Skip to main content
Log in

A real-scale soil phytoremediation

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

In the present investigation, a phytoremediation process with a combination of different plant species (Populus nigra (var.italica), Paulownia tomentosa and Cytisus scoparius), and natural growing vegetation has been proposed at real-scale (10.000 m2) to bioremediate and functionally recover a soil historically contaminated by heavy metals and hydrocarbons. In the attempts to assess both effectiveness and evolution of the remediation system towards a natural soil ecosystem, besides the pollution parameters, also parameters describing the efficiency of the microbiological components (enzyme activities), were investigated. In 3 years, the total content of hydrocarbons and heavy metals in soil decreased with time (40 % and 20–40 %, respectively), reaching concentrations under the limit of National legislation and making the site suitable for environmental reusing. The reduction in pollutants was probably the reason of the increase in dehydrogenase (indicator of overall microbial activity), β-glucosidase and phosphatase activities, enzymes related to C and P cycles, respectively. However, this trend was obviously due also to the increase of chemical nutrients, acting as substrate of these enzymes. Moreover, a phytotest carried out with Raphanus sativus, showed, after 3 years, a significant increase in percentage of plant growth, confirming a reduction in soil toxicity and an improvement in soil nutritional state. Therefore, this phytoremediation system seems very promising to perform both decontamination and functional recovery of a polluted soil at real-scale level.

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
Fig. 6

Similar content being viewed by others

References

  • Adam G, Duncan HJ (1999) Effect of diesel fuel on growth of selected plant species. Environ Geochem Health 21:353–357

    Article  CAS  Google Scholar 

  • Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 422:198–207

    Article  PubMed  CAS  Google Scholar 

  • Alkorta I, Hernandez-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Environ Sci Biotechnol 3:71–90

    Article  CAS  Google Scholar 

  • Anderson TA, Guthrie EA, Walton BT (1993) Bioremediation in the rhizosphere. Environ Sci Technol 27:2630–2636

    Article  CAS  Google Scholar 

  • APAT (2002) Guida tecnica su metodi di analisi per il suolo e i siti contaminati: utilizzo di indicatori ecotossicologici e biologici. RTI CTN_SSC 2/2002

  • Bastida F, Moreno JL, Hernandez T, Garcia C (2006) Microbiological degradation index of soils in a semiarid climate. Soil Biol Biochem 38:3463–3473

    Article  CAS  Google Scholar 

  • Bastida F, Moreno JL, Nicolás C, Hernández T, Garcia C (2009) Soil metaproteomics: a review of an emerging environmental science. Significance, methodology and perspectives. J Soil Sci 60:845–859

    Article  CAS  Google Scholar 

  • Bastida F, Nicolás C, Moreno JL, Hernández T, Garcia C (2010) Tracing Changes in the microbial community of a hydrocarbon-polluted soil by culture-dependent proteomics. Pedoshere 20:479–485

    Article  CAS  Google Scholar 

  • Baud-Grasset F, Baud-Grasset S, Safferman SI (1993) Evaluation of the bioremediation of a contaminated soil with phytotoxicity tests. Chemosphere 26:1365–1374

    Article  CAS  Google Scholar 

  • Benndorf D, Balcke GU, Harms H, Von Bergen M (2007) Functional metaproteome analysis of protein extracts from contaminated soil and groundwater. The ISME J 1:224–234

    Article  CAS  Google Scholar 

  • Bentham H, Harris JA, Birch P, Short KC (1992) Habitat classification and soil restoration assessment using analysis of soil microbiological and physicochemical characteristics. Biol Fertil Soils 29:711–718

    Google Scholar 

  • Brady NC, Weill RR (1996) The nature and properties of soils. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–228

    Article  PubMed  CAS  Google Scholar 

  • Carroll S, Goonetilleke A, Dawes L (2004) Framework for soil suitability evaluation for sewage effluent renovation. Environ Geol 46:195–208

