Journal of Soils and Sediments

, Volume 14, Issue 4, pp 666–678 | Cite as

Mechanisms of metal-phosphates formation in the rhizosphere soils of pea and tomato: environmental and sanitary consequences

  • Annabelle Austruy
  • Muhammad Shahid
  • Tiantian Xiong
  • Maryse Castrec
  • Virginie Payre
  • Nabeel Khan Niazi
  • Muhammad Sabir
  • Camille Dumat



At the global scale, soil contamination with persistent metals such as lead (Pb), zinc (Zn), and copper (Cu) induces a serious threat of entering the human food chain. In the recent past, different natural and synthetic compounds have been used to immobilize metals in soil environments. However, the mechanisms involved in amendment-induced immobilization of metals in soil remained unclear. The objective of the present work was therefore to determine the mechanisms involved in metal-phosphates formation in the rhizospheric soils of pea and tomato currently cultivated in kitchen gardens.

Materials and methods

Pea and tomato were cultivated on a soil polluted by past industrial activities with Pb and Zn under two kinds of phosphate (P) amendments: (1) solid hydroxyapatite and (2) KH2PO4. The nature and quantities of metal-P formed in the rhizospheric soils were studied by using the selective chemical extractions and employing the combination of X-ray fluorescence micro-spectroscopy, scanning electron microscopy, and electron microprobe methods. Moreover, the influence of soil pH and organic acids excreted by plant roots on metal-P complexes formation was studied.

Results and discussion

Our results demonstrated that P amendments have no effect on metal-P complex formation in the absence of plants. But, in the presence of plants, P amendments cause Pb and Zn immobilization by forming metal-P complexes. Higher amounts of metal-P were formed in the pea rhizosphere compared to the tomato rhizosphere and in the case of soluble P compared to the solid amendment. The increase in soil-metal contact time enhanced metal-P formation.


The different forms of metal-P formed for the different plants under two kinds of P amendments indicate that several mechanisms are involved in metal immobilization. Metal-P complex formation in the contaminated soil depends on the type of P amendment added, duration of soil-plant contact, type of plant species, and excretion of organic acids by the plant roots in the rhizosphere.


Low molecular weight organic acids Metal immobilization Phosphates Rhizosphere Speciation 



This work has been supported by the National Research Agency under reference ANR-12-0011-VBDU and from ADEME, France.


