Skip to main content
SpringerLink
Log in

Vegetation Affects the Relative Abundances of Dominant Soil Bacterial Taxa and Soil Respiration Rates in an Upland Grassland Soil

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Plant-derived organic matter inputs are thought to be a key driver of soil bacterial community composition and associated soil processes. We sought to investigate the role of acid grassland vegetation on soil bacterial community structure by assessing bacterial diversity in combination with other soil variables in temporally and spatially distinct samples taken from a field-based plant removal experiment. Removal of aboveground vegetation resulted in reproducible differences in soil properties, soil respiration and bacterial diversity. Vegetated soils had significantly increased carbon and nitrogen concentrations and exhibited higher rates of respiration. Molecular analyses revealed that the soils were broadly dominated by Alphaproteobacterial and Acidobacterial lineages, with increased abundances of Alphaproteobacteria in vegetated soils and more Acidobacteria in bare soils. This field-based study contributes to a growing body of evidence documenting the effect of soil nutrient status on the relative abundances of dominant soil bacterial taxa, with Proteobacterial taxa dominating over Acidobacteria in soils exhibiting higher rates of C turnover. Furthermore, we highlight the role of aboveground vegetation in mediating this effect by demonstrating that plant removal can alter the relative abundances of dominant soil taxa with concomitant changes in soil CO2-C efflux.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Anderson JPE, Domsch KH (1973) Quantification of bacterial and fungal contributions to soil respiration. Arch Mikrobiol 93:113–127

    Article  CAS  Google Scholar 

  2. Axelrood PE, Chow ML, Radomski CC, McDermott JM, Davies J (2002) Molecular characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48:655–674

    Article  CAS  PubMed  Google Scholar 

  3. Bardgett RD (2005) Chapter 3: organism interactions and soil processes. In: Bardgett RD (ed) The biology of soil: a community and ecosystem approach. Oxford University Press, Oxford, pp 57–85

    Google Scholar 

  4. Baudoin E, Benizri E, Guckert A (2002) Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. App Soil Ecol 19:135–145

    Article  Google Scholar 

  5. Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  6. de Ridder-Duine AS, Kowalchuk GA, Klein Gunnewiek PJA, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357

    Article  Google Scholar 

  7. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  PubMed  Google Scholar 

  8. Dreyfus BL, Dommergues YR (1981) Nodulation of acacia species by fast-growing and slow-growing tropical strains of rhizobium. Appl Environ Microbiol 41:97–99

    PubMed  Google Scholar 

  9. Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen JA (2001) Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178

    Article  CAS  PubMed  Google Scholar 

  10. Fenner N, Ostle NJ, McNamara N, Sparks T, Harmens H, Reynolds B, Freeman C (2007) Elevated CO2 effects on peatland plant community carbon dynamics and DOC production. Ecosystems 10:635–647

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  12. Floyd MM, Tang J, Kane M, Emerson D (2005) Captured diversity in a culture collection: case study of the geographic and habitat distributions of environmental isolates held at the American Type Culture Collection. Appl Environ Microbiol 71:2813–2823

    Article  CAS  PubMed  Google Scholar 

  13. Griffiths RI, Bailey MJ, McNamara NP, Whiteley AS (2006) The functions and components of the Sourhope soil microbiota. App Soil Ecol 33:114–126

    Article  Google Scholar 

  14. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2003) Influence of depth and sampling time on bacterial community structure in an upland grassland soil. FEMS Microbiol Ecol 43:35–43

    Article  CAS  PubMed  Google Scholar 

  15. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491

    Article  CAS  PubMed  Google Scholar 

  16. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acid Sym Ser 41:95–98

    CAS  Google Scholar 

  17. Helal HM, Sauerbeck DR (1984) Influence of plant-roots on C and P metabolism in soil. Plant Soil 76:175–182

    Article  CAS  Google Scholar 

  18. Hooper DU, Bignell DE, Brown VK, Brussaard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, Van der Putten WH, De Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50:1049–1061

