Skip to main content
Log in

Abundance and distribution of ammonia-oxidizing archaea in Tibetan and Yunnan plateau agricultural soils of China

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

As low oxygen and high ultraviolet (UV) exposure might significantly affect the microbial existence in plateau, it could lead to a specialized microbial community. To determine the abundance and distribution of ammonia-oxidizing archaea (AOA) in agricultural soil of plateau, seven soil samples were collected respectively from farmlands in Tibet and Yunnan cultivating the wheat, highland-barley, and colza, which are located at altitudes of 3200–3800 m above sea level. Quantitative PCR (q-PCR) and clone library targeting on amoA gene were used to quantify the abundances of AOA and ammonia-oxidizing bacteria (AOB), and characterize the community structures of AOA in the samples. The number of AOA cells (9.34 × 107−2.32 × 108 g−1 soil) was 3.86–21.84 times greater than that of AOB cells (6.91 × 106−1.24 × 108 g−1 soil) in most of the samples, except a soil sample cultivating highland-barley with an AOA/AOB ratio of 0.90. Based Kendall’s correlation coefficient, no remarkable correlation between AOA abundance and the environmental factor was observed. Additionally, the diversities of AOA community were affected by total nitrogen and organic matter concentration in soils, suggesting that AOA was probably sensitive to several environmental factors, and could adjust its community structure to adapt to the environmental variation while maintaining its abundance.

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.

Similar content being viewed by others

References

  1. Wagner M, Rath G, Amann R, Koops H P, Schleifer K H. In-situ identification of ammonia-oxidizing bacteria. Systematic and Applied Microbiology, 1995, 18(2):251–264

    Article  CAS  Google Scholar 

  2. Bock E, Wagner M. Oxidation of inorganic nitrogen compounds as an energy source. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K H, Stackebrandt E, editors. The Prokaryotes-An Evolving Electronic Resource for the Microbiological Community. 3rd ed. New York: Springer, 2001, 457–495

    Google Scholar 

  3. Hallam S J, Mincer T J, Schleper C, Preston C M, Roberts K, Richardson P M, DeLong E F. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biology, 2006, 4(4):520–536

    Article  CAS  Google Scholar 

  4. Könneke M, Bernhard A E, de la Torre J R, Walker C B, Waterbury J B, Stahl D A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 2005, 437(7058):543–546

    Article  Google Scholar 

  5. Hatzenpichler R, Lebedeva E V, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. A moderately thermophilic ammoniaoxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(6):2134–2139

    Article  CAS  Google Scholar 

  6. Park B J, Park S J, Yoon D N, Schouten S, Sinninghe Damsté J S, Rhee S K. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Applied and Environmental Microbiology, 2010, 76(22):7575–7587

    Article  CAS  Google Scholar 

  7. Matsutani N, Nakagawa T, Nakamura K, Takahashi R, Yoshihara K, Tokuyama T. Enrichment of a novel marine ammonia-oxidizing archaeon obtained from sand of an eelgrass zone. Microbes Environ, 2011, 26(1):23–29

    Article  Google Scholar 

  8. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(20):8420–8425

    Article  CAS  Google Scholar 

  9. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G W, Prosser J I, Schuster S C, Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature, 2006, 442(7104):806–809

    Article  CAS  Google Scholar 

  10. Mosier A C, Francis C A. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environmental Microbiology, 2008, 10(11):3002–3016

    Article  CAS  Google Scholar 

  11. Agogué H, Brink M, Dinasquet J, Herndl G J. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature, 2008, 456(7223):788–791

    Article  Google Scholar 

  12. Kasuga I, Nakagaki H, Kurisu F, Furumai H. Predominance of ammonia-oxidizing archaea on granular activated carbon used in a full-scale advanced drinking water treatment plant. Water Research, 2010, 44(17 17SI):5039–5049

    Article  CAS  Google Scholar 

  13. Park H D, Wells G F, Bae H, Criddle C S, Francis C A. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Applied and Environmental Microbiology, 2006, 72(8):5643–5647

    Article  CAS  Google Scholar 

  14. Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polprasert C. Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresource Technology, 2011, 102(4):3694–3701

    Article  CAS  Google Scholar 

  15. Wuchter C, Abbas B, Coolen M J, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl G J, Middelburg J J, Schouten S, Sinninghe Damsté J S. Archaeal nitrification in the ocean. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33):12317–12322

