Microbial Ecology

, Volume 47, Issue 1, pp 104–113

The Relationship between Microbial Community Structure and Functional Stability, Tested Experimentally in an Upland Pasture Soil

  • B. S. Griffiths
  • H. L. Kuan
  • K. Ritz
  • L. A. Glover
  • A. E. McCaig
  • C. Fenwick


Soil collected from an upland pasture was manipulated experimentally in ways shown previously to alter microbial community structure. One set of soil was subjected to chloroform fumigation for 0, 0.5, 2, or 24 h and the other was sterilised by gamma-irradiation and inoculated with a 10−2, 10−4, 10−6, or 10−8 dilution of a soil suspension prepared from unsterilized soil. Following incubation for 8 months, to allow for the stabilization of microbial biomass and activity, the resulting microbial community structure (determined by PCR-DGGE of bacterial specific amplification products of total soil DNA) was assessed. In addition, the functional stability (defined here as the resistance and resilience of short-term decomposition of plant residues to a transient heat or a persistent copper perturbation) was determined. Changes in the active bacterial population following perturbation (determined by RT-PCR-DGGE of total soil RNA) were also monitored. The manipulations resulted in distinct shifts in microbial community structure as shown by PCR-DGGE profiles, but no significant decreases in the number of bands. These shifts in microbial community structure were associated with a reduction in functional stability. The clear correlation between altered microbial community structure and functional stability observed in this upland pasture soil was not evident when the same protocols were applied to soils in other studies. RT-PCR-DGGE profiles only detected a shift in the active bacterial population following heat, but not copper, perturbation. We conclude that the functional stability of decomposition is related to specific components of the microbial community.


  1. 1.
    Andrén, O, Balandreau, J 1999Biodiversity and soil functioning—from black box to can of worms?Appl Soil Ecol13105108CrossRefGoogle Scholar
  2. 2.
    Andrén, O, Bengtsson, J, Clarholm, M 1995

    Biodiversity and species redundancy among litter decomposers.

    Collins, HPRobertson, GPKlug, MJ eds. The Significance and Regulation of Soil Biodiversity.Kluwer AcademicAmsterdam141151
    Google Scholar
  3. 3.
    Andrén, O, Brussaard, L, Clarholm, M 1999Soil organism influence on ecosystem-level processes—bypassing the ecological hierarchy.Appl Soil Ecol11177188CrossRefGoogle Scholar
  4. 4.
    Bardgett, RD, Shine, A 1999Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands.Soil Biol Biochem31317321CrossRefGoogle Scholar
  5. 5.
    Bengtsson J (1997) What kind of diversity? Species richness, keystone species or functional groups? In: Wolters V (ed) Functional Implications of Biodiversity in Soil. Ecosystems research report no. 24, Office for Official Publications of the European Communities, Luxembourg, pp 59–66Google Scholar
  6. 6.
    Cragg, RG, Bardgett, RD 2001How changes in soil faunal diversity and composition within a trophic group influence decomposition processes.Soil Biol Biochem3320732081CrossRefGoogle Scholar
  7. 7.
    de Boer, W, Verheggen, P, Klein Gunneweick, PJA, Kowalchuk, GA, van Veen, JA 2003Microbial community composition affects soil fungistasis.Appl Environ Microbiol69835844CrossRefPubMedGoogle Scholar
  8. 8.
    Degens, BP 1998Decreases in microbial functional diversity do not result in corresponding changes in decomposition under different moisture conditions.Soil Biol Biochem3019892000CrossRefGoogle Scholar
  9. 9.
    Degens, BP, Schipper, LA, Sparling, GP, Duncan, LC 2001Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance?Soil Biol Biochem3311431153CrossRefGoogle Scholar
  10. 10.
    Dickens, HE, Anderson, JM 1999Manipulation of soil microbial community structure in bog and forest soils using chloroform fumigation.Soil Biol Biochem3120492058Google Scholar
  11. 11.
    Duffy, JE, MacDonald, KS, Rhode, JM, Parker, JD 2001Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test.Ecology8224172434Google Scholar
  12. 12.
    Ekschmitt, K, Klein, A, Pieper, B, Wolters, V 2001Biodiversity and functioning of ecological communities—why is diversity important in some cases and unimportant in others?J Plant Nutrit Soil Sci164239246CrossRefGoogle Scholar
  13. 13.
    Ettema, CH 1998Soil nematode diversity: species coexistence and ecosystem function.J Nematol30159169Google Scholar
  14. 14.
    Farrelly, V, Rainey, FA, Stackebrandt, E 1995Effects of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species.Appl Environ Microbiol6127982801PubMedGoogle Scholar
  15. 15.
    Finlay, BJ, Maberly, SC, Cooper, JI 1997Microbial diversity and ecosystem function.Oikos80209213Google Scholar
  16. 16.
    Finlay, BJ, Esteban, GF 1998Freshwater protozoa: biodiversity and ecological function.Biodivers Conserv711631186CrossRefGoogle Scholar
  17. 17.
    Finlay, BJ, Black, HIJ, Brown, S, Clarke, KJ, Esteban, GF, Hindle, RM, Olmo, JL, Rollett, A, Vickerman, K 2000Estimating the growth potential of the soil protozoan community.Protist1516980Google Scholar
  18. 18.
    Giller, K, Witter, E, McGrath, SP 1998Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review.Soil Biol Biochem3013891414Google Scholar
  19. 19.
    Griffiths, BS, Ritz, K, Wheatley, RE 1997

