Microbial Ecology

, Volume 76, Issue 4, pp 1041–1052 | Cite as

Different Recovery Processes of Soil Ammonia Oxidizers from Flooding Disturbance

  • Fei Ye
  • Mao-Hua Ma
  • Huub J. M. Op den Camp
  • Antonis Chatzinotas
  • Lei Li
  • Ming-Quan Lv
  • Sheng-Jun WuEmail author
  • Yu WangEmail author
Soil Microbiology


Understanding how microorganisms respond to environmental disturbance is one of the key focuses in microbial ecology. Ammonia-oxidizing bacteria (AOB) and archaea (AOA) are responsible for ammonia oxidation which is a crucial step in the nitrogen cycle. Although the physiology, distribution, and activity of AOA and AOB in soil have been extensively investigated, their recovery from a natural disturbance remains largely unknown. To assess the recovery capacities, including resistance and resilience, of AOA and AOB, soil samples were taken from a reservoir riparian zone which experienced periodically water flooding. The samples were classified into three groups (flooding, recovery, and control) for a high-throughput sequencing and quantitative PCR analysis. We used a relative quantitative index of both the resistance (RS) and resilience (RL) to assess the variation of gene abundance, alpha-diversity, and community composition. The AOA generally demonstrated a better recovery capability after the flooding disturbance compared to AOB. In particular, AOA were more resilient after the flooding disturbance. Taxa within the AOA and AOB showed different RS and RL values, with the most abundant taxa showing in general the highest RS indices. Soil NH4+ and Fe2+/Fe3+ were the main variables controlling the key taxa of AOA and AOB and probably influenced the resistance and resilience properties of AOA and AOB communities. The distinct mechanisms of AOA and AOB in maintaining community stability against the flooding disturbance might be linked to the different life-history strategies: the AOA community was more likely to represent r-strategists in contrast to the AOB community following a K-life strategy. Our results indicated that the AOA may play a vital role in ammonia oxidation in a fluctuating habitat and contribute to the stability of riparian ecosystem.


Archaea Ammonia-oxidizing communities Response Resistance Resilience Riparian zone 



This work was supported by the National Natural Science Foundation of China [41303053, 41571497, 41301540]. We are grateful to the Kaizhou Science & Technology Commission for the assistance in sampling and background data collection.

Supplementary material

248_2018_1183_MOESM1_ESM.doc (1.6 mb)
ESM 1 (DOC 1613 kb)