    Article  CAS  Google Scholar 

  16. Mussmann M, Brito I, Pitcher A, Sinninghe Damsté J S, Hatzenpichler R, Richter A, Nielsen J L, Nielsen P H, Müller A, Daims H, Wagner M, Head I M. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(40):16771–16776

    Article  CAS  Google Scholar 

  17. Nicol G W, Leininger S, Schleper C, Prosser J I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology, 2008, 10(11):2966–2978

    Article  CAS  Google Scholar 

  18. Zhang L M, Wang M, Prosser J I, Zheng Y M, He J Z. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiology Ecology, 2009, 70(2):208–217

    Article  CAS  Google Scholar 

  19. Di H J, Cameron K C, Shen J P, Winefield C S, O’Callaghan M, Bowatte S, He J Z. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience, 2009, 2(9):621–624

    Article  CAS  Google Scholar 

  20. Verhamme D T, Prosser J I, Nicol G W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. The ISME journal, 2011, 5(6):1067–1071

    Article  CAS  Google Scholar 

  21. Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke B M, Matthies M, Smalla K, Munch J C, Amelung W, Kaupenjohann M, Schloter M, Schleper C. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environmental Microbiology, 2009, 11(2):446–456

    Article  CAS  Google Scholar 

  22. Zhao Z Q, Li S C, Gao J B, Wang Y L. Identifying spatial patterns and dynamics of climate change using recurrence quantification analysis: a case study of qinghai-tibet plateau. International Journal of Bifurcation and Chaos in Applied Sciences and Engineering, 2011, 21(04):1127–1139

    Article  Google Scholar 

  23. Xu X K, Chen H, Levy J K. Spatiotemporal vegetation cover variations in the Qinghai-Tibet Plateau under global climate change. Chinese Science Bulletin, 2008, 53(6):915–922

    Article  Google Scholar 

  24. Xu Z H, Chen C R, He J Z, Liu J X. Trends and challenges in soil research 2009: linking global climate change to local long-term forest productivity. Journal of Soils and Sediments, 2009, 9(2):83–88

    Article  Google Scholar 

  25. Francis C A, Roberts K J, Beman J M, Santoro A E, Oakley B B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(41):14683–14688

    Article  CAS  Google Scholar 

  26. Rotthauwe J H, Witzel K P, Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology, 1997, 63(12):4704–4712

    CAS  Google Scholar 

  27. He J Z, Shen J P, Zhang L M, Zhu Y G, Zheng Y M, Xu M G, Di H J. 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. Environmental Microbiology, 2007, 9(9):2364–2374

    Article  CAS  Google Scholar 

  28. Gubry-Rangin C, Nicol G W, Prosser J I. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiology Ecology, 2010, 74(3):566–574

    Article  CAS  Google Scholar 

  29. Mertens B, Boon N, Verstraete W. Stereospecific effect of hexachlorocyclohexane on activity and structure of soil methanotrophic communities. Environmental Microbiology, 2005, 7(5):660–669

    Article  CAS  Google Scholar 

  30. Wittebolle L, Vervaeren H, Verstraete W, Boon N. Quantifying community dynamics of nitrifiers in functionally stable reactors. Applied and Environmental Microbiology, 2008, 74(1):286–293

    Article  CAS  Google Scholar 

  31. Juretschko S, Timmermann G, Schmid M, Schleifer K H, Pommerening-Röser A, Koops H P, Wagner M. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Applied and Environmental Microbiology, 1998, 64(8):3042–3051

    CAS  Google Scholar 

  32. Adair K L, Schwartz E. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microbial Ecology, 2008, 56(3):420–426

    Article  CAS  Google Scholar 

  33. Stein L Y, Arp D J. Loss of ammonia monooxygenase activity in nitrosomonas europaea upon exposure to nitrite. Applied and Environmental Microbiology, 1998, 64(10):4098–4102

    CAS  Google Scholar 

  34. Wang X, Wen X, Criddle C, Yan H, Zhang Y, Ding K. Bacterial community dynamics in two full-scale wastewater treatment systems with functional stability. Journal of Applied Microbiology, 2010, 109(4):1218–1226

    Article  CAS  Google Scholar 

  35. Suzuki M T, Giovannoni S J. Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Applied and Environmental Microbiology, 1996, 62(2):625–630

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xianghua Wen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ding, K., Wen, X., Chen, L. et al. Abundance and distribution of ammonia-oxidizing archaea in Tibetan and Yunnan plateau agricultural soils of China. Front. Environ. Sci. Eng. 8, 693–702 (2014). https://doi.org/10.1007/s11783-014-0635-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11783-014-0635-3

Keywords

Navigation