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Influence of heavy metals on the functional diversity of soil microbial communities

Abstract

Three soil types-Calcaric Phaeozem, Eutric Cambisol and Dystric Lithosol-in large container pots were experimentally contaminated with heavy metals at four different levels (light pollution: 300 ppm Zn, 100 ppm Cu, 50 ppm Ni, 50 ppm V and 3 ppm Cd; medium pollution: twofold concentrations; heavy pollution: threefold concentrations; uncontaminated control). We investigated the prognostic potential of 16 soil microbial properties (microbial biomass, respiration, N-mineralization, 13 soil enzymes involved in cycling of C, N, P and S) with regard to their ability to differentiate the four contamination levels. Microbial biomass and enzyme activities decreased with increasing heavy metal pollution, but the amount of decrease differed among the enzymes. Enzymes involved in the C-cycling were least affected, whereas vartous enzyme activities related to the cycling of N, P and S showed a considerable decrease in activity. In particular, arylsulfatase and phosphatase activities were dramatically affected. Their activity decreased to a level of a few percent of their activities in the corresponding unpolluted controls. The data suggest that aside from the loss of rare biochemical capabilities-such as the growth of organisms at the expense of aromatics (Reber 1992)-heavy metal contaminated soils lose very common biochemical propertities which are necessary for the functioning of the ecosystem. Cluster analysis as well as discriminant analysis underline the similarity of the enzyme activity pattern among the controls and among the polluted soils. The trend toward a significant functional diversity loss becomes obvious already at the lowest pollution level. This implies that concentrations of heavy metals in soils near the current EC limits will most probably lead to a considerable reduction in decomposition and nutrient cycling rates. We conclude that heavy metal pollution severely decreases the functional diversity of the soil microbial community and impairs specific pathways of nutrient cycling.

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References

  1. Alexander M (1977) Introduction to soil microbiology. John Wiley & Sons, New York

    Google Scholar 

  2. Alloway BJ (1990) Soil processes and the behaviour of metals. In: Alloway BJ (ed) Heavy metals in soils. Blackie and Son, Glasgow; John Wiley & Sons, New York, pp 7–27

    Google Scholar 

  3. Anderson J, Domsch K (1978) A physiological method for quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221

    Google Scholar 

  4. Bääth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 47:335–379

    Google Scholar 

  5. Babich H, Stotzky G (1980) Environmental factors that influence the toxicity of heavy metals and gaseous pollutants to microorganisms. CRC Crit Rev Microbiol 8:99–145

    Google Scholar 

  6. Bardgett RD, Saggar S (1994) Effects of heavy metal contamination on the short-term decomposition of labelled 14C glucose in a pasture. Soil Biol Biochem 26:727–733

    Google Scholar 

  7. Barkay T, Tripp SC, Olsen BH (1985) Effect of metal-rich sewage sludge application on the bacterial communities of grassland. Appl Environ Microbiol 49:333–337

    Google Scholar 

  8. Berg P, Rosswall T (1985) Ammonium oxidizer numbers, potential and actual oxidation rates in two Swedish arable soils. Biol Fertil Soils 1:131–140

    Google Scholar 

  9. Brookes PC (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279

    Google Scholar 

  10. Brookes PC, McGrath SP (1984) Effects of metal toxicity on the size of the soil microbial biomass. J Soil Sci 35:341–346

    Google Scholar 

  11. Brunner I, Schinner F (1984) Einltuß von Blei und Cadmium auf die mikrobielle Aktivität eines Bodens. Die Bodenkultur 35:1–12

    Google Scholar 

  12. Burkardt C, Insam H, Hutchinson TC, Reber HH (1993) Impact of heavy metals on the degradative capabilities of soil bacterial communities. Biol Fertil Soils 16:154–156

    Google Scholar 

  13. CEC: Commission of the European Communities (1986) Council Directive of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Official Journal of the European Communities L 181 (86/ 278/EEC):6–12

    Google Scholar 

  14. Chander K, Brookes PC (1991) Is the dehydrogenase assay invalid as a method to estimate microbial activity in Cu-contaminated soils? Soil Biol Biochem 23:909–915

    Google Scholar 

  15. Chander K, Brookes PC (1991) Effects of Zn, Cu, Ni in sewage sludge on microbial biomass in a sandy loam soil. Soil Biol Biochem 25:1231–1239

    Google Scholar 

  16. Fließbach A, Martens A, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26:1201–1205

    Google Scholar 

  17. Frostegard A, Tunlid A, Bääth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    Google Scholar 

  18. Garland JL, Mills AL (1991) Classification and characterization of heterotropic microbial communities on the basis of patterns of community-level sole-carbon source utilization. Appl Environ Microbiol 57:2351–2359

    Google Scholar 

  19. Gonzalez-Prieto SJ, Carballas T (1995) N biochemical diversity as a factor of soil diversity. Soil Biol Biochem 27:205–210

    Google Scholar 

  20. Horak O, Kamel AA (1990) Ein Langzeitversuch zur Untersuchung der Pflanzenverfügbarkeit von Schwermetallen. VDLUFA-Schriftenreihe 32:803–808

