Current Microbiology

, Volume 70, Issue 2, pp 282–289 | Cite as

The Influence of Land Use on the Abundance and Diversity of Ammonia Oxidizers

  • Dayong ZhaoEmail author
  • Juan Luo
  • Jianqun Wang
  • Rui Huang
  • Kun Guo
  • Yi Li
  • Qinglong L. Wu


Nitrification plays a significant role in soil nitrogen cycling, a process in which the first step can be catalyzed by ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). In this study, six soil samples with distinct land-use regimes (forestland soil, paddy soil, wheat-planted soil, fruit-planted soil, grassland soil, and rape-planted soil) were collected from Chuzhou city in the Anhui province to elucidate the effects of land use on the abundance and diversity of AOA and AOB. The abundance of the archaeal amoA gene ranged from 2.12 × 104 copies per gram of dry soil to 2.57 × 105 copies per gram of dry soil, while the abundance of the bacterial amoA gene ranged from 5.58 × 104 copies per gram of dry soil to 1.59 × 108 copies per gram of dry soil. The grassland and the rape-planted soil samples maintained the highest abundance of the bacterial and archaeal amoA genes, respectively. The abundance of the archaeal amoA gene was positively correlated with the pH (P < 0.05). The ammonia concentrations exhibited a significantly positive relation with the abundance of the bacterial amoA gene (P < 0.01) and the number of OTUs of AOB (P < 0.05). The community composition of AOB was more sensitive to the land-use regimes than that of AOA. The data obtained in this study may be useful to better understand the nitrification process in soils with different land-use regimes.


Ammonia Oxidizer amoA Gene Bacterial amoA Gene Archaeal amoA Gene amoA Gene Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the Ministry of Water Resources’ Special Funds for Scientific Research on Public Causes (201201026), National Natural Science Foundation of China (41371098), China Postdoctoral Science Foundation (2014T70470, 2014M561568) and Jiangsu Planned Projects for Postdoctoral Research Funds (1401093C).

Supplementary material

284_2014_714_MOESM1_ESM.doc (2.3 mb)
Supplementary material 1 (DOC 2347 kb)


