Skip to main content

Advertisement

SpringerLink
Log in

Distribution of ammonia-oxidizing archaea and bacteria in plateau soils across different land use types

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Ammonia oxidation is known to be performed by both ammonia-oxidizing archaea (AOA) and bacteria (AOB), although their relative significance to nitrification process in soil ecosystems remains controversial. The distribution of AOA and AOB in plateau soils with different land use types and the influential factors remains unclear. The present study investigated the abundance and structure of AOA and AOB communities in upland soils adjacent to Erhai Lake in the Yunnan Plateau (China). Quantitative PCR assays indicated a large variation in the community size of AOA and AOB communities, with the numerical dominance of AOA over AOB in most of soils. Clone library analysis illustrated a marked shift in the structure of soil AOA and AOB communities. A high abundance of Nitrososphaera- and Nitrosotalea-like AOA was observed, while Nitrosospira-like species predominated in AOB. AOA and AOB abundance was positively influenced by total nitrogen and moisture content, respectively. Moreover, moisture content might be a key determinant of AOA community composition, while C/N and nitrate nitrogen played an important role in shaping AOB community composition. However, further efforts will be necessary in order to elucidate the links between soil AOA and AOB and land use.

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

  • Chen YL, Xu ZW, Hu HW, Hu YJ, Hao ZP, Jiang Y, Chen BD (2013) Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl Soil Ecol 68:36–45

    Article  Google Scholar 

  • Dey R, Pal KK, Tilak KVBR (2012) Influence of soil and plant types on diversity of rhizobacteria. Proc Nat Acad Sci India Sect B-Biol Sci 82:341–352

    Article  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 

  • Dindaroglu T, Reis M, Akay AE, Tonguc F (2015) Hydroecological approach for determining the width of riparian buffer zones for providing soil conservation and water quality. Int J Environ Sci Technol 12:275–284

    Article  Google Scholar 

  • Ding K, Wen XH, Chen L, Huang DS, Fei F, Li YY (2014) Abundance and distribution of ammonia-oxidizing archaea in Tibetan and Yunnan plateau agricultural soils of China. Front Env Sci Eng 8:693–702

    Article  CAS  Google Scholar 

  • Fahrenfeld N, Cozzarelli IM, Bailey Z, Pruden A (2014) Insights into biodegradation through depth-resolved microbial community functional and structural profiling of a crude-oil contaminant plume. Microb Ecol 68:453–462

    Article  CAS  PubMed  Google Scholar 

  • Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A (2010) Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74:575–591

    Article  CAS  PubMed  Google Scholar 

  • He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, 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  PubMed  Google Scholar 

  • Hofferle S, Nicol GW, Pal L, Hacin J, Prosser JI, Mandic-Mulec I (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile. FEMS Microbiol Ecol 74:302–315

    Article  CAS  PubMed  Google Scholar 

  • Hu BL, Liu SA, Shen LD, Zheng P, Xu XY, Lou LP (2012) Effect of different ammonia concentrations on community succession of ammonia-oxidizing microorganisms in a simulated paddy soil column. PLoS One 7, e44122

    Article  CAS  Google Scholar 

  • Hu BL, Liu S, Wang W, Shen LD, Lou LP, Liu WP, Tian GM, Xu XY, Zheng P (2014) pH-dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. FEMS Microbiol Ecol 90:290–299

    Article  CAS  Google Scholar 

  • Jiang HC, Huang LQ, Deng Y, Wang S, Zhou Y, Liu L, Dong HL (2014) Latitudinal distribution of ammonia-oxidizing bacteria and archaea in the agricultural soils of Eastern China. Appl Environ Microbiol 80:5593–5602

    Article  PubMed Central  PubMed  Google Scholar 

  • Ke XB, Lu YH (2012) Adaptation of ammonia-oxidizing microorganisms to environment shift of paddy field soil. FEMS Microbiol Ecol 80:87–97

    Article  CAS  PubMed  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  • Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci U S A 108:15892–15897

