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Impact of heavy metal amended sewage sludge on forest soils as assessed by bacterial and fungal biosensors

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Abstract

Bacterial and fungal bioluminescence-based biosensors were used as indicators of potential heavy metal toxicity to microorganisms in the needle litter of a mature Pinus radiata forest under heavy metal contaminated sewage sludge. Sewage sludge was amended with increasing concentrations of Cu, Ni and Zn and applied to the surface of a mature P. radiata forest. The response of the bacterial and fungal biosensors to soluble Cu, Ni and Zn in needle litter extracts was investigated. The bioluminescence response of the bacterial biosensor Escherichia coli HB101 pUCD607 declined as water-soluble Zn concentrations increased. The effective concentrations that gave a 50% reduction in bioluminescence (EC50 values) for water-soluble Zn and total litter Zn were 1.3 mg l−1 and 3700 mg kg−1, respectively. The bioluminescence response of the fungal biosensor Armillaria mellea declined as soluble Cu concentrations increased. The EC50 values for water-soluble Cu and total litter Cu were 0.12 mg l−1 and 540 mg kg−1, respectively. No decline in bioluminescence was noted for either the bacterial or fungal biosensor on exposure to increasing concentrations of water-soluble Ni. The use of a combination of bacterial and fungal biosensors offers a rapid and sensitive tool for assessing toxicity of heavy metals to microorganisms and, thus, elucidating the environmental impact of contaminants in sewage sludge on litter dwelling microorganisms.

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References

  • Bell PF, James BR, Chaney RL (1991) Heavy metal extract ability in long-term sewage sludge and metal salt-amended soils. J Environ Qual 20:481–486

    CAS  Google Scholar 

  • Brockway DG (1983) Forest floor, soil, and vegetation responses to sludge fertilization in red and white pine plantations. Soil Sci Soc Am J 47:776–784

    Article  Google Scholar 

  • Chaudri AM, Knight BP, Barbosa-Jefferson VL, Preston S, Paton GI, Killham K, Coad N, Nicholson FA, Chambers BJ, McGrath SP (1999) Determination of acute Zn toxicity in pore water from soils previously treated with sewage sludge using bioluminescence assays. Environ Sci Technol 33:1880–1885

    Article  CAS  Google Scholar 

  • Chaudri AM, Lawlor K, Preston S, Paton GI, Killham K, McGrath SP (2000) Response of a Rhizobium-based luminescence biosensor to Zn and Cu in soil solutions from sewage sludge treated soils. Soil Biol Biochem 32:383–388

    Article  CAS  Google Scholar 

  • Coppola S, Dumontet S, Pontonio M, Basile G, Marino P (1988) Effect of cadmium-bearing sewage sludge on crop plants and microorganisms in two different soils. Agric Ecosyst Environ 20:181–194

    Article  CAS  Google Scholar 

  • Council of the European Communities (1991) Council Directive of 21 May 1991 concerning urban wastewater treatment (91/271/EEC). Official Journal of the European Communities L135:42–52

    Google Scholar 

  • Cox JE (1978) Soils and agriculture of part Paparua County, Canterbury, New Zealand. Soil Bur Bull 34:27–28

    Google Scholar 

  • Davis RD, Carlton-Smith CH (1981) The preparation of sewage sludges of controlled metal content for experimental purposes. Environ Pollut 2:167–177

    Article  CAS  Google Scholar 

  • Forge TA, Berrow ML, Darbyshire JF, Warren A (1993) Protozoan bioassays of soil amended with sewage sludge and heavy metals, using the common soil ciliate Colpoda steinii. Biol Fertil Soils 16:282–286

    Article  CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    Article  CAS  Google Scholar 

  • Hiroki M (1992) Effects of heavy metal contamination on soil microbial population. Soil Sci Plant Nutr 38:141–147

    CAS  Google Scholar 

  • Horswell J, Speir TW, Van Schaik AP (2003) Bio-indicators to assess impacts of heavy metals in land-applied sewage sludge. Soil Biol Biochem 35:1501–1505

    Article  CAS  Google Scholar 

  • Luo YM, Christie P (2001) Short-term effects of alkaline biosolids on pH and trace metals in oligotrophic forest peat and on growth of Picea sitchensis. Forestry 74:145–159

    Article  Google Scholar 

  • Marx DH, Berry CR, Kormanik PP (1995) Application of municipal sewage sludge to forest and degraded land. In: Agricultural utilization of urban and industrial by-products. American Soc. of Agronomy, ASA Special Publication No. 58, pp 275–295

  • McGrath SP, Knight B, Killham K, Preston S, Paton GI (1999) Assessment of the toxicity of metals in soils amended with sewage sludge using a chemical speciation technique and a lux-based biosensor. Environ Toxicol Chem 18:659–663

    Article  CAS  Google Scholar 

  • McLaren RG, Crawford DV (1973) Studies on soil copper. 1. Fractionation of copper in soils. J Soil Sci 24:172–181

    Article  CAS  Google Scholar 

  • McLaren RG, Clucas LM (2001) Fractionation of copper, nickel, and zinc in metal-spiked sewage sludge. J Environ Qual 30:1968–1975