    Relationships between functional diversity and genetic diversity in complex microbial communities.

    Insam, HRangger, A eds. Microbial Communities: Functional versus Structural Approaches.Springer-VerlagBerlin19
    Google Scholar
  20. 20.
    Griffiths, BS, Díaz-Ravina, M, Ritz, K, McNicol, JW, Ebblewhite, N, Bååth, E 1997Community DNA hybridisation and %G+C profiles of microbial communities from heavy metal polluted soils.FEMS Microbiol Ecol24103112CrossRefPubMedGoogle Scholar
  21. 21.
    Griffiths, BS, Ritz, K, Bardgett, RD, Cook, R, Christensen, S, Ekelund, F, Sørensen, S, Bååth, E, Bloem, J, de Ruiter, PC, Dolfing, J 2000Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship.Oikos90279294Google Scholar
  22. 22.
    Griffiths, BS, Ritz, K, Wheatley, RE, Kuan, HL, Boag, B, Christensen, S, Ekelund, F, Sørensen, S, Muller, S, Bloem, J 2001An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities.Soil Biol Biochem3317131722CrossRefGoogle Scholar
  23. 23.
    Griffiths, BS, Bonkowski, M, Roy, J, Ritz, K 2001Functional stability, substrate utilisation and biological indicators of soils following environmental impacts.Appl Soil Ecol164961CrossRefGoogle Scholar
  24. 24.
    Griffiths, RI, Whiteley, AS, O’Donnell, AG, Bailey, M 2000A rapid method for the co-extraction of DNA and RNA from natural environments for the analysis of rDNA and rRNA based microbial community composition.Appl Environ Microbiol6654885491Google Scholar
  25. 25.
    Grime, JP 1997Biodiversity and ecosystem function: the debate deepens.Science27712601261CrossRefGoogle Scholar
  26. 26.
    Hooper, DU, Vitousek, PM 1997The effects of plant composition and diversity on ecosystem processes.Science27713021305Google Scholar
  27. 27.
    Loreau, M 2000Biodiversity and ecosystem functioning; recent theoretical advances.Oikos91317Google Scholar
  28. 28.
    Martens, R 1995Current methods for measuring microbial biomass in soil: potentials and limitations.Biol Fertil Soils198799Google Scholar
  29. 29.
    McCaig, AE, Glover, LA, Prosser, JI 1999Molecular analysis of eubacterial community structure and diversity in unimproved and improved upland grass pastures.Appl Environ Microbiol6517211730PubMedGoogle Scholar
  30. 30.
    McCaig, AE, Glover, LA, Prosser, JI 2001Numerical analysis of grassland bacterial community structure under different land management regimes using 16S rDNA sequence data and denaturing gradient gel electrophoresis banding patterns.Appl Environ Microbiol6745544559Google Scholar
  31. 31.
    McNaughton, SJ 1988Diversity and stability.Nature333204205CrossRefGoogle Scholar
  32. 32.
    McNaughton, SJ 1994

    Biodiversity and function in grazing ecosystems.

