observed in the FQ soil while lowest PNR was found in the QY soil. Quantitative PCR analysis of AOB amoA genes demonstrated that AOB abundance was significantly higher in the high N-loading treatments than in the control for the QY soil only, while no significant difference among treatments in the SY and FQ soils. A significant positive correlation between PNR and AOB amoA abundance, however, was found for the SY and FQ soils, but not for the QY soil. Little difference in AOA amoA abundance between different N-loading treatments was observed for all the soils.

Conclusions

This study suggested that ammonia oxidation capacity in the FQ and SY soils was higher than those in the QY soil with the addition of ammonium fertilizer for a short-term. These findings indicated that understanding the differential responses of biological nitrification to varying input levels of ammonium fertilizer is important for maximizing N use efficiency and thereby improving agricultural fertilization management.

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References

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  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 

  • 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, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

    Article  CAS  Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343

    Article  CAS  Google Scholar 

  • Fernandez-Guerra A, Casamayor EO (2012) Habitat-associated phylogenetic community patterns of microbial ammonia oxidizers. PLoS ONE 7:e47330

    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 U S A 102:14683–14688

    Article  CAS  Google Scholar 

  • Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809

    Article  CAS  Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296

    Article  CAS  Google Scholar 

  • Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108:21206–21211

    Article  CAS  Google Scholar 

  • Haynes RJ (1986) Chapter 3 - Nitrification. In: Haynes RJ (ed) Mineral nitrogen in the plant–soil system. Academic Press, pp 127–165

  • He JZ, Shen JP, Zhang LM, Zhu YM, Zheng YG, Xu MG, Di HJ (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  Google Scholar 

  • He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154

    Article  CAS  Google Scholar 

  • Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13:1439–1449

    Article  Google Scholar 

  • Hu HW, Xu ZH, He JZ (2014) Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. Adv Agron 125:261–302

    Article  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  Google Scholar 

  • Kurola J, Salkinoja-Salonen M, Aarnio T, Hultman J, Romantschuk M (2005) Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. FEMS Microbiol Lett 250:33–38

    Article  CAS  Google Scholar 

  • Levicnik-Hofferle S, Nicol GW, Ausec L, Mandic-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  CAS  Google Scholar 

  • 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

    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  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  Google Scholar 

  • Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B, Lebauer D, Scow KM (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 70:1008–1016

    Article  CAS  Google Scholar 

  • Phillips CJ, Harris D, Dollhopf SL, Gross KL, Prosser JI, Paul EA (2000) Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl Environ Microbiol 66:5410–5418

    Article  CAS  Google Scholar 

  • Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke BM, Matthies M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456

    Article  CAS  Google Scholar 

  • Schleper C (2010) Ammonia oxidation: Different niches for bacteria and archaea? ISME J 4:1092–1094

    Article  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611

    Article  CAS  Google Scholar 

  • Shen JP, Zhang LM, Guo JF, Ray JL, He JZ (2010) Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Appl Soil Ecol 46:119–124

    Article  Google Scholar 

  • Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296

    CAS  Google Scholar 

  • Shen JP, Cao P, Hu HW, He JZ (2013) Differential response of archaeal groups to land use change in an acidic red soil. Sci Total Environ 461:742–749

    Article  Google Scholar 

  • Shen JP, Xu ZH, He JZ (2014) Frontiers in the microbial processes of ammonia oxidation in soils and sediments. J Soils Sediments 14:1023–1029

    Article  CAS  Google Scholar 

  • Silva MCPE, Poly F, Guillaumaud N, van Elsas JD, Salles JF (2012) Fluctuations in ammonia oxidizing communities across agricultural soils are driven by soil structure and pH. Front Microbiol 3:77

    Article  Google Scholar 

  • Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: Terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790

    Article  CAS  Google Scholar 

  • Ste-Marie C, Pare D (1999) Soil, pH and N availability effects on net nitrification in the forest floors of a range of boreal forest stands. Soil Biol Biochem 31:1579–1589

    Article  CAS  Google Scholar 

  • Suzuki I, Dular U, Kwok SC (1974) Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol 120:556–558

    CAS  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  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  Google Scholar 

  • Wessen E, Soderstrom M, Stenberg M, Bru D, Hellman M, Welsh A, Thomsen F, Klemedtson L, Philippot L, Hallin S (2011) Spatial distribution of ammonia-oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISME J 5:1213–1225

    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 HY, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: Evidence from a national soil survey. Environ Microbiol 15:2545–2556

    Article  CAS  Google Scholar 

  • Yuan F, Ran W, Shen QR, Wang DZ (2005) Characterization of nitrifying bacteria communities of soils from different ecological regions of China by molecular and conventional methods. Biol Fertil Soils 41:22–27

    Article  CAS  Google Scholar 

  • Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U S A 107:17240–17245

    Article  CAS  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  Google Scholar 

Download references

Acknowledgments

We appreciate the helpful suggestions and English improvements from Dr. Jessica L. Ray, Uni Research AS, Norway. The assistances in sampling by staff at the Qiyang (QY), Fengqiu (FQ) and Shenyang (SY) experiment stations are sincerely appreciated. This work was financially support by the Natural Science Foundation of China (41371265) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020200).

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Correspondence to Ji-Zheng He.

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Responsible editor: Ian Anderson

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Shen, JP., Zhang, LM. & He, JZ. Contrasting response of nitrification capacity in three agricultural soils to N addition during short-term incubation. J Soils Sediments 14, 1861–1868 (2014). https://doi.org/10.1007/s11368-014-0968-3

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