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The Biogeography of Ammonia-Oxidizing Bacterial Communities in Soil

  • Soil Microbiology
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Abstract

Although ammonia-oxidizing bacteria (AOB) are likely to play a key role in the soil nitrogen cycle, we have only a limited understanding of how the diversity and composition of soil AOB communities change across ecosystem types. We examined 23 soils collected from across North America and used sequence-based analyses to compare the AOB communities in each of the distinct soils. Using 97% 16S rRNA sequence similarity groups, we identified only 24 unique AOB phylotypes across all of the soils sampled. The majority of the sequences collected were in the Nitrosospira lineages (representing 80% of all the sequences collected), and AOB belonging to Nitrosospira cluster 3 were particularly common in our clone libraries and ubiquitous across the soil types. Community composition was highly variable across the collected soils, and similar ecosystem types did not always harbor similar AOB communities. We did not find any significant correlations between AOB community composition and measures of N availability. From the suite of environmental variables measured, we found the strongest correlation between temperature and AOB community composition; soils exposed to similar mean annual temperatures tended to have similar AOB communities. This finding is consistent with previous studies and suggests that temperature selects for specific AOB lineages. Given that distinct AOB taxa are likely to have unique functional attributes, the biogeographical patterns exhibited by soil AOB may be directly relevant to understanding soil nitrogen dynamics under changing environmental conditions.

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References

  1. Martiny JBH, Bohannan BJM, Brown J, Colwell R, Fuhrman J, Green J, Horner-Devine M, Kane M, Krumins J, Kuske C, Morin P, Naeem S, Ovreas L, Reysenbach A, Smith V, Staley J (2006) Microbial biogeography: putting microorganisms on the map. Nature Rev Microbiol 4:102–112

    Article  CAS  Google Scholar 

  2. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: From taxonomy to traits. Science 320:1039–1043

    Article  PubMed  CAS  Google Scholar 

  3. Horner-Devine M, Lage M, Hughes J, Bohannan B (2004) A taxa-area relationship for bacteria. Nature 432:750–753

    Article  PubMed  CAS  Google Scholar 

  4. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: A model for molecular microbial ecology. Ann Rev Microbiol 55:485

    Article  CAS  Google Scholar 

  5. Purkhold U, Wagner M, Timmermann G, Pommerening-Roser A, Koops HP (2003) 16 S 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  PubMed  CAS  Google Scholar 

  6. 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 442:806–809

    Article  PubMed  CAS  Google Scholar 

  7. Prosser J, Nicol G (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–2941

    Article  PubMed  CAS  Google Scholar 

  8. Webster G, Embley TM, Freitag TE, Smith Z, Prosser JI (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7:676–684

    Article  PubMed  CAS  Google Scholar 

  9. Boyle-Yarwood S, Bottomley P, Myrold D (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10:2956–2965

    Article  PubMed  CAS  Google Scholar 

  10. Carney KM, Matson PA, Bohannan BJM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7:684–694

    Article  Google Scholar 

  11. 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  PubMed  CAS  Google Scholar 

  12. Shen J, Zhang L, Zhu Y, Zhang J, He J (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611

    Article  PubMed  CAS  Google Scholar 

  13. Avrahami S, Liesack W, Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5:691–705

    Article  PubMed  CAS  Google Scholar 

  14. Horz HP, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci USA 101:15136–15141

    Article  PubMed  CAS  Google Scholar 

  15. Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99–110

    Article  PubMed  CAS  Google Scholar 

  16. Chu HY, Fujii T, Morimoto S, Lin XG, Yagi K, Hu JL, Zhang JB (2007) Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Appl Environ Microbiol 73:485–491

    Article  PubMed  CAS  Google Scholar 

  17. Bottomley PJ, Taylor AE, Boyle SA, McMahon SK, Rich JJ, Cromack K, Myrold DD (2004) Responses of nitrification and ammonia-oxidizing bacteria to reciprocal transfers of soil between adjacent coniferous forest and meadow vegetation in the Cascade Mountains of Oregon. Microbial Ecol 48:500–508

    Article  CAS  Google Scholar 

  18. Avrahami S, Conrad R (2005) Cold-temperate climate: a factor for selection of ammonia oxidizers in upland soil? Can J Microbiol 51:709–714

    Article  PubMed  CAS  Google Scholar 

  19. McCaig AE, Glover LA, Prosser JI (2001) Numerical analysis of grassland bacterial community structure under different land management regimens by using 16 S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl Environ Microbiol 67:4554–4559

    Article  PubMed  CAS  Google Scholar 

  20. Bruns MA, Stephen JR, Kowalchuk GA, Prosser JI, Paul EA (1999) Comparative diversity of ammonia oxidizer 16 S rRNA gene sequences in native, tilled, and successional soils. Appl Environ Microbiol 65:2994–3000

    PubMed  CAS  Google Scholar 

  21. Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of beta-proteobacterial ammonia oxidizer populations. Appl Environ Microbiol 68:20–30

    Article  PubMed  CAS  Google Scholar 

  22. Fierer N, Jackson R (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  PubMed  CAS  Google Scholar 

  23. McCaig AE, Embley TM, Prosser JI (1994) Molecular analysis of enrichment cultures of marine ammonia oxidizers. FEMS Microbiol Lett 120:363–367

    Article  PubMed  CAS  Google Scholar 

  24. Kowalchuk GA, Stephen JR, DeBoer W, Prosser JI, Embley TM, Woldendorp JW (1997) Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16 S ribosomal DNA fragments. Appl Environ Microbiol 63:1489–1497

