Skip to main content

Advertisement

Log in

Biological attributes of rehabilitated soils contaminated with heavy metals

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study aimed to evaluate the effects of two rehabilitation systems in sites contaminated by Zn, Cu, Pb, and Cd on biological soil attributes [microbial biomass carbon (Cmic), basal and induced respiration, enzymatic activities, microorganism plate count, and bacterial and fungal community diversity and structure by denaturing gradient gel electrophoresis (DGGE)]. These systems (S1 and S2) consisted of excavation (trenching) and replacement of contaminated soil by uncontaminated soil in rows with Eucalyptus camaldulensis planting (S1-R and S2-R), free of understory vegetation (S1-BR), or completely covered by Brachiaria decumbens (S2-BR) in between rows. A contaminated, non-rehabilitated (NR) site and two contamination-free sites [Cerrado (C) and pasture (P)] were used as controls. Cmic, densities of bacteria and actinobacteria, and enzymatic activities (β-glucosidase, acid phosphatase, and urease) were significantly higher in the rehabilitated sites of system 2 (S2-R and S2-BR). However, even under high heavy metal contents (S1-R), the rehabilitation with eucalyptus was also effective. DGGE analysis revealed similarity in the diversity and structure of bacteria and fungi communities between rehabilitated sites and C site (uncontaminated). Principal component analysis showed clustering of rehabilitated sites (S2-R and S2-BR) with contamination-free sites, and S1-R was intermediate between the most and least contaminated sites, demonstrating that the soil replacement and revegetation improved the biological condition of the soil. The attributes that most explained these clustering were bacterial density, acid phosphatase, β-glucosidase, fungal and actinobacterial densities, Cmic, and induced respiration.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Accioly AMA (2001) Amendments and strategies for establishment of vegetation in soils of contaminated areas by heavy metals, Doctoral Thesis, Federal University of Lavras (in Portuguese)

  • Accioly AMA, Siqueira JO (2000) Chemical contamination and soil bioremediation. In: Novais RF, Venegas VHA, Schaefer CE (eds) Topics in soil science. Soc Bras Cienc Solo, Viçosa, pp 299–352 (in Portuguese)

    Google Scholar 

  • Alef K (1995) Estimation of soil respiration. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, New York, pp 464–470

    Google Scholar 

  • Anderson JPE (1982) Soil respiration. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Chemical and microbiological properties. Am Soc Agron, Madison, pp 831–871

    Google Scholar 

  • Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such pH, on the microbial biomass of forest soil. Soil Biol Biochem 25:393–395

    Article  Google Scholar 

  • Anderson IC, Campbell CD, Prosser JI (2003) Diversity of fungi in organic soils under a moorland - Scots pine (Pinus sylvestris L.) gradient. Environ Microbiol 5:1121–1132

    Article  Google Scholar 

  • Balasoiu CF, Zagury GJZ, Deschênes L (2001) Partitioning and speciation of chromium, copper, and arsenic in CCA-contaminated soils: influence of soil composition. Sci Total Environ 280:239–255

    Article  CAS  Google Scholar 

  • Bouyoucos GJ (1951) A recalibration of the hydrometer method for making analysis of soils. Agric J 43:433–437

    Google Scholar 

  • Briuns MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Carneiro MAC, Siqueira JO, Moreira FMS (2008) Soil organic carbon, total nitrogen, microbial biomass and activity in two rehabilitation chronosequences after bauxite mining. Rev Bras Cienc Solo 32:621–632

    Article  CAS  Google Scholar 

  • Cébron A, Beguiristain T, Faure P, Norini MP, Masfaraud JF, Leyval C (2009) Influence of vegetation on the in situ bacterial community and polycyclic aromatic hydrocarbon (PAH) degraders in aged PAH-contaminated or thermal-desorption-treated soil. Appl Environ Microbiol 75:6322–6330

    Article  Google Scholar 

  • Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14

    Article  Google Scholar 

  • Clemente R, de la Fuente C, Moral R, Bernal MP (2007) Changes in microbial biomass parameters of a heavy metal-contaminated calcareous soil during a field remediation experiment. J Environ Qual 36:1137–1144

    Article  CAS  Google Scholar 

  • Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277

    Article  CAS  Google Scholar 

  • Dias-Júnior HE, Moreira FMS, Siqueira JO, Silva R (1998) Heavy metals, microbial density and activity in a soil contaminated by wastes from a zinc industry. Rev Bras Cienc Solo 22:631–640 (in Portuguese)

    Article  Google Scholar 

  • Dick RP, Breakwell DP, Turco RF (1996) Soil enzyme activities and biodiversity measurements as integrative microbiological indicators. In: Doran JW, Jones AJ (eds) Methods for assessing soil quality. Soil Sci Soc Am, Madison, pp 247–272

    Google Scholar 

  • Diels L, Geets J, Dejonghe W, Van RS, Vanbroekhoven K, Szewczyk A, Malina G (2006) Heavy metal immobilization in groundwater by in situ bioprecipitation: comments and questions about efficiency and sustainability of the process. Proc Annu Int Conf Soils, Sediments, Water Energy 11:100–112

