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Applied Microbiology and Biotechnology

, Volume 102, Issue 19, pp 8561–8571 | Cite as

Diversity and community structure of ammonia oxidizers in a marsh wetland of the northeast China

  • Dawen Gao
  • Fengqin Liu
  • Lu Li
  • Chuhong Chen
  • Hong Liang
Environmental biotechnology

Abstract

As an interface of terrestrial and aquatic ecosystems, wetland is a hotspot of the global nitrogen cycle. Ammonia oxidation is an essential part of the nitrogen cycle and is conducted by ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). Based on the amoA gene, the distribution and genetic diversity of AOA and AOB in the marsh wetland soil with different soil layers and vegetation had been investigated. The result showed that both soil layer and vegetation significantly influenced the diversity and abundance of AOA and AOB. AOB dominated numerically in all soil samples. The average bacterial amoA gene copies (2.62 × 109 copies/g dry soil) was 100-fold higher than the average archaeal amoA gene copies. In the soil sample under the Phragmites australis, the highest archaeal amoA gene was in depth 20–40 cm, whereas the bacterial amoA gene was more abundant in depth 0–20 cm. For the soil under Calamagrostis angustifolia, the highest archaeal and bacterial amoA gene were both detected in depth 0–20 cm. The dominated AOA was cluster AII, which was most related to the amoA gene found in aquatic habitat. Cluster BI accounted for 59.1% of bacterial amoA gene and it was related to the amoA gene found in the terrestrial habitat. CCA analysis revealed that NO3 was the main factor for AOA and AOB community structure in the P. australis soil. However, NO2 and NH4+ were important factors for AOA and AOB in the soil under C. angustifolia.

Keywords

Ammonia-oxidizing archaea Ammonia-oxidizing bacteria Distribution Genetic diversity amoA gene 

Notes

Funding

This research was supported by the National Natural Science Foundation of China (No. 31470543) and the State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (2014DX07).

