Journal of Soils and Sediments

, Volume 13, Issue 8, pp 1439–1449 | Cite as

pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing

  • Hang-Wei Hu
  • Li-Mei Zhang
  • Yu Dai
  • Hong-Jie Di
  • Ji-Zheng He
SOILS, SEC 5 • SOIL AND LANDSCAPE ECOLOGY • RESEARCH ARTICLE

Abstract

Purpose

Ammonia-oxidizing archaea (AOA) and bacteria (AOB) are ubiquitous and important for nitrogen transformations in terrestrial ecosystems. However, the distribution patterns of these microorganisms as affected by the terrestrial environments across a large geographical scale are not well understood. This study was designed to gain insights into the ecological characteristics of AOA and AOB in 65 soils, collected from a wide range of soil and ecosystem types.

Materials and methods

Barcoded pyrosequencing in combination with quantitative PCR was employed to characterize the relative abundance, diversity, and community composition of archaeal 16S rRNA gene, and AOA and AOB amoA genes in 65 soil samples.

Results and discussion

The operational taxonomic unit richness and Shannon diversity of Thaumarchaeota, AOA, and AOB were highly variable among different soils, but their variations were best explained by soil pH. Soil pH was strongly correlated with the overall community composition of ammonia oxidizers, as measured by the pairwise Bray–Curtis dissimilarity across all sites. These findings were further corroborated by the evident pH-dependent distribution patterns of four thaumarchaeal groups (I.1a-associated, I.1b, I.1c, and I.1c-associated) and four AOB clusters (2, 3a.1, 10, and 12). The ratios of AOA to AOB amoA gene copy numbers significantly decreased with increasing pH, suggesting a competitive advantage of AOA over AOB in acidic soils.

Conclusions

These results suggest that the distribution of ammonia oxidizers across large-scale biogeographical settings can be largely predicted along the soil pH gradient, thus providing important indications for the ecological characteristics of AOA and AOB in different soils.

Keywords

454 Pyrosequencing Ammonia oxidizers Nitrogen cycling Soil pH Spatial distribution Thaumarchaeota 

Notes

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (41230857, 41171217, 41020114001, and 41025004). We are grateful to Profs. Linghao Li and Daizhang Wang, Dr. Wenyan Han for access to the field trial stations, and Drs. Yong Zheng, Huaiying Yao, Mei Yin, Qichun Zhang, Zili Yi, and Xianjun Liu for assistance in soil sampling.

Supplementary material

11368_2013_726_MOESM1_ESM.doc (165 kb)
ESM 1(DOC 165 kb)