    Article  CAS  Google Scholar 

  • Ceccanti B, Garcia C, Masciandaro G, Macci C, Doni S (2006) Soil Bioremediation: combination of earthworms and compost for the ecological remediation of a hydrocarbon polluted soil. Water Air Soil Pollut 177:383–397

    Article  CAS  Google Scholar 

  • Chauhan A, Jain RK (2010) Biodegradation: gaining insight through proteomics. Biodegradation 21:861–879

    Article  PubMed  CAS  Google Scholar 

  • Chourey K, Jansson J, VerBerkmoes N, Shah M, Chavarria KL, Tom LM, Brodie EL, Hettich RL (2010) Direct cellular lysis/protein extraction protocol for soil metaproteomics. J Proteome Res 9:6615–6622

    Article  PubMed  CAS  Google Scholar 

  • Di Lonardo S, Capuana M, Arnetoli M, Gabbrielli R, Gonnelli C (2011) Exploring the metal phytoremediation potential of three Populus alba L. clones using an in vitro screening. Environ Sci Pollut Res 18:82–90

    Article  CAS  Google Scholar 

  • Dick RP (1992) A review: long-term effects of agricultural systems on soil biochemical and microbial parameters. Agric Ecosystems Environ 40:25–36

    Article  CAS  Google Scholar 

  • Dick R (1996) Soil enzyme activities and biodiversity measurements as integrative microbiological indicators. In: Doran J, Jones A (eds) Methods for assessing soil quality. Soil Science Society of America, Madison, pp 121–156

    Google Scholar 

  • Dick WA, Tabatabai MA (1993) Significance and potential uses of soil enzymes. In: Blaine F (ed) Soil microbial ecology. Application in Agricultural and Environmental Management, Marcel Dekker, pp 95–127

    Google Scholar 

  • Doni S, Macci C, Peruzzi E, Arenella M, Ceccanti B, Masciandaro G (2012) In situ phytoremediation of a historically contaminated soil by metals, hydrocarbons and polychlorobiphenyls. J Environ Monit 14:1383–1390

    Article  PubMed  CAS  Google Scholar 

  • Doumett S, Lamperi L, Checchini L, Azzarello E, Mugnai S, Mancuso S, Petruzzelli G, Del Bubba M (2008) Heavy metal distribution between contaminated soil and Paulownia tomentosa, in a pilot-scale assisted phytoremediation study: influence of different complexing agents. Chemosphere 72:1481–1490

    Article  PubMed  CAS  Google Scholar 

  • Eapen S, D’Souza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23:97–114

    Article  PubMed  CAS  Google Scholar 

  • Eldor P (2007) Soil Microbiology, Ecology, and Biochemistry. In: Eldor P (ed) Tercera. Academic Press, Chennai, India

    Google Scholar 

  • EPA (2000) Introduction to Phytoremediation. EPA 600-R-99-107, Office of Research and Development. http://clu-in.org/download/remed/introphyto.pdf

  • Ferro AM, Rock SA, Kennedy J, Herrick JJ, Turner DL (1999) Phytoremediation of soils contaminated with wood preservatives: greenhouse and field evaluations. Int J Phytorem 1:289–306

    Article  CAS  Google Scholar 

  • Fogarty G, Facelli JM (1999) Growth and competition of Cytisus scoparius, an invasive shrub, and Australian native shrubs. Plant Ecol 144:27–35

    Article  Google Scholar 

  • Frick CM, Farrell RE, Germida JJ (1999) Assessment of phytoremediation as an in-situ technique for cleaning oil-contaminated sites. PTAC Petroleum Technology Alliance Canada Calgary, Alberta

    Google Scholar 

  • Fuentes M, Govaerts B, De Leon F, Hidalgo C, Dendooven L, Sayre KD, Etchevers J (2009) Fourteen years of applying zero and conventional tillage, crop rotation and residue management systems and its effect on physical and chemical soil quality. Eur J Agron 30:228–237