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alves RJE, Wanek W, Zappe A, Richter A, Svenning MM, Schleper C, Urich T (2013) Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea. ISME J 7(8):1620–1631CrossRefPubMedPubMedCentralGoogle Scholar
  2. Banning NC, Maccarone LD, Fisk LM, Murphy DV (2015) Ammonia-oxidising bacteria not archaea dominate nitrification activity in semi-arid agricultural soil. Sci Rep 5(1):11146–11146CrossRefPubMedPubMedCentralGoogle Scholar
  3. Che J, Zhao XQ, Zhou X, Jia ZJ, Shen RF (2015) High pH-enhanced soil nitrification was associated with ammonia-oxidizing bacteria rather than archaea in acidic soils. Appl Soil Ecol 85:21–29CrossRefGoogle Scholar
  4. Chen C-H, Gao D-W, Tao Y (2013) Diversity and distribution of ammonia-oxidizing Archaea in the seasonally frozen soils in northeastern China. Appl Microbiol Biotechnol 97(14):6571–6579CrossRefPubMedGoogle Scholar
  5. Di H, Cameron K, Shen JP, Winefield C, O’Callaghan M, Bowatte S, He J (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2(9):621–624CrossRefGoogle Scholar
  6. e Silva P, Poly F, Guillaumaud N, van Elsas JD, Salles JF (2012) Fluctuations in ammonia oxidizing communities across agricultural soils are driven by soil structure and pH. Front Microbiol 3:77CrossRefGoogle Scholar
  7. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33(5):855–869CrossRefPubMedGoogle Scholar
  8. Francis CA, O'Mullan GD, Ward BB (2003) Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1(2):129–140CrossRefGoogle Scholar
  9. 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. Proc Natl Acad Sci U S A 102(41):14683–14688CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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(3):575–591CrossRefPubMedGoogle Scholar
  11. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108(52):21206–21211CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hansen J, Andersen FO (1981) Effects of Phragmites australis roots and rhizomes on redox potentials, nitrification and bacterial numbers in the sediment. In: Proceedings of the 9th Nordic Symposium on Sediments. Scripta Limnologica Norr Malmo, Sweden, p 72–88Google Scholar
  13. He J-Z, Hu H-W, Zhang L-M (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154CrossRefGoogle Scholar
  14. Head IM, Hiorns WD, Embley TM, McCarthy AJ, Saunders JR (1993) The phylogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal RNA gene sequences. Microbiology 139(6):1147–1153Google Scholar
  15. Horak RE, Qin W, Schauer AJ, Armbrust EV, Ingalls AE, Moffett JW, Stahl DA, Devol AH (2013) Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J 7(10):2023–2033CrossRefPubMedPubMedCentralGoogle Scholar
  16. Huang R, Wu Y, Zhang J, Zhong W, Jia Z, Cai Z (2012) Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils. J Soils Sediments 12(3):420–428CrossRefGoogle Scholar
  17. Huang R, Zhao D, Zeng J, Luo J, Shen F, Cao X, Jiang C, Huang F, Feng J, Zhou C (2016) Abundance and community composition of ammonia oxidizers in rhizosphere sediment of two submerged macrophytes. J Freshw Ecol:1–13Google Scholar
  18. Hussain Q, Liu Y, Jin Z, Zhang A, Pan G, Li L, Crowley D, Zhang X, Song X, Cui L (2011) Temporal dynamics of ammonia oxidizer (amoA) and denitrifier (nirK) communities in the rhizosphere of a rice ecosystem from Tai Lake region, China. Appl Soil Ecol 48(2):210–218CrossRefGoogle Scholar
  19. Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11(7):1658–1671CrossRefPubMedGoogle Scholar
  20. Jiang X, Hou X, Zhou X, Xin X, Wright A, Jia Z (2015) pH regulates key players of nitrification in paddy soils. Soil Biol Biochem 81:9–16CrossRefGoogle Scholar
  21. Jin T, Zhang T, Yan Q (2010) Characterization and quantification of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in a nitrogen-removing reactor using T-RFLP and qPCR. Appl Microbiol Biotechnol 87(3):1167–1176CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kleineidam K, Košmrlj K, Kublik S, Palmer I, Pfab H, Ruser R, Fiedler S, Schloter M (2011) Influence of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 84(1):182–186CrossRefPubMedGoogle Scholar
  23. Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543–546CrossRefPubMedGoogle Scholar
  24. 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(38):15892–15897CrossRefPubMedPubMedCentralGoogle Scholar
  25. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G, Prosser J, Schuster S, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104):806–809CrossRefPubMedGoogle Scholar
  26. Li M, Gu J-D (2013) Community structure and transcript responses of anammox bacteria, AOA, and AOB in mangrove sediment microcosms amended with ammonium and nitrite. Appl Microbiol Biotechnol 97(22):9859–9874CrossRefPubMedGoogle Scholar
  27. Li H, Weng B-S, Huang F-Y, Su J-Q, Yang X-R (2015) pH regulates ammonia-oxidizing bacteria and archaea in paddy soils in Southern China. Appl Microbiol Biotechnol 99(14):6113–6123CrossRefPubMedGoogle Scholar
  28. Martens-Habbena W, Berube PM, Urakawa H, José R, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461(7266):976–979CrossRefPubMedGoogle Scholar
  29. Philippot L, Hallin S, Börjesson G, Baggs E (2009) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321(1–2):61–81CrossRefGoogle Scholar
  30. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531CrossRefPubMedGoogle Scholar
  31. Purkhold U, Wagner M, Timmermann G, Pommerening-Röser A, Koops H-P (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(5):1485–1494CrossRefPubMedGoogle Scholar
  32. Shen J-P, Zhang L-M, Di HJ, He J-Z (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3(3):296PubMedPubMedCentralGoogle Scholar
  33. Sims A, Horton J, Gajaraj S, McIntosh S, Miles RJ, Mueller R, Reed R, Hu Z (2012) Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands. Water Res 46(13):4121–4129CrossRefPubMedGoogle Scholar
  34. Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI (2016) Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol 92(7):fiw091CrossRefPubMedGoogle Scholar
  35. Trias R, Ruiz-Rueda O, García-Lledó A, Vilar-Sanz A, López-Flores R, Quintana XD, Hallin S, Bañeras L (2012) Emergent macrophytes act selectively on ammonia-oxidizing bacteria and archaea. Appl Environ Microbiol 78(17):6352–6356CrossRefPubMedPubMedCentralGoogle Scholar
  36. Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5(6):1067–1071CrossRefPubMedPubMedCentralGoogle Scholar
  37. Wang S, Wang Y, Feng X, Zhai L, Zhu G (2011) Quantitative analyses of ammonia-oxidizing Archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol 90(2):779–787CrossRefPubMedGoogle Scholar
  38. Ward BB, O'Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing γ-Proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environ Microbiol 68(8):4153–4157CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wei B, Yu X, Zhang S, Gu L (2011) Comparison of the community structures of ammonia-oxidizing bacteria and archaea in rhizoplanes of floating aquatic macrophytes. Microbiol Res 166(6):468–474CrossRefPubMedGoogle Scholar
  40. Wessén E, Hallin S, Philippot L (2010) Differential responses of bacterial and archaeal groups at high taxonomical ranks to soil management. Soil Biol Biochem 42(10):1759–1765CrossRefGoogle Scholar
  41. Zhang L-M, Hu H-W, Shen J-P, He J-Z (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6(5):1032–1045CrossRefPubMedGoogle Scholar
  42. Zhang J, Liu B, Zhou X, Chu J, Li Y, Wang M (2015) Effects of emergent aquatic plants on abundance and community structure of ammonia-oxidising microorganisms. Ecol Eng 81:504–513CrossRefGoogle Scholar
  43. Zhong W, Bian B, Gao N, Min J, Shi W, Lin X, Shen W (2016) Nitrogen fertilization induced changes in ammonia oxidation are attributable mostly to bacteria rather than archaea in greenhouse-based high N input vegetable soil. Soil Biol Biochem 93:150–159CrossRefGoogle Scholar
  44. Zhou L, Wang S, Zou Y, Xia C, Zhu G (2015) Species, abundance and function of ammonia-oxidizing Archaea in inland waters across China. Sci Rep 5(1):15969–15969CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhou X, Zhang J, Li Y, Liu B, Chu J, Wang M, He Z (2016) Distribution characteristics of ammonia oxidizing microorganisms in rhizosphere sediments of cattail. Ecol Eng 88:99–111CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Urban Water Resource and EnvironmentHarbin Institute of TechnologyHarbinChina
  2. 2.School of EnvironmentHarbin Institute of TechnologyHarbinChina

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