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Comparative Resistance and Resilience of Soil Microbial Communities and Enzyme Activities in Adjacent Native Forest and Agricultural Soils

  • Soil Microbiology
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Abstract

Degradation of soil properties following deforestation and long-term soil cultivation may lead to decreases in soil microbial diversity and functional stability. In this study, we investigated the differences in the stability (resistance and resilience) of microbial community composition and enzyme activities in adjacent soils under either native tropical forest (FST) or in agricultural cropping use for 14 years (AGR). Mineral soil samples (0 to 5 cm) from both areas were incubated at 40°C, 50°C, 60°C, or 70°C for 15 min in order to successively reduce the microbial biomass. Three and 30 days after the heat shocks, fluorescein diacetate (FDA) hydrolysis, cellulase and laccase activities, and phospholipid-derived fatty acids-based microbial community composition were measured. Microbial biomass was reduced up to 25% in both soils 3 days after the heat shocks. The higher initial values of microbial biomass, enzyme activity, total and particulate soil organic carbon, and aggregate stability in the FST soil coincided with higher enzymatic stability after heat shocks. FDA hydrolysis activity was less affected (more resistance) and cellulase and laccase activities recovered more rapidly (more resilience) in the FST soil relative to the AGR counterpart. In the AGR soil, laccase activity did not show resilience to any heat shock level up to 30 days after the disturbance. Within each soil type, the microbial community composition did not differ between heat shock and control samples at day 3. However, at day 30, FST soil samples treated at 60°C and 70°C contained a microbial community significantly different from the control and with lower biomass regardless of high enzyme resilience. Results of this study show that deforestation followed by long-term cultivation changed microbial community composition and had differential effects on microbial functional stability. Both soils displayed similar resilience to FDA hydrolysis, a composite measure of a broad range of hydrolases, supporting the concept of high functional redundancy in soil microbial communities. In contrast, the resilience of the substrate-specific activities of laccase and cellulase were lower in AGR soils, indicating a less diverse community of microorganisms capable of producing these enzymes and confirming that specific microbial functions are more sensitive measurements for evaluating change in the ecological stability of soils.

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References

  1. Ahn M, Zimmerman AR, Martínez CE, Archibald DD, Bollag J, Dec J (2007) Characteristics of Trametes villosa laccase adsorbed on aluminum hydroxide. Enzyme Microb Technol 41:141–148

    Article  CAS  Google Scholar 

  2. 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 

  3. Bossio DA, Girvan MS, Verchot L, Bullimore J, Borelli T, Albrecht A, Scow KM, Ball AS, Pretty JN, Osborn AM (2005) Soil microbial community response to land use change in an agricultural landscape of Western Kenya. Microb Ecol 49:50–62

    Article  PubMed  CAS  Google Scholar 

  4. Bouyoucos GJ (1927) The hydrometer as a new and rapid method for determining the colloidal content of soils. Soil Sci 23:319–331

    Article  CAS  Google Scholar 

  5. Braga JM, Defelipo BV (1974) Determinação espectrofotométrica de fósforo em extrato de solo e material vegetal. Rev Ceres 21:73–85

    CAS  Google Scholar 

  6. Bray JR, Curtis JT (1957) An ordination of the upland forest communities in southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  7. Breiman L, Friedman JH, Olshen RA, Stone CG (1984) Classification and regression trees. Chapman & Hall/CRC, Belmont, CA, USA

    Google Scholar 

  8. Buckley DH, Schmidt TM (2001) The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 42:11–21

    PubMed  CAS  Google Scholar 

  9. Butler JL, Williams MA, Bottomley PJ, Myrold DD (2003) Microbial community dynamics associated with rhizosphere carbon flow. Appl Environ Microbiol 69:6793–6800

    Article  PubMed  CAS  Google Scholar 

  10. Cambardella CA, Elliot ET (1992) Particulate soil organic matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783

    Google Scholar 

  11. De’ath G (2002) Multivariate regression trees: a new technique for modeling species–environmental relationships. Ecology 83:1105–1117

    Google Scholar 

  12. De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for the analysis of complex ecological data. Ecology 81:3178–3192