    Schulze, E-DMooney, HA eds. Biodiversity and ecosystem function.Springer-VerlagBerlin361383
    Google Scholar
  33. 33.
    Metcalfe, AC, Krsek, M, Gooday, GW, Prosser, JI, Wellington, EMH 2002Molecular analysis of a bacterial chitinolytic community in an upland pasture.Appl Environ Microbiol6850425050CrossRefPubMedGoogle Scholar
  34. 34.
    Mikola, J, Setälä, H 1998Relating species diversity to ecosystem function: mechanistic backgrounds and experimental approach with a decomposer food web.Oikos83180194Google Scholar
  35. 35.
    Muir, JW 1956The Soils round Jedburgh and Morebattle.Her Majesty’s Stationery OfficeEdinburghGoogle Scholar
  36. 36.
    Müller, AK, Westergaard, K, Christensen, S, Sørensen, SJ 2002The diversity and function of soil microbial communities exposed to different disturbances.Microb Ecol444958CrossRefPubMedGoogle Scholar
  37. 37.
    Muyzer, G, de Wall, EC, Uitterlinden, AG 1993Profiling of complex microbial populations by denaturant gradient gel electrophoresis analysis of polymerase chain reaction–amplified genes coding for 16S rRNA.Appl Environ Microbiol59695700PubMedGoogle Scholar
  38. 38.
    Nübel, U, Engelen, B, Felske, A, Snaidr, J, Weishuber, A, Amann, RI, Ludwig, W, Backhaus, H 1996Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis.J Bacteriol17856365643PubMedGoogle Scholar
  39. 39.
    Powlson, DS, Jenkinson, DS 1976The effects of biocidal treatments on metabolism in soil—II. Gamma irradiation, autoclaving, air-drying and fumigation.Soil Biol Biochem8179188Google Scholar
  40. 40.
    Ritz, K, Griffiths, BS, Wheatley, RE 1992Soil microbial biomass and activity under a potato crop fertilised with N with and without C.Biol Fertil Soils12265271Google Scholar
  41. 41.
    Ritz, K, Wheatley, RE, Griffiths, BS 1997Effects of animal manure application and crop plants upon size and activity of soil microbial biomass under organically grown spring barley.Biol Fertil Soils24372377Google Scholar
  42. 42.
    Salonius, PO 1981Metabolic capabilities of forest soil microbial populations with reduced species diversity.Soil Biol Biochem13110CrossRefGoogle Scholar
  43. 43.
    Symstad, AJ, Tilman, D, Willson, J, Knops, JMH 1998Species loss and ecosystem functioning: effects of species identity and community composition.Oikos81389397Google Scholar
  44. 44.
    van Beelan, P, Fleuren-Kemilä, AK, Huys, MPA, van Montfort, ACP, van Vlaardingen, PLA 1991The toxic effects of pollutants on the mineralization of acetate in subsoil microcosms.Environ Toxicol Chem10775789Google Scholar
  45. 45.
    van der Heijden, MGA, Klironomos, JN, Ursic, M, Moutoglis, P, Streitwolf-Engel, R, Boller, T, Wiemken, A, Sanders, IR 1998Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity.Nature3966972CrossRefGoogle Scholar
  46. 46.
    von Wintzingerode, F, Göbel, UB, Stackebrandt, E 1997Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis.FEMS Microbiol Rev21213229PubMedGoogle Scholar
  47. 47.
    Wardle, DA, Zackrisson, O, Hörnberg, G, Gallzet, C 1997The influence of island area on ecosystem properties.Science27712961299Google Scholar
  48. 48.
    Wardle, DA, Bonner, KL, Barker, GM, Yeates, GW, Nicholson, KS, Bardgett, RD, Watson, RN, Ghiani, A 1999Experimental reductions in plant functional diversity in a perennial grassland: implications for vegetation dynamics, decomposer food-webs, soil biodiversity and ecosystem function.Ecol Monogr69535568Google Scholar
  49. 49.
    Westergaard, K, Muller, AK, Christensen, S, Bloem, J, Sørensen, SJ 2001Effects of tylosin as a disturbance on the soil microbial community.Soil Biol Biochem3320612071CrossRefGoogle Scholar
  50. 50.
    Wheatley, RE, MacDonald, R, Smith, AM 1989Extraction of nitrogen from soils.Biol Fertil Soils8189190Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • B. S. Griffiths
    • 1
  • H. L. Kuan
    • 1
  • K. Ritz
    • 2
  • L. A. Glover
    • 3
  • A. E. McCaig
    • 3
    • 4
  • C. Fenwick
    • 3
    • 5
  1. 1.Plant–Soil Interface ProgrammeScottish Crop Research Institute, Invergowrie, Dundee DD2 5DAUK
  2. 2.National Soil Resources InstituteCranfield University, Silsoe, Bedfordshire MK45 4DTUK
  3. 3.Department of Molecular and Cell Biology, Institute of Medical SciencesUniversity of Aberdeen, Aberdeen AB25 2ZDUK
  4. 4.The Engineering and Physical Sciences Research Council, Polaris House, North Star Avenue, Swindon SN2 1ETUK
  5. 5.The Natural Environment Research Council, Polaris House, North Star Avenue, Swindon SN2 1EUUK

Personalised recommendations