Skip to main content
Log in

Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD

  • Original Article
  • Published:
Environmental Earth Sciences Aims and scope Submit manuscript

Abstract

A laboratory study was conducted to evaluate the response of soil enzyme activities (namely dehydrogenase, phosphatase and urease) to different levels of trace element pollution in soil representative area. The improved ecological dose model and random-amplified polymorphic DNA (RAPD) were used to assess soil health. The 50% ecological dose (ED50) values modified by toxicant coefficient were calculated from the best-fit model, and determination values from the regression analysis for the three enzyme activities were studied after the incubation periods. The results showed that the elevated heavy metal concentration negatively affects the total population size of bacteria and actinomycetes and enzymatic activity; dehydrogenase (ED50 = 777) was the most sensitive soil enzyme, whereas urease activity (ED50 = 2,857) showed the lowest inhibition; combined pollution or elevated toxicant level would increase disappearing RAPD bands, and the number of denoting polymorphic bands was greater in combined polluted soils. All three mathematical modified models satisfactorily described the inhibition of soil enzyme activities caused by Cd and Pb, by giving the best fit.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen ON (1959) Experiments in soil bacteriology, 3rd edn. Burgess Publishing Co., Minneapolis, p 117

    Google Scholar 

  • Atesiet I, Suzen HS, Aydin A (2004) The oxidative DNA base damage in tests of rats after intraperitoneal cadmium injection. Biometals 17:371–377. doi:10.1023/B:BIOM.0000029416.95488.5f

    Article  Google Scholar 

  • Atienzar FA, Cordi B, Evenden AJ (1999) Qualitative assessment of genotoxicity using random amplified polymorphic DNA: comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Environ Toxicol Chem 18:2275–2282. doi:10.1897/1551-5028(1999)018<2275:QAOGUR>2.3.CO;2

    Google Scholar 

  • Atienzar FA, Venier P, Jha AN (2002) Evaluation of the random amplified polymorphic DNA (RAPD) assay for the detection of DNA damage and mutations. Mutat Res 521:151–163

    Google Scholar 

  • Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 47:335–379. doi:10.1007/BF00279331

    Article  Google Scholar 

  • Babich H, Bewley RJF, Stotzky G (1983) Application of the ecological dose concept to the impact of heavy metals on some microbe-mediated ecological processes in soil. Arch Environ Contam Toxicol 12:421–426

    Google Scholar 

  • Bej AK, Perlin M, Atlas RM (1992) Effect of introducing genetically engineered microorganisms on soil microbial community diversity. FEMS Microbiol Ecol 86:169–176. doi:10.1111/j.1574-6968.1991.tb04806.x

    Article  Google Scholar 

  • Belyaeva ON, Haynes RJ, Birukova OA (2005) Barley yield and soil microbial and enzyme activities as affected by contamination of two soils with lead, zinc or copper. Biol Fertil Soils 41:85–94. doi:10.1007/s00374-004-0820-9

    Article  Google Scholar 

  • Bowditch BM, Albright DG, Williams JGK (1993) Use of randomly amplified polymorphic DNA markers in comparative genomic studies. Methods Enzymol 224:294–309. doi:10.1016/0076-6879(93)24022-M

    Article  Google Scholar 

  • Chander K, Dyckmans J, Joergensen RGJ, Meyer BG, Raubuch M (2001) Different sources of heavy metals and their long-term effects on soil microbial properties. Biol Fertil Soils 34:241–247. doi:10.1007/s003740100406

    Article  Google Scholar 

  • Chen X, Tang JJ, Fang ZG, Hu S (2002) Phosphate-solubilizing microbes in rhizosphere soils of 19 weeds in southeastern China. J Zhejiang Univ Sci 3:355–361

    Google Scholar 

  • Cookson P (1999) Special variation in soil urease activity around irrigated date palms. Arid Soil Res Rehabil 13:155–169. doi:10.1080/089030699263393

    Article  Google Scholar 

  • Dick RP (1997) Soil enzyme activities as integrative indicators of soil health. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB, Wallingford, pp 121–156

    Google Scholar 

  • Dweikat I, Mackenzie S, Levy M (1993) Pedigree assessment using RAPD-DGGE in cereal crop species. Theor Appl Genet 85:497–505. doi:10.1007/BF00220905

    Article  Google Scholar 

  • Fliessbach A, Martens R, Reber HH (1994) Soil microbial biomass and activity in soils treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26:1201–1205. doi:10.1016/0038-0717(94)90144-9

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28:55–63. doi:10.1016/0038-0717(95)00100-X

