Skip to main content
Log in

Changes in Soil Bacterial Community Structure with Increasing Disturbance Frequency

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Little is known of the responsiveness of soil bacterial community structure to disturbance. In this study, we subjected a soil microcosm to physical disturbance, sterilizing 90 % of the soil volume each time, at a range of frequencies. We analysed the bacterial community structure using 454 pyrosequencing of the 16S rRNA gene. Bacterial diversity was found to decline with the increasing disturbance frequencies. Total bacterial abundance was, however, higher at intermediate and high disturbance frequencies, compared to low and no-disturbance treatments. Changing disturbance frequency also led to changes in community composition, with changes in overall species composition and some groups becoming abundant at the expense of others. Some phylogenetic groups were found to be relatively more disturbance-sensitive or tolerant than others. With increasing disturbance frequency, phylogenetic species variability (an index of community composition) itself became more variable from one sample to another, suggesting a greater role of chance in community composition. Compared to the tightly clustered community of the original undisturbed soil, in all the aged disturbed soils the lists of most abundant operational taxonomic units (OTUs) in each replicate were very different, suggesting a possible role of stochasticity in resource colonization and exploitation in the aged and disturbed soils. For example, colonization may be affected by whichever localized concentrations of bacterial populations happen to survive the last disturbance and be reincorporated in abundance into each pot. Overall, it appears that the soil bacterial community is very sensitive to physical disturbance, losing diversity, and that certain groups have identifiable ‘high disturbance’ vs. ‘low disturbance’ niches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Adler PB, Hillerislambers J, Levine JM (2007) A niche for neutrality. Ecol Lett 10:95–104

    Article  PubMed  Google Scholar 

  2. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519

    Article  PubMed  CAS  Google Scholar 

  3. Baath E (1998) Growth rates of bacterial communities in soils at varying pH: A comparison of the thymidine and leucine incorporation techniques. Microb Ecol 36:316–327

    Article  PubMed  CAS  Google Scholar 

  4. Borneman J, Triplett EW (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63:2647–2653

    PubMed  CAS  Google Scholar 

  5. Bowen JL et al (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5:1540–1548

    Article  PubMed  Google Scholar 

  6. Buckling A, Kassen R, Bell G, Rainey PB (2000) Disturbance and diversity in experimental microcosms. Nature 408:961–964

    Article  PubMed  CAS  Google Scholar 

  7. Chesson PL, Warner RR (1981) Environmental variability promotes coexistence in lottery competitive-systems. Am Nat 117:923–943

    Article  Google Scholar 

  8. Chun J, Kim KY, Lee JH, Choi Y (2010) The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 10:101

    Article  PubMed  Google Scholar 

  9. Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorials. Primer-E Ltd, Plymouth

    Google Scholar 

  10. Connell JH (1978) Diversity in tropical rain forests and coral reefs—high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199:1302–1310

    Article  PubMed  CAS  Google Scholar 

  11. DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77:6295–6300

    Article  PubMed  CAS  Google Scholar 

  12. Dewhirst FE et al (2010) The human oral microbiome. J Bacteriol 192:5002–5017

    Article  PubMed  CAS  Google Scholar 

  13. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  14. Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    Article  PubMed  CAS  Google Scholar 

  15. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409

    Article  PubMed  Google Scholar 

  16. Griffiths BS et al (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

    Article  Google Scholar 

  17. Grime JP (1973) Control of species density in herbaceous vegation. J Environ Manag 1:151–167

    Google Scholar 

  18. Grime JP (2001) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, Chichester

    Google Scholar 

  19. Haichar FZ et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  PubMed  CAS  Google Scholar 

  20. Helmus MR, Bland TJ, Williams CK, Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169

  21. Helmus MR, Keller WB, Paterson MJ, Yan ND, Cannon CH, Rusak JA (2010) Communities contain closely related species during ecosystem disturbance. Ecol Lett 13:162–174

    Article  PubMed  Google Scholar 

  22. Hugenholtz P, Tyson GW, Webb RI, Wagner AM, Blackall LL (2001) Investigation of candidate division TM7, a recently recognized major lineage of the domain Bacteria with no known pure-culture representatives. Appl Environ Microbiol 67:411–419

    Article  PubMed  CAS  Google Scholar 

  23. Huston M (1979) General hypothesis of species-diversity. Am Nat 113:81–101

    Article  Google Scholar 

  24. Huston MA (1994) Biological diversity: The coexistence of species on changing landscapes. Cambridge University Press, Cambridge

    Google Scholar 

  25. Ikeda H (2003) Testing the intermediate disturbance hypothesis on species diversity in herbaceous plant communities along a human trampling gradient using a 4-year experiment in an old-field. Ecol Res 18:185–197

    Article  Google Scholar 

  26. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  PubMed  CAS  Google Scholar 