    Article  CAS  Google Scholar 

  • Garcia C, Hernandez T, Costa F, Ceccanti C, Gianni A (1993) Hydrolases in the organic matter fractions of sewage sludge: changes with compostine. Bioresour Technol 45:47–52

    Article  CAS  Google Scholar 

  • Garcia G, Zanuzzi AL, Faz A (2005) Evaluation of heavy metal availability prior to an in situ soil phytoremediation program. Biodegradation 16:187–194

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30

    Article  CAS  Google Scholar 

  • Gianfreda L, Rao MA, Piotrowska A, Palumbo G, Colombo C (2005) Soil enzyme activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution. Sci Total Environ 34:265–279

    Article  Google Scholar 

  • Gudin C, Syratt WJ (1975) Biological aspects of land rehabilitation following hydrocarbon contamination. Environ Pollut 8:107–112

    Article  Google Scholar 

  • Gurska J, Wang WX, Gerhardt KE, Khalid AM, Isherwood DM, Huang XD, Glick BR, Greenberg BM (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43:4472–4479

    Article  PubMed  CAS  Google Scholar 

  • Henner P, Schiavon M, Druelle V, Lichtfous E (1999) Phytotoxicity of ancient gaswork soils. Effect of polycyclic aromatic hydrocarbons (PAHs) on plant germination. Org Geochem 30:963–969

    Article  CAS  Google Scholar 

  • Hu ZY, Zhu YG, Li M, Zhang LG, Cao ZH, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393

    Article  PubMed  CAS  Google Scholar 

  • HUJI (2006) The Protein Purification Facility, Protein Precipitation Protocols.The Wolfson Centre for Applied Structural Biology, the Hebrew University ofJerusalem. Available from: http://wolfson.huji.ac.il

  • Hutchinson SL, Schwab AP, Banks MK (2003) Biodegradation of petroleum hydrocarbons in the rhizosphere. In: McCutcheon S, Schnoor J (eds) Phytoremediation: transformation and control of contaminants. John Wiley & Sons, Inc., Hoboken, pp 355–386

    Google Scholar 

  • Iannelli R, Bianchi V, Macci C, Peruzzi E, Chiellini C, Petroni G, Masciandaro G (2012) Assessment of pollution impact on biological activity and structure of seabed bacterial communities in the Port of Livorno (Italy). Sci Total Environ 426:56–64

    Article  PubMed  CAS  Google Scholar 

  • Indorante SJ, Follmer LR, Hammer RD, Koenig PG (1990) Particle-size analysis by a modified pipette procedure. Soil Sci Soc Am J 54:560–563

    Article  Google Scholar 

  • Jalali M, Khanlari ZV (2008) Effect of aging process on the fractionation of heavy metals in some calcareous soils of Iran. Geoderma 143:26–40

    Article  CAS  Google Scholar 

  • Joner EJ, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159

    Article  CAS  Google Scholar 

  • Kaasalainen M, Yli-Halla M (2003) Use of sequential extraction to assess metal partitioning in soils. Environ Pollut 126:225–233

    Article  PubMed  CAS  Google Scholar 

  • Kacalkova L, Tlusto P (2011) The uptake of persistent organic pollutants by plants. Cent Eur J Biol 6:223–235

    Article  CAS  Google Scholar 

  • Keith LH, Telliard WA (1979) Priority pollutants is a perspective view. Environ Sci Technol 13:416–423

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Zhu YG, Ding H (2007) Lead and cadmium in leaves of deciduous trees in Beijing, China: development of a metal accumulation index (MAI). Environ Pollut 145:387–390

    Article  PubMed  CAS  Google Scholar 

  • Lu A, Zhang S, Shan XQ (2005) Time effect on the fractionation of heavy metals in soils. Geoderma 125:225–234

    Article  CAS  Google Scholar 

  • Luo CL, Shen ZG, Li XD (2008) Root exudates increase metal accumulation in mixed cultures: implications for naturally enhanced phytoextraction. Water Air Soil Pollut 193:147–154