    Google Scholar 

  13. Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33:1143–1153

    Article  CAS  Google Scholar 

  14. Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196

    Article  CAS  Google Scholar 

  15. Dick RP, Breakwell DP, Turco RF (1996) Soil enzyme activity and biodiversity measurements as integrative microbiological indicators. In: Doran, JW, Jones, AJ (eds.) Methods for assessing soil quality, vol. SSSA Special Publication 49. SSSA, Madison, pp. 247-271

  16. Dinesh R, Chaudhuri SG, Sheeja TE (2004) Soil biochemical and microbial indices in wet tropical forests: effects of deforestation and cultivation. J Plant Nutr Soil Sci 167:24–32

    Article  CAS  Google Scholar 

  17. Ehrlich PR, Ehrlich AH (1981) Extinction: the causes and consequences of the disappearance of species. Random House, New York

    Google Scholar 

  18. Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  19. Girvan MS, Campbell CD, Killham K, Prosser JI, Glover LA (2005) Bacterial diversity promotes community stability and functional resilience after perturbation. Environ Microbiol 7:301–313

    Article  PubMed  CAS  Google Scholar 

  20. Green VS, Stott DE, Diack M (2006) Assay for fluorescein diacetate hydrolytic activity: optimization for soil samples. Soil Biol Biochem 38:693–701

    Article  CAS  Google Scholar 

  21. Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb Ecol 47:104–113

    Article  PubMed  CAS  Google Scholar 

  22. Griffiths BS, Ritz K, Bardgett RD, Cook R, Christensen S, Ekelund F, Sørensen SJ, Bååth E, Bloem J, de Ruiter PC, Dolfing J, Nicolardot B (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 

  23. Griffiths BS, Ritz K, Wheatley RE, Kuan HL, Boag B, Christensen S (2001) An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities. Soil Biol Biochem 33:1713–1722

    Article  CAS  Google Scholar 

  24. Guilbault GG, Kramer DN (1964) Fluorometric determination of lipase, acylase, alpha- and gamma-chymotrypsin and inhibitors of these enzymes. Anal Chem 36:409–412

    Article  CAS  Google Scholar 

  25. Hope CFA, Burns RG (1987) Activity, origins and location of cellulases in a silt loam soil. Biol Fertil Soils 5:164–170

    Article  CAS  Google Scholar 

  26. Huang Q, Liang W, Cai P (2005) Adsorption, desorption and activities of acid phosphatase on various colloidal particles from an Ultisol. Colloids Surf B 45:209–214

    Article  CAS  Google Scholar 

  27. Islam KR, Weil RR (2000) Land use effects on soil quality in a tropical forest ecosystem of Bangladesh. Agric Ecosyst Environ 79:9–16

    Article  Google Scholar 

  28. Kandeler E (1990) Characterization of free and adsorbed phosphatases in soils. Biol Fertil Soils 9:199–202

    Article  CAS  Google Scholar 

  29. Kemper WD, Rosenau RC (1986) Aggregate stability and size distribution. In: Klute A (ed) Methods of soil analysis Part 1. ASA/SSSA, Madison, WI, pp 425–441

    Google Scholar 

  30. Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129

    Article  Google Scholar 

  31. Lang E, Eller G, Zadrazil F (1997) Lignocellulose decomposition and production of ligninolytic enzymes during interaction of white rot fungi with soil microorganisms. Microb Ecol 34:1–10

    Article  PubMed  CAS  Google Scholar 

  32. Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91:3–17

    Article  Google Scholar 

  33. MacArthur RH (1955) Fluctuations of animal populations and a measure of community stability. Ecology 73:1943–1967

    Google Scholar 

  34. Mather PM (1976) Computational methods of multivariate analysis in physical geography. J. Wiley & Sons, London

    Google Scholar 

  35. Mendes IC, Bottomley PJ, Dick RP, Bandick AK (1999) Microbial biomass and activities in soil aggregates affected by winter cover crops. Soil Sci Soc Am J 63:873–881