  1. 1.
    Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microb Ecol 56:420–426PubMedCrossRefGoogle Scholar
  2. 2.
    Avrahami S, Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microbiol 69:6152–6164PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Appl Environ Microbiol 72:7767–7777PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Bernhard AE, Bollmann A (2010) Estuarine nitrifiers: new players, patterns and processes. Estuar Coast Shelf S 88:1–11CrossRefGoogle Scholar
  5. 5.
    Boyle-Yarwood SA, Bottomley PJ, Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10:2956–2965PubMedCrossRefGoogle Scholar
  6. 6.
    Briones AM, Okabe S, Umemiya Y, Ramsing NB, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 68:3067–3075PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Chen X, Zhang LM, Shen JP, Xu Z, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516CrossRefGoogle Scholar
  8. 8.
    Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil. Environ Microbiol 10:1978–1987PubMedCrossRefGoogle Scholar
  9. 9.
    De BW, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33:853–866CrossRefGoogle Scholar
  10. 10.
    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 2:621–624CrossRefGoogle Scholar
  11. 11.
    Francis CA, Beman JM, Kuypers MM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. The ISME J 1:19–27CrossRefGoogle Scholar
  12. 12.
    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. P Natl Acad Sci USA 102:14683–14688CrossRefGoogle Scholar
  13. 13.
    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 69:1800–1809PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574PubMedCrossRefGoogle Scholar
  15. 15.
    Hastings RC, Butler C, Singleton I, Saunders JR, McCarthy AJ (2000) Analysis of ammonia-oxidizing bacteria populations in acid forest soil during conditions of moisture limitation. Lett Appl Microbiol 30:14–18PubMedCrossRefGoogle Scholar
  16. 16.
    Hermansson A, Lindgren PE (2001) Quantification of ammonia-oxidizing bacteria in arable soil by real-time PCR. Appl Environ Microbiol 67:972–976PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    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 9:2364–2374PubMedCrossRefGoogle Scholar
  18. 18.
    Hu A, Yao T, Jiao N, Liu Y, Yang Z, Liu X (2010) Community structures of ammonia-oxidising archaea and bacteria in high-altitude lakes on the Tibetan Plateau. Freshw Biol 55:2375–2390Google Scholar
  19. 19.
    Jia Z, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671PubMedCrossRefGoogle Scholar
  20. 20.
    Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546PubMedCrossRefGoogle Scholar
  21. 21.
    Koski-Vähälä J, Hartikainen H, Tallberg P (2001) Phosphorus mobilization from various sediment pools in response to increased pH and silicate concentration. J Environ Qual 30:546–552PubMedCrossRefGoogle Scholar
  22. 22.
    Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiol Ecol 31:207–215PubMedCrossRefGoogle Scholar
  23. 23.
    Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99–110PubMedCrossRefGoogle Scholar
  24. 24.
    Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529PubMedCrossRefGoogle Scholar
  25. 25.
    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 442:806–809PubMedCrossRefGoogle Scholar
  26. 26.
    Li XR, Xiao YP, Ren WW, Liu ZF, Shi JH, Quan ZX (2012) Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary. JZUS-B 13:769–782Google Scholar
  27. 27.
    Morimoto S, Hayatsu M, Takada HY, Nagaoka K, Yamazaki M, Karasawa T, Takenaka M, Akiyama H (2011) Quantitative analyses of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in fields with different soil types. Microbes Environ 26:248–253PubMedCrossRefGoogle Scholar
  28. 28.
    Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016PubMedCrossRefGoogle Scholar
  29. 29.
    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 10:2966–2978PubMedCrossRefGoogle Scholar
  30. 30.
    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 70:1008–1016PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Onodera Y, Nakagawa T, Takahashi R, Tokuyama T (2009) Seasonal change in vertical distribution of ammonia-oxidizing archaea and bacteria and their nitrification in temperate forest soil. Microbes Environ 25:28–35CrossRefGoogle Scholar
  32. 32.
    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 63:4704–4712PubMedCentralPubMedGoogle Scholar
  33. 33.
    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 11:446–456PubMedCrossRefGoogle Scholar
  34. 34.
    Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296–302PubMedCentralPubMedGoogle Scholar
  35. 35.
    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 10:1601–1611PubMedCrossRefGoogle Scholar
  36. 36.
    Suzuki C, Nagaoka K, Shimada A, Takenaka M (2009) Bacterial communities are more dependent on soil type than fertilizer type, but the reverse is true for fungal communities. Soil Sci Plant Nutr 55:80–90CrossRefGoogle Scholar
  37. 37.
    Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  38. 38.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995PubMedCrossRefGoogle Scholar
  40. 40.
    Wang Y, Ke X, Wu L, Lu Y (2009) Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Syst Appl Microbiol 32:27–36PubMedCrossRefGoogle Scholar
  41. 41.
    Webster G, Embley TM, Freitag TE, Smith Z, Prosser JI (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7:676–684PubMedCrossRefGoogle Scholar
  42. 42.
    Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of β-proteobacterial ammonia oxidizer populations. Appl Environ Microbiol 68:20–30PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Weidler GW, Dornmayr-Pfaffenhuemer M, Gerbl FW, Heinen W, Stan-Lotter H (2007) Communities of archaea and bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing crenarchaeota. Appl Environ Microbiol 73:259–270PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Zeng J, Zhao DY, Huang R, Wu QL (2012) Abundance and community composition of ammonia-oxidizing archaea and bacteria in two different zones of Lake Taihu. Can J Microbiol 58:1018–1026PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Dayong Zhao
    • 1
    • 2
    Email author
  • Juan Luo
    • 2
  • Jianqun Wang
    • 2
  • Rui Huang
    • 2
  • Kun Guo
    • 2
  • Yi Li
    • 2
  • Qinglong L. Wu
    • 3
  1. 1.State Key Laboratory of Hydrology-Water Resources and Hydraulic EngineeringHohai UniversityNanjingChina
  2. 2.College of Hydrology and Water ResourcesHohai UniversityNanjingChina
  3. 3.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingChina

Personalised recommendations