References

  1. Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured archaea. ISME J 4:182–190CrossRefGoogle Scholar
  2. Bates ST, Berg-Lyons D, Caporaso JG et al (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917CrossRefGoogle Scholar
  3. Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157CrossRefGoogle Scholar
  4. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252CrossRefGoogle Scholar
  5. Cao P, Zhang LM, Shen JP et al (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol Ecol 80:146–158CrossRefGoogle Scholar
  6. Chen X, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil types determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516CrossRefGoogle Scholar
  7. 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 2:621–624CrossRefGoogle Scholar
  8. Di HJ, Cameron KC, Sherlock RR, Shen JP, He JZ, Winefield CS (2010) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J Soils Sediments 10:943–954CrossRefGoogle Scholar
  9. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869CrossRefGoogle Scholar
  10. 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 USA 102:14683–14688CrossRefGoogle Scholar
  11. Gubry-Rangin C, Hai B, Quince C et al (2012) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA 108:21206–21211CrossRefGoogle Scholar
  12. Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574CrossRefGoogle Scholar
  13. He JZ, Shen JP, Zhang LM et al (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 9:2364–2374CrossRefGoogle Scholar
  14. He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154CrossRefGoogle Scholar
  15. Höfferle Š, Nicol GW, Ausec L, Mulec I, Prosser JI (2012) Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol Ecol 80:114–123CrossRefGoogle Scholar
  16. Hu HW, Zhang LM, Yuan CL, He JZ (2013) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27CrossRefGoogle Scholar
  17. Huang R, Wu YC, Zhang JB, Zhong WH, Jia ZJ, Cai ZC (2012) Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils. J Soils Sediments 12:420–428CrossRefGoogle Scholar
  18. Kan J, Clingenpeel S, Macur RE et al (2011) Archaea in Yellowstone Lake. ISME J 5:1784–1795CrossRefGoogle Scholar
  19. Kemnitz D, Kolb S, Conrad R (2007) High abundance of Crenarchaeota in a temperate acidic forest soil. FEMS Microbiol Ecol 60:442–448CrossRefGoogle Scholar
  20. Kim JG, Jung MY, Park SJ et al (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ Microbiol 14:1528–1543CrossRefGoogle Scholar
  21. Könneke M, Bernhard AE, Torre JR et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefGoogle Scholar
  22. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120CrossRefGoogle Scholar
  23. 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 USA 108:15892–15897CrossRefGoogle Scholar
  24. Leininger S, Urich T, Schloter M et al (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809CrossRefGoogle Scholar
  25. Li JJ, Zheng YM, Yan JX, Li HJ, He JZ (2013) Succession of plant and soil microbial communities with restoration of abandoned land in the Loess Plateau, China. J Soils Sediments 13:760–769CrossRefGoogle Scholar
  26. Long XE, 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 12:1124–1133CrossRefGoogle Scholar
  27. Mincer TJ, Church MJ, Taylor LT et al (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162–1175CrossRefGoogle Scholar
  28. Nelson DM, Cann IKO, Mackie RL (2010) Response of archaeal communities in the rhizosphere of maize and soybean to elevated atmospheric CO2 concentrations. PLoS One 5:e15897CrossRefGoogle Scholar
  29. 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 10:2966–2978CrossRefGoogle Scholar
  30. Pester M, Rattei T, Flechl S et al (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539CrossRefGoogle Scholar
  31. Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306CrossRefGoogle Scholar
  32. Purkhold U, Pommerening-Roser A, Juretschko S et al (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 66:5368–5382CrossRefGoogle Scholar
  33. Quince C, Lanzen A, Curtis TP et al (2009) Noise and the accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639–641CrossRefGoogle Scholar
  34. Rosso L, Lobry JR, Bajard S, Flandrois JP (1995) Convenient model to describe the combined effects of temperature and pH on microbial growth. Appl Environ Microbiol 61:610–616Google Scholar
  35. 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 63:4704–4712Google Scholar
  36. Schleper C (2010) Ammonia oxidation: different niches for bacteria and archaea? ISME J 4:1092–1094CrossRefGoogle Scholar
  37. Schleper C, Nicol GW (2010) Ammonia-oxidizing archaea—physiology, ecology and evolution. Adv Microb Physiol 57:1–41CrossRefGoogle Scholar
  38. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  39. Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296Google Scholar
  40. Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611CrossRefGoogle Scholar
  41. Shen XY, Zhang LM, Shen JP, Li LH, Yuan CL, He JZ (2011) Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland. J Soils Sediments 11:1243–1252CrossRefGoogle Scholar
  42. Spang A, Hatzenpichler R, Brochier-Armanet C et al (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331–340CrossRefGoogle Scholar
  43. Stephen JR, Kowalchuk GA, Bruns MAV et al (1998) Analysis of β-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64:2958–2965Google Scholar
  44. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  45. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364CrossRefGoogle Scholar
  46. Tourna M, Stieglmeier M, Spang A et al (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425CrossRefGoogle Scholar
  47. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323CrossRefGoogle Scholar
  48. Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071CrossRefGoogle Scholar
  49. Walker CB, de la Torre JR, Klotz MG et al (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107:8818–8823CrossRefGoogle Scholar
  50. Ying JY, Zhang LM, He JZ (2010) Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environ Microbiol Rep 2:304–312CrossRefGoogle Scholar
  51. Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045CrossRefGoogle Scholar
  52. Zhang LM, Wang M, Prosser JI, Zheng YM, He JZ (2009) Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol Ecol 70:208–217CrossRefGoogle Scholar
  53. Zhang LM, Offre PR, He JZ et al (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci USA 107:17240–17245CrossRefGoogle Scholar
  54. Zheng YM, Cao P, Fu BJ, Hughes J, He JZ (2013) Ecological drivers 750 of biogeographic patterns of soil archaeal community. PLoS One 751 8(5):e63375. doi:10.1371/journal.pone.0063375 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Hang-Wei Hu
    • 1
    • 2
  • Li-Mei Zhang
    • 1
  • Yu Dai
    • 1
    • 2
  • Hong-Jie Di
    • 3
  • Ji-Zheng He
    • 1
  1. 1.State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  2. 2.Graduate SchoolChinese Academy of SciencesBeijingChina
  3. 3.Centre for Soil and Environmental ResearchLincoln UniversityChristchurchNew Zealand

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