    Article  Google Scholar 

  • Haanstra L, Doelman P, Oude-Voshaar JH (1985) The use of sigmoidal dose response curves in soil ecotoxicological research. Plant Soil 84:293–297. doi:10.1007/BF02143194

    Article  Google Scholar 

  • He MC, Wang ZJ, Tang HX (1998) The chemical, toxicological and ecological studies in assessing the heavy metal pollution in Le An River, China. Wat Res 32(2):510–518. doi:10.1016/S0043-1354(97)00229-7

    Article  Google Scholar 

  • Hinojosa MB, Carreira JA, Rodríguez-Maroto JM, García-Ruíz R (2008) Effects of pyrite sludge pollution on soil enzyme activities: ecological dose–response model. Sci Total Environ 396:89–99. doi:10.1016/j.scitotenv.2008.02.014

    Article  Google Scholar 

  • Hiroki M (1993) Effect of arsenic pollution on soil microbial-population. Soil Sci Plant Nutrient 39:227–235

    Google Scholar 

  • Jensen HI (1951) Notes on the biology of Azotobacter. Proc Soc Appl Bacteriol 14:89–94

    Google Scholar 

  • Kristensen HL, Debosz K, McCarty GW (2003) Short-term effects of tillage on mineralization of nitrogen and carbon in soil. Soil Biol Biochem. 35:979–986. doi:10.1016/S0038-0717(03)00159-7

    Article  Google Scholar 

  • Liu W, Li PJ, Qi XM, Zhou QX (2005) DNA changes in barley (Hordeum vulgare) seedlings induced by cadmium pollution using RAPD analysis. Chemosphere 61:158–167. doi:10.1016/j.chemosphere.2005.02.078

    Article  Google Scholar 

  • Lobo MC, Sastre I, Vicente MA (2000) Enzymes as a measurement of environmental impact on soil. In: Garcia C, Hernandez MT (eds) Research and perspectives of soil enzymology in Spain. CEBAS-CSIC, Spain, pp 325–352

    Google Scholar 

  • Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Maliszewska-Kordybach B, Smreczak B (2003) Habitat function of agricultural soils as affected by heavy metals and polycyclic aromatic hydrocarbons contamination. Environ Int 28:719–728. doi:10.1016/S0160-4120(02)00117-4

    Article  Google Scholar 

  • Martin JP (1950) Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Sci 69:215–232

    Article  Google Scholar 

  • McBride MB (1989) Reactions controlling heavy metals solubility in soils. In: Stewart BA (ed) Advances in soil science. Springer, New York, pp 1–56

    Google Scholar 

  • Mench M, Renella G, Gelsomino A, Landi L, Nannipieri P (2006) Biochemical parameters and bacterial species richness in soils contaminated by sludge-borne metals and remediated with inorganic soil amendments. Environ Pollut 144:24–31. doi:10.1016/j.envpol.2006.01.014

    Article  Google Scholar 

  • Moreno JL, Herna’ndez T, Garcı’a C (1999) Effects of a cadmium contaminated sewage sludge compost on dynamics of organic matter and microbial activity in an arid soil. Biol Fertil Soils 28:230–237. doi:10.1007/s003740050487

    Article  Google Scholar 

  • Moreno JL, Landi C, Garcı’a L, Falchini L, Pietramellara G, Nannipieri P (2001) The ecological dose value (ED50) for assessing Cd toxicity on ATP content and dehydrogenase and urease activities of soil. Soil Biol Biochem 33:483–489. doi:10.1016/S0038-0717(00)00189-9

    Article  Google Scholar 

  • Moreno JL, Garcı’a C, Herna’ndez T (2003) Toxic effect of cadmium and nickel on soil enzymes and the influence of adding sewage sludge. Eur J Soil Sci 54:377–386. doi:10.1046/j.1365-2389.2003.00533.x

    Article  Google Scholar 

  • Nair SK, Subba-Rao NS (1977) Microbiology of the root region of coconut and cacao under mixed cropping. Plant Soil 46:511–519. doi:10.1007/BF00015910

    Article  Google Scholar 

  • 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, Melbourne, pp 238–244

    Google Scholar 

  • Nannipieri P, Gregos S, Ceccanti B (1990) Ecological significance of the biological activity in soil. In: Bollag JM, Stotzy G (eds) Soil biochemistry, vol 6. Marcel Dekker, New York, pp 293–355

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. doi:10.1073/pnas.76.10.5269

    Article  Google Scholar 

  • Nelson JR, Lawrence CW, Hinkle DC (1996) Thymine–thymine dimmer bypass by yeast DNA–polymerase–zeta. Science 272:1646–1649. doi:10.1126/science.272.5268.1646