    Google Scholar 

  21. Howard PJA (1972) Problems in the estimation of biological activity in soil. Oikos 23:235–240

    Google Scholar 

  22. Jäggi W (1976) Die Bestimmung der CO2-Bildung als Mass der bodenbiologischen Aktivität. Schweiz Landwirtsch Forsch 15:371–380

    Google Scholar 

  23. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Marcel Dekker, New York, pp 415–471

    Google Scholar 

  24. Kamel AA (1990) Ein Langzeitversuch zur Untersuchung der Pflanzenverfügbarkeit von Schwermetallen in verschiedenen Böden. PhD Thesis, Universität für Bodenkultur, Vienna

    Google Scholar 

  25. Kandeler E, Mentler M, Pfeffer M, Horak O (1990) Bodenbiologische Beurteilung der Toxozität von Schwermetallen in künstlich belasteten Böden. VDLUFA-Schriftenreihe 32:621–626

    Google Scholar 

  26. Keeney DR (1982) Nitrogen—availability indices. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Am Soc Agron, Madison, Wisconsin, pp 711–733

    Google Scholar 

  27. Ladd JN (1985) Soil enzymes. In: Vaughan D, Malcom E (eds) Soil organic matter and biological activity. Martinus Nijhoff Dr H Junk Publishers, Dordrecht, Netherlands, pp 175–221

    Google Scholar 

  28. Leita L, De Nobili M, Muhlbachova G, Mondini C, Marchiol L, Zerbi G (1995) Bioavailability and effects of heavy metals on soil microbial biomass survival during laboratory incubation. Biol Fertil Soils 19:103–108

    Google Scholar 

  29. Lummerstorfer E (1993) Wirkung abgestufter Schwermetallgaben auf bodenmikrobiologische Prozesse und auf Wachstum und Schwermetallaufnahme von Sommergerste und Winterendivie. PhD Thesis, Universität Salzburg

  30. Magurran AE (1991) Ecological diversity and its measurement. Chapman and Hall, London

    Google Scholar 

  31. McGrath SP (1994) Effects of heavy metals from sewage sludge on soil microbes in agricultural ecosystems. In: Ross SM (ed) Toxic metals in soil-plant systems. John Wiley & Sons, Chichester, pp 247–274

    Google Scholar 

  32. Nannipieri P (1994) The potential use of soil enzymes as indicators of productivity, sustainability and pollution. In: Pankhurst CE, Doube BM, Gupta VVSR, Grace PR (eds) Soil biota: management in sustainable farming systems. CSIRO Australia, Victoria, pp 238–244

    Google Scholar 

  33. Nannipieri P, Grego S, Ceccanti B (1990) Ecological significance of the biological activity in soil. In: Bollag JM, Stotzky G (eds) Soil biochemistry, vol 6, pp 293–355

  34. Nordgren A, Bääth E, Söderström B (1985) Soil microfungi in an area polluted by heavy metals. Can J Bot 63:448–455

    Google Scholar 

  35. Ohya H, Fujiwara S, Somai Y, Yamaguchi M (1988) Microbial biomass and activity in urban soils contaminated with Zn and Pb. Biol Fertil Soils 6:9–13

    Google Scholar 

  36. Perry ADM, Amaranthus MP, Borchers JG, Borchers SL, Brainerd RE (1989) Bootstrapping in ecosystems. Bioscience 39:230–237

    Google Scholar 

  37. Podani J (1990) Syn-Tax IV—computer programs for data analysis in ecology and systematics on IBM-PC and Macintosh computers. UNIDA International Centre for Science and High Technology, Trieste

    Google Scholar 

  38. Reber HH (1992) Simultaneous estimates of the diversity and the degradative capability of heavy-metal-affected soil bacteria communities. Biol Soil Fertil 13:181–186

    Google Scholar 

  39. Schinner F, Öhlinger R, Kandeler E, Margesin R (1996) Methods in soil biology. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  40. Sinsabaugh RL (1994) Enzymic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74

    Google Scholar 

  41. Sterritt RM, Lester JN (1980) Interaction of heavy metals with bacteria. Sci Total Environ 14:5–17

    Google Scholar 

  42. Thun R, Herrmann R et al (1949) Die Untersuchung von Böden. Neumann, Radebeul Berlin, pp 15–28

    Google Scholar 

  43. Tyler G (1981) Heavy metals in soil biology and biochemistry. In: Paul EA, Ladd JN (eds) soil biochemistry, vol 5, pp 371–413

  44. Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and proposed modification of chromic titration method. Soil Sci 37:29–38

    Google Scholar 

  45. Zak JC, Willig MR, Moorhead DL, Woldman HG (1994) Functional diversity of microbial communities: A quantitative approach. Soil Biol Biochem 26:1101–1108

    Google Scholar 

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Correspondence to F. Kandeler.

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Dedicated to Professor J. C. G. Ottow on the occasion of his 60th birthday

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Kandeler, F., Kampichler, C. & Horak, O. Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23, 299–306 (1996). https://doi.org/10.1007/BF00335958

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Key words

  • Heavy metals
  • Soil microbial biomass
  • Soil enzymes
  • Functional diversity