  27. Kang SH, Mills AL (2004) Soil bacterial community structure changes following disturbance of the overlying plant community. Soil Sci 169:55–65

    Article  CAS  Google Scholar 

  28. Kembel SW et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  PubMed  CAS  Google Scholar 

  29. Kim OS et al (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  PubMed  CAS  Google Scholar 

  30. Langenheder S, Szekely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–1094

    Article  PubMed  Google Scholar 

  31. Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410

    Article  PubMed  Google Scholar 

  32. Lenssen JPM, van de Steeg HM, de Kroon H (2004) Does disturbance favour weak competitors? Mechanisms of changing plant abundance after flooding. J Veg Sci 15:305–314

    Google Scholar 

  33. 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 

  34. Lubchenco J, Menge BA (1978) Community-development and persistence in a low rocky inter-tidal zone. Ecol Monogr 48:67–94

    Article  Google Scholar 

  35. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  36. Mcardle BH, Gaston KJ, Lawton JH (1990) Variation in the size of animal populations—patterns, problems and artifacts. J Anim Ecol 59:439–454

    Article  Google Scholar 

  37. Miller MA et al. (2009) The CIPRES Portals. CIPRES. URL:http://www.phylo.org/sub_sections/portal

  38. Molino JF, Sabatier D (2001) Tree diversity in tropical rain forests: a validation of the intermediate disturbance hypothesis. Science 294:1702–1704

    Article  PubMed  CAS  Google Scholar 

  39. Ofiteru ID et al (2010) Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci U S A 107:15345–15350

    Article  PubMed  CAS  Google Scholar 

  40. Paine RT, Levin SA (1981) Inter-tidal landscapes—disturbance and the dynamics of pattern. Ecol Monogr 51:145–178

    Article  Google Scholar 

  41. Peter H, Beier S, Bertilsson S, Lindstrom ES, Langenheder S, Tranvik LJ (2011) Function-specific response to depletion of microbial diversity. ISME J 5:351–361

    Article  PubMed  CAS  Google Scholar 

  42. Rousk J, Baath E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30

    Article  PubMed  CAS  Google Scholar 

  43. Schloss PD, Gevers D, Westcott SL (2011) Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies. PLoS One 6:e27310

    Article  PubMed  CAS  Google Scholar 

  44. Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed  CAS  Google Scholar 

  45. Shade A, Read JS, Welkie DG, Kratz TK, Wu CH, McMahon KD (2011) Resistance, resilience and recovery: aquatic bacterial dynamics after water column disturbance. Environ Microbiol 13:2752–2767

    Article  PubMed  CAS  Google Scholar 

  46. Shrestha PM, Noll M, Liesack W (2007) Phylogenetic identity, growth-response time and rRNA operon copy number of soil bacteria indicate different stages of community succession. Environ Microbiol 9:2464–2474

    Article  PubMed  CAS  Google Scholar 

  47. Smalla K et al (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  PubMed  CAS  Google Scholar 

  48. Sousa WP (1984) The role of disturbance in natural communities. Annu Rev Ecol Syst 15:353–391

    Article  Google Scholar 

  49. Stackebrandt E, Goebel BM (1994) A Place for DNA-DNA Reassociation and 16s Ribosomal-Rna Sequence-analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  50. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  51. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton

    Google Scholar 

  52. Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Article  Google Scholar 

  53. Trosvik P, Stenseth NC, Rudi K (2010) Convergent temporal dynamics of the human infant gut microbiota. ISME J 4:151–158

    Article  PubMed  CAS  Google Scholar 

  54. Vieira-Silva S, Rocha EP (2010) The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet 6:e1000808

    Article  PubMed  Google Scholar 

  55. Violle C, Pu Z, Jiang L (2010) Experimental demonstration of the importance of competition under disturbance. Proc Natl Acad Sci U S A 107:12925–12929

    Article  PubMed  CAS  Google Scholar 

  56. Wertz S et al (2007) Early-stage bacterial colonization between a sterilized remoulded soil clod and natural soil aggregates of the same soil. Soil Biol Biochem 39:3127–3137

    Article  CAS  Google Scholar 

  57. Wertz S et al (2006) Maintenance of soil functioning following erosion of microbial diversity. Environ Microbiol 8:2162–2169

    Article  PubMed  CAS  Google Scholar 

  58. Wertz S et al (2007) Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ Microbiol 9:2211–2219

    Article  PubMed  Google Scholar 

  59. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (NRF-2011-0015787). We thank Y-M. Oh, K-H. Lee, and W-S. Kim of SNU for their help with experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan Adams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 174 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, M., Heo, E., Kang, H. et al. Changes in Soil Bacterial Community Structure with Increasing Disturbance Frequency. Microb Ecol 66, 171–181 (2013). https://doi.org/10.1007/s00248-013-0237-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0237-9

Keywords

Navigation