    Article  Google Scholar 

  • Nguyen C (2003) Rhizo deposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396. doi:10.1051/agro:2003011

    Article  Google Scholar 

  • Ogram A, Feng X (1997) Methods of soil microbial community analysis. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenback LD, Walter MV (eds) Manual of environmental microbiology. American Society for Microbiology, Washington, pp 422–430

    Google Scholar 

  • Renella G, Ortigoza ALR, Landi L, Nannipieri P (2003) Additive effects of copper and zinc on cadmium toxicity on phosphatase activities and ATP content of soil as estimated by the ecological dose (ED50). Soil Biol Biochem 35:1203–1210. doi:10.1016/S0038-0717(03)00181-0

    Article  Google Scholar 

  • Renella G, Mench M, Gelsomin A, Landi L, Nannipieri P (2005) Functional activity and microbial community structure in soils amended with bimetallic sludges. Soil Biol Biochem 37:1498–1506. doi:10.1016/j.soilbio.2005.01.013

    Article  Google Scholar 

  • Rong ZY, Yin HW (2004) A method for genotoxicity detection using random amplified polymorphism DNA with Danio rerio. Ecotoxicol Environ Saf 58:96–103. doi:10.1016/j.ecoenv.2003.09.016

    Article  Google Scholar 

  • Smolders E, Buekers J, Oliver I, McLaughlin MJ (2004) Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environ Toxicol Chem 23:2633–2640. doi:10.1897/04-27

    Article  Google Scholar 

  • Speir TW, Kettles HA, Parshotam A, Searle PL, Vlaar LNC (1995) A simple kinetic approach to derive the ecological dose value, ED50, for the assessment of Cr(VI) toxicity to soil biological properties. Soil Biol Biochem 27:801–810. doi:10.1016/0038-0717(94)00231-O

    Article  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 30:1–307

    Google Scholar 

  • Tabatabai MA, Bremner JM (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–487. doi:10.1016/0038-0717(72)90064-8

    Article  Google Scholar 

  • Viketoft M, Palmborg C, Sohlenius B, Huss-Danell K, Bengtsson J (2005) Plant species effects on soil nematode communities in experimental grasslands. Appl Soil Ecol 30:91–103. doi:10.1016/j.apsoil.2005.02.007

    Article  Google Scholar 

  • Waisberg M, Joseph P, Hale B (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117. doi:10.1016/S0300-483X(03)00305-6

    Article  Google Scholar 

  • Walker C, Goodyear C, Anderson D, Titball RW (2000) Identification of Arsenic resistant bacteria in the soil of a former munitions factory at Locknitz, Germany. Land Contam Reclam 8:13–18

    Google Scholar 

  • Wang YP, Shi JK, Wanh H, Lin Q, Chen XC, Chen YX (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67:75–81. doi:10.1016/j.ecoenv.2006.03.007

    Article  Google Scholar 

  • Welp G (1999) Inhibitory effects of the total and water-soluble concentrations of nine different metals on the dehydrogenase activity of a loess soil. Biol Fertil Soils 30:132–139. doi:10.1007/s003740050599

    Article  Google Scholar 

  • Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88:91–108. doi:10.1016/0269-7491(95)91052-M

    Article  Google Scholar 

  • Yang YH, Yao J, Hu S (2000) Effects of agricultural chemicals on DNA sequence diversity of soil microbial community: a study with RAPD marker. Microb Ecol 39:72–79. doi:10.1007/s002489900180

    Article  Google Scholar 

  • Yang Z, Liu S, Zheng D, Feng S (2006) Effects of cadmium, zinc and lead on soil enzyme activities. J Environ Sci 18:1135–1141. doi:10.1016/S1001-0742(06)60051-X

    Article  Google Scholar 

  • Zheng CR, Tu C, Chen HM (1999) Effect of combined heavy metal pollution on nitrogen mineralization potential, urease and phosphatase activities in a Typic Udic Ferrisol. Pedosphere 9(3):251–258

    Google Scholar 

  • Zhou JZ, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    Google Scholar 

Download references

Acknowledgments

This work was financially supported by Science Foundation of Shanghai (NO.07DZ12055, NO.07DZ19604 and NO.07JC14025), and National High-Tech Research and Development Plan (“863” Plan) (NO.2007AA10Z441).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yang Gao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gao, Y., Zhou, P., Mao, L. et al. Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD. Environ Earth Sci 60, 603–612 (2010). https://doi.org/10.1007/s12665-009-0200-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12665-009-0200-8

Keywords

Navigation