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lehtovirta-Morley LE, Ge CR, Ross J, Yao HY, Nicol GW, Prosser JI (2014) Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. FEMS Microbiol Ecol 89:542–552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li XR, Xiao YP, RenWW LZF, Shi JH, Quan ZX (2012) Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze River estuary. J Zhejiang Univ-SCI B 13:769–782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Y, Zhang JX, Zhang XL, Xie SG (2014) Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Appl Microbiol Biotechnol 98:5697–5707

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang JX, Zhao L, Li YZ, Dai Y, Xie SG (2015) Distribution of sediment ammonia-oxidizing microorganisms in plateau freshwater lakes. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-6341-z

    Google Scholar 

  • Long X, Chen CR, Xu ZH, Linder S, He JZ (2012) Abundance and community structure of ammonia oxidizing bacteria and archaea in a Sweden boreal forest soil under 19-year fertilization and 12-year warming. J Soils Sediments 12:1124–1133

    Article  CAS  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371

    Article  PubMed Central  PubMed  Google Scholar 

  • Meyer A, Focks A, Radl V, Welzl G, Schoning I, Schloter M (2014) Influence of land use intensity on the diversity of ammonia oxidizing bacteria and archaea in soils from grassland ecosystems. Microb Ecol 67:161–166

    Article  CAS  PubMed  Google Scholar 

  • Mintie AT, Heichen RS, Cromack K, Myrold DD, Bottomley PJ (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Appl Environ Microbiol 69:3129–3136

    Article  CAS  PubMed Central  PubMed  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 

  • Paranychianakis NV, Tsiknia M, Giannakis G, Nikolaidis NP, Kalogerakis N (2013) Nitrogen cycling and relationships between ammonia oxidizers and denitrifiers in a clay–loam soil. Appl Microbiol Biotechnol 97:5507–5515

    Article  CAS  PubMed  Google Scholar 

  • Park HD, Noguera DR (2007) Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations. J Appl Microbiol 102:1401–1417

    Article  CAS  PubMed  Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

    Article  CAS  PubMed  Google Scholar 

  • Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Purkhold U, Wagner M, Timmermann G, Pommerening-Roser A, Koops HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the Nitrosomonads. Int J Syst Evol Microbiol 53:1485–1494

    Article  CAS  PubMed  Google Scholar 

  • Qin HL, Yuan HZ, Zhang H, Zhu YJ, Yin CM, Tan ZJ, Wu JS, Wei WX (2013) Ammonia-oxidizing archaea are more important than ammonia-oxidizing bacteria in nitrification and NO3 −–N loss in acidic soil of sloped land. Biol Fertil Soils 49:767–776

    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 Environ Microbiol 75:7537–7754

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stroobants A, Degrune F, Olivier C, Muys C, Roisin C, Colinet G, Bodson B, Portetelle D, Vandenbol M (2014) Diversity of bacterial communities in a profile of a winter wheat field: known and unknown members. Microb Ecol 68:822–833

    Article  CAS  PubMed  Google Scholar 

  • Szukics U, Hackl E, Zechmeister-Boltenstern S, Sessitsch A (2012) Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiol Res 167:103–109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6, Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thion C, Prosser JI (2014) Differential response of nonadapted ammonia-oxidising archaea and bacteria to drying-rewetting stress. FEMS Microbiol Ecol 90:380–389

    CAS  PubMed  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, EngelM SM, WagnerM RA (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Urakawa H, Garcia JC, Nielsen JL, Le VQ, Kozlowski JA, Stein LY, Lim CK, Pommerening-Roser A, Martens-Habbena W, Stahl DA, Klotz MG (2015) Nitrosospira lacus sp. nov., a psychrotolerant, ammonia-oxidizing bacterium from sandy lake sediment. Int J Syst Evol Microbiol 65:242–250

    Article  PubMed  Google Scholar 

  • Vasileiadis S, Coppolecchia D, Puglisi E, Balloi A, Mapelli F, Hamon RE, Daffonchio D, Trevisan M (2012) Response of ammonia oxidizing bacteria and archaea to acute zinc stress and different moisture regimes in soil. Microb Ecol 64:1028–1037

