Biology and Fertility of Soils

, Volume 55, Issue 4, pp 419–424 | Cite as

Community shift of microbial ammonia oxidizers in air-dried rice soils after 22 years of nitrogen fertilization

  • Zhongjun JiaEmail author
  • Xiaojing Hu
  • Weiwei Xia
  • Dario Fornara
  • Paolo Nannipieri
  • James Tiedje
Short Communication


In this study, we show that composition shifts of ammonia oxidizer communities imposed by a 22-year field fertilization regime could be well retained in both fresh and air-dried soils. The abundance and composition of ammonia-oxidizing bacteria (AOB) and archaea (AOA) were measured in fresh soils, which received no fertilization (CK), chemical fertilization (NPK), and chemical plus organic matter fertilization (NPK/OM) for 22 years. The air-drying treatment of fresh soil was also conducted for pairwise analysis. We found that in fresh soils DGGE fingerprints of AOB showed significant changes under both NPK and NPK/OM treatments when compared with control (CK) and that microbial shift was almost identical in air-dried soils. Long-term nutrient fertilization did not affect AOA communities in either air-dried or fresh soils. Compared to CK treatment, real-time PCR indicated that AOB amoA genes increased significantly in fresh soils of NPK (59-fold) and NPK/OM (48-fold) plots and in air-dried NPK and NPK/OM soils by 22-fold and 19-fold respectively. Our results demonstrate that community shifts of AOB in fresh soils under chronic N fertilization could be well preserved in air-dried soils, despite the apparent decline in absolute abundance of ammonia oxidizers. These results suggest that air-dried soil could be a useful resource for deciphering the adaptive strategy of ammonia oxidizers under N enrichment when the significant changes of community composition occurred in fresh soils.


Air-dried soil Fresh soil Long-term fertilization Ammonia oxidizers 



We thank Prof. Penny Hirsch for constructive comments and suggestions. The authors also want to thank Dr. Yucheng WU, Xue ZHOU, and Baozhan WANG for technical support and the members of our lab for helpful discussion.

Funding information

This study was financially supported from the National Natural Science Foundation of China (41530857, 41501267, 41471208); the State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences (Y20160025); and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15040000).

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests

Supplementary material

374_2019_1352_MOESM1_ESM.docx (115 kb)
ESM 1 (DOCX 114 kb)