    PubMed  CAS  Google Scholar 

  25. DeSantis T, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006) NAST: a multiple sequence alignment server for comparative analysis of 16 S rRNA genes. Nucleic Acids Res 34:W394–399

    Article  PubMed  CAS  Google Scholar 

  26. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463

    Article  PubMed  CAS  Google Scholar 

  27. Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: A web-based bioinformatics platform for analyses of large 16 S rDNA libraries. BMC Bioinformatics 7:57

    Article  PubMed  CAS  Google Scholar 

  28. Colwell R (2005) EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5.<purl.oclc.org/estimates>.

  29. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Article  Google Scholar 

  30. Webb C, Ackerly D, Kembel S (2007) Phylocom: software for the analysis of community phylogenetic structure and character evolution. Version 3.41. http://www.phylodiversity.net/phylocom.

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

    Article  CAS  Google Scholar 

  32. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  PubMed  CAS  Google Scholar 

  33. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molec Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  34. Systat for Windows (2004) Systat Software version 11. Systat Software, Richmond

    Google Scholar 

  35. Rossello-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  CAS  Google Scholar 

  36. Avrahami S, Bohannan BJA (2007) Response of Nitrosospira sp strain AF-Like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173

    Article  PubMed  CAS  Google Scholar 

  37. Nugroho RA, Roling WFM, Laverman AM, Zoomer HR, Verhoef HA (2005) Presence of Nitrosospira cluster 2 bacteria corresponds to N transformation rates in nine acid Scots pine forest soils. FEMS Microbiol Ecol 53:473–481

    Article  PubMed  CAS  Google Scholar 

  38. Smith Z, McCaig AE, Stephen JR, Embley TM, Prosser JI (2001) Species diversity of uncultured and cultured populations of soil and marine ammonia oxidizing bacteria. Microbial Ecol 42:228–237

    Article  CAS  Google Scholar 

  39. Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiol Ecol 31:207–215

    Article  PubMed  CAS  Google Scholar 

  40. Hastings RC, Butler C, Singleton I, Saunders JR, McCarthy AJ (2000) Analysis of ammonia-oxidizing bacteria populations in acid forest soil during conditions of moisture limitation. Lett Appl Microbiol 30:14–18

    Article  PubMed  CAS  Google Scholar 

  41. Koops HP, Pommerening-Roser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37:1–9

    Article  CAS  Google Scholar 

  42. Hastings RC, Ceccherini MT, Miclaus N, Saunders JR, Bazzicalupo M, McCarthy AJ (1997) Direct molecular biological analysis of ammonia oxidising bacteria populations in cultivated soil plots treated with swine manure. FEMS Microbiol Ecol 23:45–54

    Article  CAS  Google Scholar 

  43. Phillips CJ, Harris D, Dollhopf SL, Gross KL, Prosser JI, Paul EA (2000) Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl Environ Microbiol 66:5410–5418

    Article  PubMed  CAS  Google Scholar 

  44. Fierer N (2008) Microbial biogeography: patterns in microbial diversity across space and time. In: Zengler K (ed) Accessing Uncultivated Microorganisms: from the Environment to Organisms and Genomes and Back. ASM Press, Washington DC, pp 95–115

    Google Scholar 

  45. Urakawa H, Tajima Y, Numata Y, Tsuneda S (2008) Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems. Appl Environ Microbiol 74:894–900

    Article  PubMed  CAS  Google Scholar 

  46. Avrahami S, Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microbiol 69:6152–6164

    Article  PubMed  CAS  Google Scholar 

  47. Jiang QQ, Bakken LR (1999) Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol Ecol 30:171–186

    Article  PubMed  CAS  Google Scholar 

  48. Anderson OE, Boswell FC, Harrison RM (1971) Variations in low temperature adaptability of nitrifiers in acid soils. Soil Sci Soc Amer Proc 35:68–71

    Article  CAS  Google Scholar 

  49. Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317

    Article  CAS  Google Scholar 

  50. Dalias P, Anderson JM, Bottner P, Couteaux MM (2002) Temperature responses of net nitrogen mineralization and nitrification in conifer forest soils incubated under standard laboratory conditions. Soil Biol Biochem 34:691–701

    Article  CAS  Google Scholar 

  51. Thamdrup B, Fleischer S (1998) Temperature dependence of oxygen respiration, nitrogen mineralization, and nitrification in Arctic sediments. Aquatic Microb Ecol 15:191–199

    Article  Google Scholar 

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Acknowledgements

We thank the many individuals who donated their time and resources to help with soil collection. We particularly want to thank Ben Colman for his help with the soil analyses. In addition, both Josh Schimel and Rob Jackson provided valuable logistical and intellectual support for this project. Four anonymous reviewers provided very useful comments on a previous draft of this manuscript. This work was supported by grants awarded to N.F. from the National Science Foundation (MCB 0610970) and the Andrew W. Mellon Foundation, a Smithsonian Institution Fellowship to K.C., and a National Science Foundation grant (DEB 0516400) to P.M.

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Correspondence to Noah Fierer.

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Fierer, N., Carney, K.M., Horner-Devine, M.C. et al. The Biogeography of Ammonia-Oxidizing Bacterial Communities in Soil. Microb Ecol 58, 435–445 (2009). https://doi.org/10.1007/s00248-009-9517-9

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  • DOI: https://doi.org/10.1007/s00248-009-9517-9

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