    Google Scholar 

  • Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606

    Article  CAS  Google Scholar 

  • Eivazi F, Tabatabai MA (1990) Factors affecting glucosidase and galactosidase activities in soils. Soil Biol Biochem 22:891–897

    Article  CAS  Google Scholar 

  • Epelde L, Becerril JM, Kowalchuk GA, Deng Y, Zhou J, Garbisu C (2010) Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities. Appl Environ Microbiol 76:7843–7853

    Article  CAS  Google Scholar 

  • Farrell M, Griffith GW, Hobbs PJ, Perkins WT, Jones DL (2010) Microbial diversity and activity are increased by compost amendment of metal-contaminated soil. FEMS Microbiol Ecol 71:94–105

    Article  CAS  Google Scholar 

  • Ferreira DF (2011) Sisvar a computer statistical analysis system. Cienc Agrotec 35:1039–1042

    Google Scholar 

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

    Article  Google Scholar 

  • Gao Y, Zhou P, Mao L, Zhi Y, Zhang C, Shi W (2010) Effects of plant species coexistence on soil enzyme activities and soil microbial community structure under Cd and Pb combined pollution. J Environ Sci 22:1040–1048

    Article  CAS  Google Scholar 

  • Ge CR, Zhang QC (2011) Microbial community structure and enzyme activities in a sequence of copper-polluted soils. Pedosphere 21:164–169

    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 

  • Gómez-Sagasti MT, Alkorta I, Becerril JM, Epelde L, Anza M, Garbisu C (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Pollut 223:3249–3262

    Article  Google Scholar 

  • Gremion F, Chatzinotas A, Kaufmann K, Von Sigler W, Harms H (2004) Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol Ecol 48:273–283

    Article  CAS  Google Scholar 

  • Gülser F, Erdogan E (2008) The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ Monit Assess 145:127–133

    Article  Google Scholar 

  • Jenkinson DS (1976) The effects of biocidal treatments on metabolism in soil—IV. The decomposition of fumigated organisms in soil. Soil Biol Biochem 8:203–208

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC, Boca Raton

    Google Scholar 

  • Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306

    Article  CAS  Google Scholar 

  • Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28:61–69

    Article  CAS  Google Scholar 

  • Khan S, Cao Q, Hesham AL, Xia Y, He JZ (2007) Soil enzymatic activities and microbial community structure with different application rates of Cd and Pb. J Environ Sci 19:834–840

    Article  CAS  Google Scholar 

  • Khan S, Hesham AL, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296

    Article  CAS  Google Scholar 

  • Kiikkila O, Pennanen T, Perkiomaki J, Derome J, Fritze H (2002) Organic material as a copper immobilising agent: a microcosm study on remediation. Basic Appl Ecol 3:245–253

    Article  CAS  Google Scholar 

  • Lee SH, Park H, Koo N, Hyun S, Hwang A (2011) Evaluation of the effectiveness of various amendments on trace metals stabilization by chemical and biological methods. J Hazard Mater 188:44–51

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martin JP (1950) Use of acids rose-bengall and streptomicin in the plate method for estimating soil fungi. Soil Sci 134:215–232

    Article  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metalcontaminated soils. Plant Soil 232:207–214

    Article  CAS  Google Scholar 

  • Mehlich, A. (1953) Determination of P, Ca, Mg, K, Na and NH4. North Carolina Soil Testing Laboratories, Raleigh, NC

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Soil Biology, vol 26. Springer Verlag, Berlin, pp 215–241

    Chapter  Google Scholar 

  • National Environmental Council (CONAMA) (2009) Resolution No 420. http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=620. Accessed November 2013 (in Portuguese)

  • Niemeyer JC, Lolata GB, Carvalho GM, Silva EM, Sousa JP, Nogueira MA (2012) Microbial indicators of soil health as tools for ecological risk assessment of a metal contaminated site in Brazil. Appl Soil Ecol 59:96–105

    Article  Google Scholar 

  • Niklińska M, Chodak M, Laskowski R (2005) Characterization of the forest humus microbial community in a heavy metal polluted area. Soil Biol Biochem 37:2185–94

    Article  Google Scholar 

  • Nwachukwu OI, Pulford ID (2011) Microbial respiration as an indication of metal toxicity in contaminated organic materials and soil. J Hazard Mater 185:1140–1147

    Article  CAS  Google Scholar 

  • Oliniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228

    Article  Google Scholar 

  • Øvreås L, Forney L, Daae FL, Torvisk V (1997) Distribution of bacterioplankton in meromictic lake saelevannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373

    Google Scholar 

  • Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng 37:1889–1894

    Article  Google Scholar 

  • Powlson DS, Hirsch PR, Brookes PC (2001) The role of soil microorganisms in soil organic matter conservation in the tropics. Nutr Cycl Agroecosyst 61:41–51