  1. 1.
    Rykiel EJ (1985) Towards a definition of ecological disturbance. Aust. J. Ecol. 10:361–365. CrossRefGoogle Scholar
  2. 2.
    Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JBH, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545. CrossRefGoogle Scholar
  4. 4.
    Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology: theory and practice. Ecology 65:1–13. CrossRefGoogle Scholar
  5. 5.
    Collie JS, Richardson K, Steele JH (2004) Regime shifts: can ecological theory illuminate the mechanisms? Prog. Oceanogr. 60:281–302. CrossRefGoogle Scholar
  6. 6.
    Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–581. CrossRefGoogle Scholar
  7. 7.
    Meyer AF, Lipson DA, Martin AP, Schadt CW, Schmidt SK (2004) Molecular and metabolic characterization of cold-tolerant alpine soil Pseudomonas sensu stricto. Appl. Environ. Microbiol. 70:483–489. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Allison SD, Martiny JBH (2008) Colloquium paper: resistance, resilience, and redundancy in microbial communities. PNAS 105:11512–11519. CrossRefPubMedGoogle Scholar
  9. 9.
    Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 37:112–129. CrossRefPubMedGoogle Scholar
  10. 10.
    Karakoç C, Singer A, Johst K, Harms H, Chatzinotas A (2017) Transient recovery dynamics of a predator–prey system under press and pulse disturbances. BMC Ecol. 17:13. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    IPCC (2007) Climate Change 2007: synthesis report. In: Pachauri, RK and Reisinger, A (eds) Contribution of working groups I, II and III to the fourth assessment report of the Intergovernmental Panel on Climate Changed. IPCC, Geneva, Switzerland, pp 104Google Scholar
  12. 12.
    You J, Das A, Dolan EM, Hu ZQ (2009) Ammonia-oxidizing archaea involved in nitrogen removal. Water Res. 43:1801–1809. CrossRefPubMedGoogle Scholar
  13. 13.
    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. CrossRefPubMedGoogle Scholar
  14. 14.
    Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. PNAS 105:2134–2139. CrossRefPubMedGoogle Scholar
  15. 15.
    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. PNAS 102:14683–14688. CrossRefPubMedGoogle Scholar
  16. 16.
    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 442:806–809. CrossRefPubMedGoogle Scholar
  17. 17.
    Yang F, Liu WW, Wang J, Liao L, Wang Y (2012) Riparian vegetation’s responses to the new hydrological regimes from the Three Gorges Project: clues to revegetation in reservoir water-level-fluctuation zone. Acta Ecol. Sin. 32:89–98. CrossRefGoogle Scholar
  18. 18.
    Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11:1658–1671. CrossRefPubMedGoogle Scholar
  19. 19.
    Nicol GW, Schleper C (2006) Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol. 14:207–212. CrossRefPubMedGoogle Scholar
  20. 20.
    He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, 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. CrossRefPubMedGoogle Scholar
  21. 21.
    Santoro AE, Francis CA, De Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ. Microbiol. 10:1068–1079. CrossRefPubMedGoogle Scholar
  22. 22.
    de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10:810–818. CrossRefPubMedGoogle Scholar
  23. 23.
    Thion C, Prosser JI (2014) Differential response of nonadapted ammonia-oxidising archaea and bacteria to drying-rewetting stress. FEMS Microbiol. Ecol. 90:380–389. CrossRefPubMedGoogle Scholar
  24. 24.
    Liu S, Hu BL, He ZF, Zhang B, Tian GM, Zheng P, Fang F (2015) Ammonia-oxidizing archaea have better adaptability in oxygenated/hypoxic alternant conditions compared to ammonia-oxidizing bacteria. Appl Microbiol Biotechnol 99:8587–8596. CrossRefPubMedGoogle Scholar
  25. 25.
    China Three Gorges Corporation (2017) Brief introduction of Three Gorges Corporation. Accessed 1 Mar 2017
  26. 26.
    Bao YH, Gao P, He XB (2015) The water-level fluctuation zone of Three Gorges Reservoir—a unique geomorphological unit. Earth-Sci. Rev. 150:14–24. CrossRefGoogle Scholar
  27. 27.
    Wen Z, Ma M, Zhang C, Yi X, Chen J, Wu S (2017) Estimating seasonal aboveground biomass of a riparian pioneer plant community: an exploratory analysis by canopy structural data. Ecol. Indic. 83:441–450. CrossRefGoogle Scholar
  28. 28.
    Ye C, Li SY, Yang YY, Xiao S, Zhang JQ, Zhang QF (2015) Advancing analysis of spatio-temporal variations of soil nutrients in the water level fluctuation zone of China’s Three Gorges Reservoir using self-organizing map. PLoS One 10:e0121210. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Stumm W, Sulzberger B (1992) The cycling of iron in natural environments: considerations based on laboratory studies of heterogeneous redox processes. Geochim Cosmochim Acta 56:3233–3257. CrossRefGoogle Scholar
  30. 30.
    Zheng GD, Takano B, Kuno A, Matsuo M (2001) Iron speciation in modern sediment from Erhai Lake, southwestern China: redox conditions in an ancient environment. Appl. Geochem. 16:1201–1213. CrossRefGoogle Scholar
  31. 31.
    Dean WE (1974) Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. J. Sediment. Res. 44:242–248. CrossRefGoogle Scholar
  32. 32.
    Bao SD (2000) Chemical analysis for agricultural soil. China Agriculture Press, Beijing (In Chinese)Google Scholar
  33. 33.