    CAS  Google Scholar 

  36. Naeem S, Li S (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509

    Article  CAS  Google Scholar 

  37. Niku-Paavola ML, Raaska L, Itavaara M (1990) Detection of white-rot fungi by a non-toxic stain. Mycol Res 94:27–31

    Article  Google Scholar 

  38. Nimmo JR, Perkins KS (2002) Aggregate stability and size distribution. In: Dane JH, Topp GC (eds) Methods of soil analysis Part 4 Physical methods. SSSA, Madison, WI, pp 317–328

    Google Scholar 

  39. Nizovtseva DV, Semenov AM (1995) Influence of moisture on cellulase activity of micro-organisms in upper peat. Microbiology (Read) 64:841–846

    Google Scholar 

  40. Nourbakhsh F (2007) Decoupling of soil biological properties by deforestation. Agric Ecosyst Environ 121:435–438

    Article  Google Scholar 

  41. Nusslein K, Tiedje JM (1999) Soil bacterial community shift correlated with change from forest to pasture vegetation in a tropical soil. Appl Environ Microbiol 65:3622–3626

    PubMed  CAS  Google Scholar 

  42. Olsson PA, Bååth E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629

    Article  CAS  Google Scholar 

  43. Schinner F, von Mersi W (1990) Xylanase-, CM-cellulase-, and invertase activity in soil: an improved method. Soil Biol Biochem 22:511–515

    Article  CAS  Google Scholar 

  44. Schnürer J, Rosswall T (1982) Fluorescein diacetate hydrolysis as a measurement of total microbial activity in soil and litter. Appl Environ Microbiol 43:1256–1261

    PubMed  Google Scholar 

  45. Semenov AM, Nizovtseva DV (1995) Influence of temperature and mineral supply on cellulase activity and micromycete development in samples of peat from the upper bog. Microbiology 64:97–103

    CAS  Google Scholar 

  46. Solomon D, Lehmann J, Zech W, Fritzsche F, Tekalign M (2002) Soil organic matter composition in the subhumid Ethiopian highlands as influenced by deforestation and agricultural management. Soil Sci Soc Am J 66:68–82

    Article  CAS  Google Scholar 

  47. Solomon D, Tekalign M, Zech W, Fritzsche F, Lehmann J (2002) Soil organic matter dynamics in the subhumid agroecosystems of the Ethiopian highlands: evidence from natural 13C abundance and particle-size fractionation. Soil Sci Soc Am J 66:969–978

    CAS  Google Scholar 

  48. van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24

    Article  Google Scholar 

  49. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Article  CAS  Google Scholar 

  50. White DC, Pinkart HC, Ringelberg DB (1997) Biomass measurements: biochemical approaches. In: Hurst CJ, Knudsen GR (eds) Manual of Environmental Microbiology. ASM Press, Washington, DC, pp 91–101

    Google Scholar 

  51. Wright DA, Killham K, Glover LA, Prosser JI (1995) Role of pore size location in determining bacterial activity during predation by protozoa in soil. Appl Environ Microbiol 61:3537–3543

    PubMed  CAS  Google Scholar 

  52. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The first author acknowledges the fellowship support from the Brazilian Federal Agency for Graduate Education (CAPES).

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Authors and Affiliations

  1. Embrapa Agrobiologia, Seropédica, RJ, Brazil

    Guilherme Chaer

  2. Embrapa Tabuleiros Costeiros, Aracaju, SE, Brazil

    Marcelo Fernandes

  3. Crop and Soil Science, Oregon State University, Corvallis, OR, USA

    David Myrold

  4. Microbiology, Oregon State University, Corvallis, OR, USA

    Peter Bottomley

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  1. Guilherme Chaer
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  2. Marcelo Fernandes
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  4. Peter Bottomley
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Correspondence to Guilherme Chaer.

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Chaer, G., Fernandes, M., Myrold, D. et al. Comparative Resistance and Resilience of Soil Microbial Communities and Enzyme Activities in Adjacent Native Forest and Agricultural Soils. Microb Ecol 58, 414–424 (2009). https://doi.org/10.1007/s00248-009-9508-x

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  • DOI: https://doi.org/10.1007/s00248-009-9508-x

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