  1. Alves RJE, Minh BQ, Urich T, von Haeseler A, Schleper C (2018) Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun 9:1517CrossRefGoogle Scholar
  2. Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2:16242CrossRefGoogle Scholar
  3. Cary SC, Fierer N (2014) The importance of sample archiving in microbial ecology. Nat Rev Microbiol 12:789–790CrossRefGoogle Scholar
  4. Chu HY, Lin XG, Fujii T, Morimoto S, Yagi K, Hu JL, Zhang JB (2007) Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol Biochem 39:2971–2976Google Scholar
  5. Clark IM, Hirsch PR (2008) Survival of bacterial DNA and culturable bacteria in archived soils from the Rothamsted Broadbalk experiment. Soil Biol Biochem 40:1090–1102CrossRefGoogle Scholar
  6. Dadenko EV, Kazeev KS, Kolesnikov SI, Val'kov VF (2009) Changes in the enzymatic activity of soil samples upon their storage. Eurasian Soil Sci 42:1380–1385CrossRefGoogle Scholar
  7. Dolfing J, Feng YZ (2015) The importance of soil archives for microbial ecology. Nat Rev Microbiol 13:1Google Scholar
  8. Dolfing J, Vos A, Bloem J, Ehlert PAI, Naumova NB, Kuikman PJ (2004) Microbial diversity in archived soils. Science 306:813–813CrossRefGoogle Scholar
  9. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868CrossRefGoogle Scholar
  10. Feng YZ, Chen RR, Hu JL, Zhao F, Wang JH, Chu HY, Zhang JB, Dolfing J, Lin XG (2015) Bacillus asahii comes to the fore in organic manure fertilized alkaline soils. Soil Biol Biochem 81:186–194Google Scholar
  11. Galloway JN, Leach AM, Bleeker A, Erisman JW (2013) A chronology of human understanding of the nitrogen cycle. Philos Trans R Soc B 368:20130120CrossRefGoogle Scholar
  12. Gleeson DB, Müller C, Banerjee S, Ma W, Siciliano SD, Murphy DV (2010) Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Biol Biochem 42:1888–1891CrossRefGoogle Scholar
  13. Halverson LJ, Jones TM, Firestone MK (2000) Release of intracellular solutes by four soil bacteria exposed to dilution stress. Soil Sci Soc Am J 64:1630–1637CrossRefGoogle Scholar
  14. Kakumanu ML, Cantrell CL, Williams MA (2013) Microbial community response to varying magnitudes of desiccation in soil: a test of the osmolyte accumulation hypothesis. Soil Biol Biochem 57:644–653CrossRefGoogle Scholar
  15. Knapp CW, Dolfing J, Ehlert PAI, Graham DW (2009) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44:580–587CrossRefGoogle Scholar
  16. Koops HP, Purkhold U, Pommerening-Roser A, Timmermann G, Wagner M (2006) The lithoautotrophic ammonia-oxidizing bacteria. Prokaryotes 778–811Google Scholar
  17. Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Dunfield KE (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39:2977–2991CrossRefGoogle Scholar
  18. Liu R, Hayden HL, Suter H, Hu HW, Lam SK, He JZ, Mele PM, Chen DL (2017) The effect of temperature and moisture on the source of N2O and contributions from ammonia oxidizers in an agricultural soil. Biol Fertil Soils 53:141–152Google Scholar
  19. Pietramellara G, Ascher J, Borgogni F, Ceccherini MT, Guerri G, Nannipieri P (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45:219–235CrossRefGoogle Scholar
  20. Placella SA, Firestone MK (2013) Transcriptional response of nitrifying communities to wetting of dry soil. Appl Environ Microbiol 79:3294–3302CrossRefGoogle Scholar
  21. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805Google Scholar
  22. Rotthauwe J, Witzel K, 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 63:4704–4712Google Scholar
  23. Salonius PO (1983) Effects of air drying on the respiration of forest soil microbial populations. Soil Biol Biochem 15:199–203CrossRefGoogle Scholar
  24. Thomson BC, Ostle NJ, McNamara NP, Whiteley AS, Griffiths RI (2010) Effects of sieving, drying and rewetting upon soil bacterial community structure and respiration rates. J Microbiol Methods 83:69–73CrossRefGoogle Scholar
  25. Turner BL, Driessen JP, Haygarth PM, Mckelvie ID (2003) Potential contribution of lysed bacterial cells to phosphorus solubilisation in two rewetted Australian pasture soils. Soil Biol Biochem 35:187–189CrossRefGoogle Scholar
  26. Wang Q, Liu YR, Zhang CJ, Zhang LM, Han LL, Shen JP, He JZ (2017) Responses of soil nitrous oxide production and abundances and composition of associated microbial communities to nitrogen and water amendment. Biol Fertil Soils 53:601–611CrossRefGoogle Scholar
  27. Wessén 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 45:193–200CrossRefGoogle Scholar
  28. 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 75:1431–1439Google Scholar
  29. Zornoza R, Guerrero C, Mataix-Solera J, Arcenegui V, Garcia-Renes F, Mataix-Beneyto J (2007) Assessing the effects of air-drying and rewetting pre-treatment on soil microbial biomass, basal respiration, metabolic quotient and soluble carbon under Mediterranean conditions. Eur J Soil Biol 43:120–129CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zhongjun Jia
    • 1
    Email author
  • Xiaojing Hu
    • 1
  • Weiwei Xia
    • 2
  • Dario Fornara
    • 3
  • Paolo Nannipieri
    • 4
  • James Tiedje
    • 5
  1. 1.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingPeople’s Republic of China
  2. 2.Jiangsu Key Laboratory of Agricultural Meteorology, College of Applied MeteorologyNanjing University of Information Science and TechnologyNanjingPeople’s Republic of China
  3. 3.Agri-Food and Biosciences InstituteBelfastUK
  4. 4.Department of Agrifood Production and Environmental SciencesUniversity of FlorenceFlorenceItaly
  5. 5.Center for Microbial EcologyMichigan State UniversityEast LansingUSA

Personalised recommendations