    Article  CAS  Google Scholar 

  • Macci C, Doni S, Peruzzi E, Masciandaro G, Mennone C, Ceccanti B (2012) Almond tree and organic fertilization for soil quality improvement in southern Italy. J Environ Manage 95:215–222

    Article  Google Scholar 

  • Macek T, Mackova M, Kas J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18:23–34

    Article  PubMed  CAS  Google Scholar 

  • Manns HR, Maxwell CD, Emery RJN (2007) The effect of ground cover or initial organic carbon on soil fungi, aggregation, moisture and organic carbon in one season with oat (Avena sativa) plots. Soil Tillage Res 96:83–94

    Article  Google Scholar 

  • Margesin R, Zimmerbauer A, Schinner F (2000) Monitoring of bioremediation by soil biological activities. Chemosphere 40:339–346

    Article  PubMed  CAS  Google Scholar 

  • Masciandaro G, Ceccanti B, Ronchi V, Bauer C (2000) Kinetic parameter of dehydrogenase in the assessment of the response of soil to vermicompost and inorganic fertilisers. Biol Fertil Soils 32:479–483

    Article  CAS  Google Scholar 

  • Masciandaro G, Fantoni E, Macci C, Doni S, Peruzzi E, Ceccanti B (2009) A preliminar ecological approach in the design and operation of a full-scale bioremediation system. Bull Sci Inf 17:59–65

    Google Scholar 

  • Matsunaga A, Yashuhara A (2003) Complete dechlorination of 1-chloronaphthalene by electrochemical reduction with naphthalene radical anion as mediator. Environ Sci Technol 37:3435–3441

    Article  PubMed  CAS  Google Scholar 

  • Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162

    Article  PubMed  CAS  Google Scholar 

  • Mocko A, Waclawek W (2004) Three-step extraction procedure for determination of heavy metals availability to vegetables. Anal Bioanal Chem 380:813–817

    Article  PubMed  CAS  Google Scholar 

  • Moreno B, Nogales R, Macci C, Masciandaro G, Benitez E (2011) Microbial eco-physiological profiles to estimate the effectiveness of rhizoremediation of trichloroethylene-contaminated soils. Ecol Indic 11:1563–1571

    Article  CAS  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nannipieri P (2006) Role of stabilised enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer-Verlag, Heidelberg, pp 75–94

    Chapter  Google Scholar 

  • Nannipieri P, Ceccanti B, Cervelli S, Matarese E (1980) Extraction of phosphatase, urease, proteases, organic carbon and nitrogen from soil. Soil Sci Soc Am J 44:1011–1016

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Nedunuri KV, Govindaraju RS, Banks MK, Schwab AP, Chen Z (2000) Evaluation of phytoremediation for field-scale degradation of total petroleum hydrocarbons. J Environ Eng 126:483–490

    Article  CAS  Google Scholar 

  • Newman EI (1985) The rhizosphere: carbon sources and microbial populations. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil: plants. Blackwell Scientific Publications, Oxford, UK, Microbes and Animals, pp 107–121

    Google Scholar 

  • Nielsen M, Winding A (2002) Microorganisms as indicators of soil health. National Environmental Research Institute, Denmark

    Google Scholar 

  • Nowack B, Schulin R, Luster J (2010) Metal fractionation in a contaminated soil after reforestation: temporal changes versus spatial variability. Environ Pollut 158:3272–3278

    Article  PubMed  CAS  Google Scholar 

  • Palmroth MRT, Koskinen PEP, Kaksonen AH, Munster U, Pichtel J, Puhakka JA (2007) Metabolic and phylogenetic analysis of microbial communities during phytoremediation of soil contaminated with weathered hydrocarbons and heavy metals. Biodegradation 18:769–782

    Article  PubMed  CAS  Google Scholar 

  • Perrin-Ganier C, Schiavon F, Morel JL, Schiavon M (2001) Effect of sludge-amendment or nutrition addition on the biodegradation of the herbicide isoproturon in soil. Chemosphere 44:887–892