    Article  Google Scholar 

  • Renella G, Mench M, Landi L, Nannipieri P (2005) Microbial activity and hydrolase synthesis in long-term Cd-contaminated soils. Soil Biol Biochem 37:33–139

    Google Scholar 

  • Ribeiro Filho MR, Curi N, Siqueira JO, Motta PEF (1999) Heavy metals in soils from a waste area in a zinc processing industry. Rev Bras Cienc Solo 23:453–464

    Article  CAS  Google Scholar 

  • Santos JV, Rangel WM, Guimarães AZ, Jaramillo PMD, Rufini M, Marra LMM, Varón López M, Silva MAP, Soares CRFS, Moreira FMS (2013) Soil biological attributes in arsenic-contaminated gold mining sites after revegetation. Ecotoxicology 22:1526–1537

    Article  Google Scholar 

  • Saviozzi A, Bufalino P, Levi-Minzi R, Riffaldi R (2002) Biochemical activities in a degraded soil restored by two amendments: a laboratory study. Biol Fertil Soils 35:96–101

    Article  CAS  Google Scholar 

  • Schipper LA, Lee WG (2004) Microbial biomass, respiration and diversity in ultramafic soils of West Dome, New Zealand. Plant Soil 262:151–8

    Article  CAS  Google Scholar 

  • Simona C, Angela RF, Santo Amalia V (2004) Suitability of soil microbial parameters as indicators of heavy metal pollution. Water Air Soil Pollut 158:21–35

    Article  Google Scholar 

  • Smit E, Leeflang P, Glandorf B, Van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621

    CAS  Google Scholar 

  • Sparling GP (1992) Ratio of microbial biomass carbon to soil organic carbon as a sensitive indicator of changes in soil organic matter. Aust J Soil Res 30:195–207

  • Stefanowicz AM, Kapusta P, Szarek-Łukaszewska G, Grodzińska K, Niklińska M, Vogt RV (2012) Soil fertility and plant diversity enhance microbial performance in metal-polluted soils. Sci Total Environ 439:211–219

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1970) Arylsulfatase activity of soils. Soil Sci Soc Am Proc 34:225–229

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–483

    Article  CAS  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) CANOCO Reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

  • USEPA (2007) Method 3051 A: microwave assisted acid digestion of sediments, sludges, soils, and oils: revision 1. Technical report. US Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Usman ARA, Kuzyakov Y, Stahr K (2004) Dynamics of organic C mineralization and the mobile fraction of heavy metals in a calcareous soil incubated with organic wastes. Water Air Soil Pollut 158:401–418

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Vásquez-Murrieta MS, Migueles-Garduño I, Franco-Hernández O, Govaerts B, Dendooven L (2006) C and N mineralization and microbial biomass in heavy-metal contaminated soil. Eur J Soil Biol 42:89–98

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang YP, Shi JY, Lin Q, Chen XC, Chen YX (2007a) Heavy metal availability and impact on activity of soil microorganisms along a Cu/Zn contamination gradient. J Environ Sci 19:848–53

    Article  CAS  Google Scholar 

  • Wang Y, Shi J, Wang H, Lin Q, Chen X, Chen Y (2007b) 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

    Article  CAS  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Winding A, Hund-Rinke K, Rutgers M (2005) The use of microorganism in ecological soil classification and assessment concepts. Ecotoxicol Environ Saf 62:230–248

    Article  CAS  Google Scholar 

  • Wollum AG (1982) Cultural methods for soil microorganisms. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2: chemical and microbiological properties, 2nd edn. Soil Sci Soc Am, Madison, pp 781–814

  • Yang D, Zeng DH, Zhang J, Li LJ, Mao R (2011) Chemical and microbial properties in contaminated soils around a magnesite mine in northeast China. Land Degrad Dev 23:256–262

    Article  Google Scholar 

  • Zhang FP, Li CF, Tong LG, Yue LX, Li P, Ciren YJ, Cao CG (2010) Response of microbial characteristics to heavy metal pollution of mining soils in central Tibet, China. Appl Soil Ecol 45:144–151

    Article  Google Scholar 

  • Zhang Y, Dong X, Jiang D, Cao B, Ge S, Hu M (2013) Assessment of the ecological security of immobilized enzyme remediation process with biological indicators of soil health. Environ Sci Pollut Res 20:5773–5780

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Coordination of Improvement of Higher Education Personnel (Capes), the Minas Gerais Research Support Foundation (FAPEMIG), and the National Council of Scientific and Technological Development (CNPq) for their financial support and fellowships granted to the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fatima Maria de Souza Moreira.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Responsible editor: Zhihong Xu

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valentim dos Santos, J., Varón-López, M., Fonsêca Sousa Soares, C. et al. Biological attributes of rehabilitated soils contaminated with heavy metals. Environ Sci Pollut Res 23, 6735–6748 (2016). https://doi.org/10.1007/s11356-015-5904-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5904-6

Keywords

Navigation