    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. 63:4704–4712PubMedPubMedCentralGoogle Scholar
  34. 34.
    Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 14:525–539. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Norton JM, Alzerreca JJ, Suwa Y, Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch. Microbiol. 177:139–149. CrossRefPubMedGoogle Scholar
  36. 36.
    Xiang XJ, He D, He JS, Myrold DD, Chu HY (2017) Ammonia-oxidizing bacteria rather than archaea respond to short-term urea amendment in an alpine grassland. Soil Biol. Biochem. 107:218–225. CrossRefGoogle Scholar
  37. 37.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731–2739. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    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. CrossRefGoogle Scholar
  39. 39.
    Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol. Biochem. 96:4–15. CrossRefGoogle Scholar
  40. 40.
    Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops HP, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol. Biochem. 36:1907–1912. CrossRefGoogle Scholar
  42. 42.
    Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310. CrossRefPubMedGoogle Scholar
  43. 43.
    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 461:976–979. CrossRefPubMedGoogle Scholar
  44. 44.
    Ke X, Lu Y (2012) Adaptation of ammonia-oxidizing microorganisms to environment shift of paddy field soil. FEMS Microbiol. Ecol. 80:87–97. CrossRefPubMedGoogle Scholar
  45. 45.
    Xie Z, Le Roux X, Wang CP, Gu ZK, An M, Nan HY, Chen BZ, Li F, Liu YJ, Du GZ, Feng HY, Ma XJ (2014) Identifying response groups of soil nitrifiers and denitrifiers to grazing and associated soil environmental drivers in Tibetan alpine meadows. Soil Biol. Biochem. 77:89–99. CrossRefGoogle Scholar
  46. 46.
    Lee SH, Sorensen JW, Grady KL, Tobin TC, Shade A (2017) Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fire. ISME J 11:1447–1459. CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Griffiths BS, Ritz K, Bardgett RD, Cook R, Christensen S, Ekelund F, Sørensen SJ, Bååth E, Bloem J, Ruiter PCD (2000) Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90:279–294. CrossRefGoogle Scholar
  48. 48.
    Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326. CrossRefGoogle Scholar
  49. 49.
    Chen J, Nie YX, Liu W, Wang ZF, Shen WJ (2017) Ammonia-oxidizing archaea are more resistant than denitrifiers to seasonal precipitation changes in an acidic subtropical forest soil. Front Microbiol 8:1384. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Ng EL, Patti AF, Rose MT, Schefe CR, Smernik RJ, Cavagnaro TR (2015) Do organic inputs alter resistance and resilience of soil microbial community to drying? Soil Biol Biochem 81:58–66. CrossRefGoogle Scholar
  51. 51.
    Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784.[0777:Tuossp]2.0.Co;2CrossRefGoogle Scholar
  52. 52.
    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. CrossRefGoogle Scholar
  53. 53.
    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. CrossRefPubMedGoogle Scholar
  54. 54.
    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. CrossRefPubMedGoogle Scholar
  55. 55.
    de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265. CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Fetzer I, Johst K, Schäwe R, Banitz T, Harms H, Chatzinotas A (2015) The extent of functional redundancy changes as species’ roles shift in different environments. PNAS 112:14888–14893. CrossRefPubMedGoogle Scholar
  57. 57.
    de Vries FT, Liiri ME, Bjørnlund L, Bowker MA, Christensen S, Setälä HM, Bardgett RD (2012) Land use alters the resistance and resilience of soil food webs to drought. Nat. Clim. Chang. 2:276–280. CrossRefGoogle Scholar
  58. 58.
    De Leij FA, Whipps JM, Lynch JM (1994) The use of colony development for the characterization of bacterial communities in soil and on roots. Microb Ecol 27:81–97. CrossRefPubMedGoogle Scholar
  59. 59.
    Langer U, Böhme L, Böhme F (2004) Classification of soil microorganisms based on growth properties: a critical view of some commonly used terms. J Plant Nutr Soil Sci 167:267–269. CrossRefGoogle Scholar
  60. 60.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Bapiri A, Baath E, Rousk J (2010) Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microb. Ecol. 60:419–428. CrossRefPubMedGoogle Scholar
  62. 62.
    Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879. CrossRefPubMedGoogle Scholar
  63. 63.
    Wang YF, Gu JD (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl. Environ. Microbiol. 97:7015–7033. CrossRefGoogle Scholar
  64. 64.
    Wang SY, Wang Y, Feng XJ, Zhai LM, Zhu GB (2011) Quantitative analyses of ammonia-oxidizing archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol 90:779–787. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Chongqing Institute of Green and Intelligent TechnologyChinese Academy of SciencesChongqingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Microbiology, IWWRRadboud University NijmegenNijmegenthe Netherlands
  4. 4.Department of Environmental MicrobiologyHelmholtz Centre for Environmental Research-UFZLeipzigGermany
  5. 5.Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  6. 6.Beijing Academy of Science and TechnologyBeijingChina

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