    Article  PubMed  CAS  Google Scholar 

  • Pule BO, Mmualefe LC (2012). Analysis of Polycyclic Aromatic Hydrocarbons in Soil with Agilent Bond Elut QuEChERS AOAC Kit and HPLC-FLD. Publication Part Number 5990-5452EN http://www.chem.agilent.com (accessed 13 Apr 2012)

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees. Environ Int 29:529–540

    Article  PubMed  CAS  Google Scholar 

  • Reilley KA, Banks MK, Schwab AP (1996) Organic chemicals in the environment: dissipation of polycyclic aromatic hydrocarbons in the rhizosphere. J Environ Qual 25:212–219

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar PBAN, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474

    Article  PubMed  CAS  Google Scholar 

  • Schneider T, Riedel K (2010) Environmental proteomics: analysis of structure and function of microbial communities. Proteomics 10:785–798

    Article  PubMed  CAS  Google Scholar 

  • Siggins A, Gunnigle E, Abram F (2012) Exploring mixed microbial community functioning: recent advances in metaproteomics. FEMS Microbiol Ecol 80:265–280

    Article  PubMed  CAS  Google Scholar 

  • Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647–658

    Article  Google Scholar 

  • Tyers M, Mann M (2003) From genomics to proteomics. Nature 422:193–197

    Article  PubMed  CAS  Google Scholar 

  • Van Dillewijn P, Caballero A, Paz JA, Gonzalez-Perez MM, Oliva JM, Ramos JL (2007) Bioremediation of 2,4,6-trinitrotoluene under field conditions. Environ Sci Technol 41:1378–1383

    Article  PubMed  Google Scholar 

  • Van Epps A (2006) Phytoremediation of petroleum hydrocarbons. Environmental Protection Agency, U.S

    Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

  • Villar P, Callejon M, Alonso E, Jimenez J, Guiraúm A (2004) Optimization and validation of a new method of analysis for polycyclic aromatic hydrocarbons in sewage sludge by liquid chromatography after microwave assisted extraction. Anal Chim Acta 524:295–304

    Article  CAS  Google Scholar 

  • Violante P (2000) Metodi di analisi chimica del suolo. Franco Angeli Editore Milan, Italy

    Google Scholar 

  • Wetzel SC, Banks MK, Schwab AP (1997) Rhizosphere effects on the degradation of pyrene and anthracene in soil. In: Kruger EL,. Anderson TA, Coats JR (eds) Phytoremediation of soil and water contaminants. ACS Symposium 664. American Chemical Society, Washington, DC, pp 254–262

  • Wilmes P, Bond PL (2004) The application of two dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environ Microbiol 6:911–920

    Article  PubMed  CAS  Google Scholar 

  • Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environ Pollut 81:229–249

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Cho Y, Eum H, Kim E (2007) Destruction of chlorinated organic solvents in a two stage molten salt oxidation reactor system. Chem Eng Sci 68:5137–5143

    Google Scholar 

  • Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plan 19:1467–1476

    Article  CAS  Google Scholar 

  • Zapusek U, Lestan D (2009) Fractionation, mobility and bio-accessibility of Cu, Zn, Cd, Pb and Ni in aged artificial soil mixtures. Geoderma 154:164–169

    Article  CAS  Google Scholar 

  • Zhou QX, Song YF (2004) Principles and methods of contaminated soil remediation. Science Press, Beijing

    Google Scholar 

Download references

Acknowledgments

The study was carried out within the framework of a project financed by San Giuliano Terme Municipality and Tuscany region. The authors would like to thank Fernando Di Giovanni and Manuele Scatena for the assistance in samples collection and preparation and Daniele Baesso for his assistance in the laboratory assays.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cristina Macci.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Macci, C., Doni, S., Peruzzi, E. et al. A real-scale soil phytoremediation. Biodegradation 24, 521–538 (2013). https://doi.org/10.1007/s10532-012-9608-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-012-9608-z

Keywords

Navigation