    Article  CAS  PubMed  Google Scholar 

  • Wan R, Yang YY, Sun WM, Wang Z, Xie SG (2014a) Simazine biodegradation and community structures of ammonia-oxidizing microorganisms in bioaugmented soil: impact of ammonia and nitrate nitrogen sources. Environ Sci Pollut Res 21:3175–3181

    Article  CAS  Google Scholar 

  • Wan R, Wang Z, Xie SG (2014b) Dynamics of communities of bacteria and ammonia-oxidizing microorganisms in response to simazine attenuation in agricultural soil. Sci Total Environ 472:502–508

    Article  CAS  PubMed  Google Scholar 

  • Wang YF, Gu JD (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97:7015–7033

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang A, Wu FZ, Yang WQ, Wu ZC, Wang XX, Tan B (2012) Abundance and composition dynamics of soil ammonia-oxidizing archaea in an alpine fir forest on the eastern Tibetan Plateau of China. Can J Microbiol 58:572–580

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Wang C, Bao LL, Xie SG (2014a) Abundance and community structure of ammonia-oxidizing microorganisms in reservoir sediment and adjacent soils. Appl Microbiol Biotechnol 98:1883–1892

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wang WD, Gu JD (2014b) Community structure and abundance of ammonia-oxidizing archaea and bacteria after conversion from soybean to rice paddy in albic soils of Northeast China. Appl Microbiol Biotechnol 98:2765–2778

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Wang C, Bao LL, Xie SG (2014c) Impact of carbon source amendment on ammonia-oxidizing microorganisms in reservoir riparian soil. Ann Microbiol. doi:10.1007/s13213-014-0979-8

    PubMed Central  PubMed  Google Scholar 

  • Wertz S, Leigh AKK, Grayston SJ (2012) Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79:142–154

    Article  CAS  PubMed  Google Scholar 

  • Wessen E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45:193–200

    Article  Google Scholar 

  • Xu YG, Yu WT, Ma Q, Zhou H (2012) Responses of bacterial and archaeal ammonia oxidisers of an acidic luvisols soil to different nitrogen fertilization rates after 9 years. Biol Fertil Soils 48:827–837

    Article  CAS  Google Scholar 

  • Yang YY, Shan JW, Zhang JX, Zhang XL, Xie SG, Liu Y (2014) Ammonia- and methane-oxidizing microorganisms in high-altitude wetland sediments and adjacent agricultural soils. Appl Microbiol Biotechnol 98:10197–10209

    Article  CAS  PubMed  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:SI2545–SI2556

    Article  Google Scholar 

  • Zhao DY, Luo J, Wang JQ, Huang R, Guo K, Li Y, Wu QLL (2015) The influence of land use on the abundance and diversity of ammonia oxidizers. Curr Microbiol 70:282–289

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Yang W, Hu HW, Kim YC, Duan JC, Luo CY, Wang SP, Guo LD (2014) Ammonia oxidizers and denitrifiers in response to reciprocal elevation translocation in an alpine meadow on the Tibetan Plateau. J Soils Sediments 14:1189–1199

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (14Y02ESPCP) and National Natural Science Foundation of China (No. 51279001).

Ethical statement

No conflict of interest exits in the submission of this manuscript, and the manuscript is approved by all authors for publication. I would like to declare on behalf of my co-authors that the work described was an original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part.

Author information

Author notes

    Authors and Affiliations

    1. State Key Joint Laboratory of Environmental Simulation and Pollution Control, College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, China

      Jingxu Zhang, Yu Dai & Shuguang Xie

    2. Key Laboratory of Water and Sediment Sciences (Ministry of Education), College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, China

      Yilin Wang, Zhen Wu & Yong Liu

    Authors
    1. Jingxu Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Yu Dai
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Yilin Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Zhen Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Shuguang Xie
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Yong Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Shuguang Xie or Yong Liu.

    Additional information

    Jingxu Zhang and Yu Dai contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    ESM 1

    (PDF 67 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhang, J., Dai, Y., Wang, Y. et al. Distribution of ammonia-oxidizing archaea and bacteria in plateau soils across different land use types. Appl Microbiol Biotechnol 99, 6899–6909 (2015). https://doi.org/10.1007/s00253-015-6625-y

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00253-015-6625-y

    Keywords

    Search

    Navigation