    Article  Google Scholar 

  19. Hopkins DW, Gregorich EG (2005) Chapter four: carbon as a substrate for soil organisms. In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 57–82

    Chapter  Google Scholar 

  20. 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  CAS  PubMed  Google Scholar 

  21. Johnson D, Booth RE, Whiteley AS, Bailey MJ, Read DJ, Grime JP, Leake JR (2003) Plant community composition affects the biomass, activity and diversity of microorganisms in limestone grassland soil. Eur J Soil Sci 54:671–677

    Article  Google Scholar 

  22. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Ant Van Leeu Int J Gen and Mol Microbiol 81:509–520

    Article  Google Scholar 

  23. Kuzyakov Y (2002) Separating microbial respiration of exudates from root respiration in non-sterile soils: a comparison of four methods. Soil Biol Biochem 34:1621–1631

    Article  CAS  Google Scholar 

  24. Lane DJ (1991) Chapter 6. 16S/23S rRNA sequencing. In: Stackenbrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  25. Ledgard SF, Steele KW (1992) Biological nitrogen fixation in mixed legume grass pastures. Plant Soil 141:137–153

    Article  CAS  Google Scholar 

  26. Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522

    CAS  PubMed  Google Scholar 

  27. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  PubMed  Google Scholar 

  28. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Dymock D, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:2333–2333

    CAS  PubMed  Google Scholar 

  29. Marilley L, Vogt G, Blanc M, Aragno M (1998) Bacterial diversity in the bulk soil and rhizosphere fractions of Lolium perenne and Trifolium repens as revealed by PCR restriction analysis of 16S rDNA. Plant Soil 198:219–224

    Article  CAS  Google Scholar 

  30. Raich JW, Tufekcioglu A (2000) Vegetation and soil respiration: correlations and controls. Biogeochemistry 48:71–90

    Article  CAS  Google Scholar 

  31. Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7:828–838

    Article  CAS  PubMed  Google Scholar 

  32. Rodwell JS (1992) In: Rodwell JS (ed) British plant communities, vol 3. Cambridge University Press, Cambridge

    Google Scholar 

  33. Sait M, Davis KER, Janssen PH (2006) Effect of pH on isolation and distribution of members of subdivision 1 of the phylum Acidobacteria occurring in soil. Appl Environ Microbiol 72:1852–1857

    Article  CAS  PubMed  Google Scholar 

  34. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (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  CAS  PubMed  Google Scholar 

  35. Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291

    Article  CAS  PubMed  Google Scholar 

  36. Steer J, Harris JA (2000) Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32:869–878

    Article  CAS  Google Scholar 

  37. Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA (2004) New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70:4748–4755

    Article  CAS  PubMed  Google Scholar 

  38. Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537

    Article  CAS  Google Scholar 

  39. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  Google Scholar 

  40. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  41. Wood M, Cooper JE, Bjourson AJ (1988) Response of lotus rhizobia to acidity and aluminum in liquid culture and in soil. Plant Soil 107:227–231

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Tony O’Donnell at the University of Western Australia for comment on an earlier draft of this manuscript. In addition, we extend our gratitude to Darren Sleep at the NERC/CEH stable isotope facility for carrying out soil C and N analyses.

Author information

Authors and Affiliations

  1. Centre for Ecology & Hydrology, Mansfield Road, Oxford, OX1 3SR, UK

    Bruce C. Thomson, Mark J. Bailey, Andrew S. Whiteley & Robert I. Griffiths

  2. Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, UK

    Nick Ostle & Niall McNamara

Authors
  1. Bruce C. Thomson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nick Ostle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Niall McNamara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark J. Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew S. Whiteley
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert I. Griffiths
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert I. Griffiths.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thomson, B.C., Ostle, N., McNamara, N. et al. Vegetation Affects the Relative Abundances of Dominant Soil Bacterial Taxa and Soil Respiration Rates in an Upland Grassland Soil. Microb Ecol 59, 335–343 (2010). https://doi.org/10.1007/s00248-009-9575-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-009-9575-z

Keywords

Search

Navigation