  1. Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192CrossRefGoogle Scholar
  2. Austruy A (2012) Aspects physiologiques et biochimiques de la tolérance à l'arsenic chez les plantes supérieures dans un contexte de phytostabilisation d'une friche industrielle. Thèse de l'Université Blaise Pascal, Clermont Ferrand, 328 pGoogle Scholar
  3. Austruy A, Wanat N, Moussard C, Vernay P, Joussein E, Ledoigt G, Hitmi A (2013) Physiological impacts of soil pollution and arsenic uptake in three plant species: Agrostis capillaris, Solanum nigrum and Vicia faba. Ecotoxicol Environ Saf 90:28–34CrossRefGoogle Scholar
  4. Bolan DNS, Naidu R, Mahimairaja S, Baskaran S (1994) Influence of low-molecular-weight organic acids on the solubilization of phosphates. Biol Fert Soils 18:311–319CrossRefGoogle Scholar
  5. Cao T, Wang M, An L, Yu Y, Lou Y, Guo S, Zuo B, Liu Y, Wu J, Cao Y et al (2009) Air quality for metals and sulfur in Shanghai, China, determined with moss bags. Environ Pollut 157:1270–1278CrossRefGoogle Scholar
  6. Chaignon V, Hinsinger P (2003) A biotest for evaluating copper bioavailability to plants in a contaminated soil. J Environ Qual 32:824–833CrossRefGoogle Scholar
  7. Chrysochoou M, Dermatas D, Grubb DG (2007) Phosphate application to firing range soils for Pb immobilization: The unclear role of phosphate. J Hazard Mater 144:1–14CrossRefGoogle Scholar
  8. Crannell BS, Eighmy TT, Krzanowski JE, Eusden JD Jr, Shaw EL, Francis CA (2000) Heavy metal stabilization in municipal solid waste combustion bottom ash using soluble phosphate. Waste Manag 20:135–148CrossRefGoogle Scholar
  9. Debela F, Arocena JM, Thring RW, Whitcombe T (2010) Organic acid-induced release of lead from pyromorphite and its relevance to reclamation of Pb-contaminated soils. Chemosphere 80:450–456CrossRefGoogle Scholar
  10. Debela F, Arocena JM, Thring RW, Whitcombe T (2013) Organic acids inhibit the formation of pyromorphite and Zn-phosphate in phosphorous amended Pb- and Zn-contaminated soil. J Environ Manag 116:156–162CrossRefGoogle Scholar
  11. Douay F, Pruvot C, Waterlot C, Fritsch C, Fourrier H, Loriette A, Bidar G, Grand C, de Vaufleury A, Scheifler R (2009) Contamination of woody habitat soils around a former lead smelter in the North of France. Sci Total Environ 407:5564–5577CrossRefGoogle Scholar
  12. Dumat C, Chiquet A, Gooddy D, Aubry E, Morin G, Juillot F, Benedetti MF (2001) Metal ion geochemistry in smelter impacted soils and soil solutions. Bull Soc Geol Fr 172:539–548CrossRefGoogle Scholar
  13. Eighmy TT, Crannell BS, Butler LG, Cartledge FK, Emery EF, Oblas D, Krzanowski JE, EL Eusden S, Francis CA (1997) Heavy Metal Stabilization in Municipal Solid Waste Combustion Dry Scrubber Residue Using Soluble Phosphate. Environ Sci Technol 31:3330–3338CrossRefGoogle Scholar
  14. Foucault Y, Lévêque T, Xiong T, Schreck E, Austruy A, Shahid M, Dumat C (2013) Green manure plants for remediation of soils polluted by metals and metalloids: Ecotoxicity and human bioavailability assessment. Chemosphere 93:1430–1435CrossRefGoogle Scholar
  15. Fritsch C, Giraudoux P, Cœurdassier M, Douay F, Raoul F, Pruvot C, Waterlot C, de Vaufleury A, Scheifler R (2010) Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties, and risk for wildlife. Chemosphere 81:141–155CrossRefGoogle Scholar
  16. Hashimoto Y, Takaoka M, Oshita K, Tanida H (2009) Incomplete transformations of Pb to pyromorphite by phosphate-induced immobilization investigated by X-ray absorption fine structure (XAFS) spectroscopy. Chemosphere 76:616–622CrossRefGoogle Scholar
  17. Huang H, Li T, Gupta DK, He Z, Yang X-E, Ni B, Li M (2012) Heavy metal phytoextraction by Sedum alfredii is affected by continual clipping and phosphorus fertilization amendment. J Environ Sci 24:376–386CrossRefGoogle Scholar
  18. Jiang G, Liu Y, Huang L, Fu Q, Deng Y, Hu H (2012) Mechanism of lead immobilization by oxalic acid-activated phosphate rocks. J Environ Sci (China) 24:919–925CrossRefGoogle Scholar
  19. Kotula PG, Keenan MR, Michael JR (2003) Automated analysis of SEM X-ray spectral images: a powerful new microanalysis tool. Microsc Microanal 9:1–17CrossRefGoogle Scholar