    PubMed  CAS  Google Scholar 

  • McLaren RG, Clucas LM, Taylor MD, Hendry T (2004) Leaching of macronutrients and metals from undisturbed soils treated with metal-spiked sewage sludge. 2. Leaching of metals. Aust J Soil Res 42:459–471

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Hamon RE, McLaren RG, Speir TW, Rogers SL (2000) Review: a bioavailability-based rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Aust J Soil Res 38:1037–1086

    Article  CAS  Google Scholar 

  • New South Wales Environmental Protection Agency (NSW EPA) (1998) Environmental guidelines: use and disposal of biosolid products. NSW EPA, Sydney

  • New Zealand Waste Water Association (NZWWA) (2003) Guidelines for the safe application of biosolids to land in New Zealand. NZWWA, Wellington

  • Obbard JP, Sauerbeck DR, Jones KC (1993) Rhizobium leguminosarum bv. trifolii in soils amended with heavy metal contaminated sewage sludges. Soil Biol Biochem 25:227–231

    Article  CAS  Google Scholar 

  • Rajapaksha RMCP, Tobor-Kapùon MA, Bååth E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70:2966–2973

    Article  PubMed  CAS  Google Scholar 

  • Rattray EAS, Prosser JI, Killham K, Glover LA (1990) Luminescence-based nonextractive technique for in situ detection of Escherichia coli in soil. Appl Environ Microbiol 56:3368–3374

    PubMed  CAS  Google Scholar 

  • Shaw JJ, Kado CI (1986) Development of a Vibrio bioluminescence gene-set to monitor phytopathogenic bacteria during the ongoing disease process in a non-disruptive manner. Biotechnology 4:560–564

    Article  CAS  Google Scholar 

  • Smith SR (1996) Agricultural recycling of sewage sludge and the Environment. CAB International, Wallingford

    Google Scholar 

  • Sousa S (1999) Use of lux bacterial biosensors to assess bioremediation potential and constraints at a BTEX contaminated site. Ph.D. Thesis, University of Aberdeen

  • Sousa S, Duffy C, Weitz H, Glover LA, Bar E, Henkler R, Killham K (1998) Use of a lux-modified bacterial biosensor to identify constraints to bioremediation of BTEX-contaminated sites. Environ Toxicol Chem 17:1039–1045

    Article  CAS  Google Scholar 

  • Speir TW, van Schaik AP, Percival HJ, Close ME, Pang L (2003) Heavy metals in soil, plants and groundwater following high-rate sewage sludge application to land. Water Air Soil Pollut 150:319–358

    Article  CAS  Google Scholar 

  • Strachan G, Capel S, Maciel H, Porter AJR, Paton GI (2002) Application of cellular and immunological biosensor techniques to assess herbicide toxicity in soils. Eur J Soil Sci 53:37–44

    Article  CAS  Google Scholar 

  • Street JJ, Lindsay WL, Sabey BR (1977) Solubility and plant uptake of cadmium in soils amended with cadmium and sewage sludge. J Environ Qual 6:72–77

    Article  CAS  Google Scholar 

  • UK Department of the Environment (UK DoE) (1989) (Revised 1996) Code of practice for agricultural use of sewage sludge. HMSO, London

  • United States Environment Protection Agency (US EPA) (1993) Part 503—Standards for use and disposal of sewage sludge. Federal Register 58, pp 9387–9404

    Google Scholar 

  • Weitz HJ, Campbell CD, Killham K (2002) Development of a novel, bioluminescence-based, fungal bioassay for toxicity testing. Environ Microbiol 4:422–429

    Article  PubMed  CAS  Google Scholar 

  • Wolstenholme R, Dutch J, Moffat AJ, Bayes CD, Taylor CMA (1992) A manual of good practice for the use of sewage sludge in forestry. Forestry Commission Bulletin 107. HMSO, London

    Google Scholar 

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Acknowledgements

This work was funded by the Public Good Science Fund (PGSF), New Zealand. The fungal biosensor work was funded through the University of Aberdeen as part of the University of Aberdeen/Macaulay Institute Soil Health Initiative. We would also like to thank Dr. Graeme Paton and Professor Ken Killham (University of Aberdeen, UK) for providing us the bacterial biosensor E. coli HB101 pUCD607.

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Authors and Affiliations

  1. Institute of Environmental Science and Research Ltd., P.O. Box 50-348, Porirua, New Zealand

    Jacqui Horswell & Tom W. Speir

  2. School of Biological Sciences, Cruickshank Building, University of Aberdeen, Aberdeen, AB24 3NU, UK

    Hedda J. Weitz

  3. The Macaulay Institute, Craigiebuckler, Aberdeen, AB15 8QH, UK

    Hedda J. Weitz

  4. Landcare Research Ltd., Private Bag 11052, Palmerston North, New Zealand

    Harry J. Percival

Authors
  1. Jacqui Horswell
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  2. Hedda J. Weitz
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  3. Harry J. Percival
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  4. Tom W. Speir
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Correspondence to Jacqui Horswell.

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Horswell, J., Weitz, H.J., Percival, H.J. et al. Impact of heavy metal amended sewage sludge on forest soils as assessed by bacterial and fungal biosensors. Biol Fertil Soils 42, 569–576 (2006). https://doi.org/10.1007/s00374-005-0070-5

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  • DOI: https://doi.org/10.1007/s00374-005-0070-5

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