  20. Lapied E, Nahmani JY, Moudilou E, Chaurand P, Labille J, Rose J, Exbrayat J-M, Oughton DH, Joner EJ (2011) Ecotoxicological effects of an aged TiO2 nanocomposite measured as apoptosis in the anecic earthworm Lumbricus terrestris after exposure through water, food and soil. Environ Int 37:1105–1110CrossRefGoogle Scholar
  21. Leveque T, Capowiez Y, Schreck E, Mazzia C, Auffan M, Foucault Y, Austruy A, Dumat C (2013) Assessing ecotoxicity and uptake of metals and metalloids in relation to two different earthworm species (Eiseina hortensis and Lumbricus terrestris). Environ Pollut 179:232–241CrossRefGoogle Scholar
  22. Lopareva-Pohu A, Pourrut B, Waterlot C, Garçon G, Bidar G, Pruvot C, Shirali P, Douay F (2011) Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8-year field trial: part 1. Influence on soil parameters and metal extractability. Sci Total Environ 409:647–654CrossRefGoogle Scholar
  23. Mavropoulos E, Rossi AM, Costa AM, Perez CAC, Moreira JC, Saldanha M (2002) Studies on the mechanisms of lead immobilization by hydroxyapatite. Environ Sci Technol 36:1625–1629CrossRefGoogle Scholar
  24. Mignardi S, Corami A, Ferrini V (2012) Evaluation of the effectiveness of phosphate treatment for the remediation of mine waste soils contaminated with Cd, Cu, Pb, and Zn. Chemosphere 86:354–360CrossRefGoogle Scholar
  25. Mignardi S, Corami A, Ferrini V (2013) Immobilization of Co and Ni in Mining-Impacted Soils Using Phosphate Amendments. Water Air Soil Pollut 224:1–10CrossRefGoogle Scholar
  26. Ministry of Environment Government of Japan (2007) Current status of the Brownfields Issue in Japan Interim Report, pp. 1–26.
  27. Niazi NK, Bishop TFA, Singh B (2011a) Evaluation of spatial variability of soil arsenic adjacent to a disused cattle-dip site, using model-based geostatistics. Environ Sci Technol 45:10463–10470CrossRefGoogle Scholar
  28. Niazi NK, Singh B, Shah P (2011b) Arsenic speciation and phytoavailability in contaminated soils using a sequential extraction procedure and XANES spectroscopy. Environ Sci Technol 45:7135–7142CrossRefGoogle Scholar
  29. Niebes J-F, Dufey JE, Jaillard B, Hinsinger P (1993) Release of nonexchangeable potassium from different size fractions of two highly K-fertilized soils in the rhizosphere of rape (Brassica napus cv Drakkar). Plant Soil 155–156:403–406CrossRefGoogle Scholar
  30. Panfili F, Manceau A, Sarret G, Spadini L, Kirpichtchikova T, Bert V, Laboudigue A, Marcus MA, Ahamdach N, Libert M-F (2005) The effect of phytostabilization on Zn speciation in a dredged contaminated sediment using scanning electron microscopy, X-ray fluorescence, EXAFS spectroscopy, and principal components analysis. Geochim Cosmochim Acta 69:2265–2284CrossRefGoogle Scholar
  31. Park JH, Bolan N, Megharaj M, Naidu R (2011) Isolation of phosphate solubilizing bacteria and their potential for lead immobilization in soil. J Hazard Mater 185:829–836CrossRefGoogle Scholar
  32. Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136Google Scholar
  33. Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy Metal Stress in Plants. Springer, Berlin, pp 121–147CrossRefGoogle Scholar
  34. Radwan MA, Salama AK (2006) Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food Chem Toxicol 44:1273–1278CrossRefGoogle Scholar
  35. Raicevic S, Perovic V, Zouboulis AI (2009) Theoretical assessment of phosphate amendments for stabilization of (Pb + Zn) in polluted soil. Waste Manag 29:1779–1784CrossRefGoogle Scholar
  36. Schreck E, Foucault Y, Geret F, Pradere P, Dumat C (2011) Influence of soil ageing on bioavailability and ecotoxicity of lead carried by process waste metallic ultrafine particles. Chemosphere 85:1555–1562CrossRefGoogle Scholar
  37. Schreck E, Laplanche C, Le Guédard M, Bessoule J-J, Austruy A, Xiong T, Foucault Y, Dumat C (2013) Influence of fine process particles enriched with metals and metalloids on Lactuca sativa L. leaf fatty acid composition following air and/or soil-plant field exposure. Environ Pollut 179:242–249CrossRefGoogle Scholar
  38. Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74:78–84CrossRefGoogle Scholar
  39. Shahid M, Arshad M, Kaemmerer M, Pinelli E, Probst A, Baque D, Pradere P, Dumat C (2012a) Long-term field metal extraction by Pelargonium: phytoextraction efficiency in relation to plant maturity. Int J Phytorem 14:493–505CrossRefGoogle Scholar
  40. Shahid M, Dumat C, Aslam M, Pinelli E (2012b) Assessment of lead speciation by organic ligands using speciation models. Chem Spec Bioavailab 24:248–252CrossRefGoogle Scholar
  41. Shahid M, Dumat C, Silvestre J, Pinelli E (2012c) Effect of fulvic acids on lead-induced oxidative stress to metal sensitive Vicia faba L. plant. Biol Fertil Soils 48:689–697CrossRefGoogle Scholar
  42. Shahid M, Pinelli E, Dumat C (2012d) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J Hazard Mater 219–220:1–12CrossRefGoogle Scholar
  43. Shahid M, Ferrand E, Schreck E, Dumat C (2013a) Behavior and impact of zirconium in the soil-plant system: plant uptake and phytotoxicity. Rev Environ Contam Toxicol 221:107–127Google Scholar
  44. Shahid M, Dumat C, Pourrut B, Silvestre J, Laplanche C, Pinelli E (2013b) Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J Soils Sediments. doi: 10.1007/s11368-013-0724-0 Google Scholar
  45. Shahid M, Xiong T, Castrec-Rouelle M, Leveque T, Dumat C (2013c) Water extraction kinetics of metals, arsenic and dissolved organic carbon from industrial contaminated poplar leaves. J Environ Sci 25:2451–2459CrossRefGoogle Scholar
  46. Shahid M, Xiong T, Masood N, Leveque T, Quenea K, Austruy A, Foucault Y, Dumat C (2013d) Influence of plant species and phosphorus amendments on metal speciation and bioavailability in a smelter impacted soil: a case study of food-chain contamination. J Soils Sediments. doi: 10.1007/s11368-013-0745-8 Google Scholar
  47. Shahid M, Dumat C, Pourrut B, Sabir M, Pinelli E (2014a) Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J Geochem Explor. doi: 10.1016/j.gexplo.2014.01.003 Google Scholar
  48. Shahid M, Austruy A, Echevarria G, Arshad M, Sanaullah M, Aslam M, Nadeem M, Nasim W, Dumat C (2014b) EDTA-enhanced phytoremediation of heavy metals: a review. Soil Sediment Contam 23:389–416CrossRefGoogle Scholar
  49. Shahid M, Pinelli E, Pourrut B, Dumat C (2014c) Effect of organic ligands on lead-induced oxidative damage and antioxidant defence in the leaves of Vicia faba plants. J Geochem Explor. doi: 10.1016/j.gexplo.2014.01.008
  50. Sharma RK, Agrawal M, Marshall FM (2008) Heavy metal (Cu, Zn, Cd and Pb) contamination of vegetables in urban India: A case study in Varanasi. Environ Pollut 154:254–263CrossRefGoogle Scholar
  51. Suzuki T, Niinae M, Koga T, Akita T, Ohta M, Choso T (2014) EDDS-enhanced electrokinetic remediation of heavy metal-contaminated clay soils under neutral pH conditions. Coll Surf A: Physicochem Eng Aspects 440:145–150CrossRefGoogle Scholar
  52. Tang X, Yang J (2012) Long-term stability and risk assessment of lead in mill waste treated by soluble phosphate. Sci Total Environ 438:299–303CrossRefGoogle Scholar
  53. Uzu G, Sobanska S, Aliouane Y, Pradere P, Dumat C (2009) Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ Pollut 157:1178–1185CrossRefGoogle Scholar
  54. Valsami-Jones E, Ragnarsdottir KV, Putnis A, Bosbach D, Kemp AJ, Cressey G (1998) The dissolution of apatite in the presence of aqueous metal cations at pH 2–7. Chem Geol 151:215–233CrossRefGoogle Scholar
  55. Waterlot C, Pruvot C, Ciesielski H, Douay F (2011) Effects of a phosphorus amendment and the pH of water used for watering on the mobility and phytoavailability of Cd, Pb and Zn in highly contaminated kitchen garden soils. Ecol Eng 37:1081–1093CrossRefGoogle Scholar
  56. Weng W, Han G, Du P, Shen G (2002) The effect of citric acid addition on the formation of sol–gel derived hydroxyapatite. Mater Chem Phys 74:92–97CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Annabelle Austruy
    • 1
    • 2
  • Muhammad Shahid
    • 3
  • Tiantian Xiong
    • 1
  • Maryse Castrec
    • 4
  • Virginie Payre
    • 1
  • Nabeel Khan Niazi
    • 5
  • Muhammad Sabir
    • 5
  • Camille Dumat
    • 1
  1. 1.INPT, UPS; EcoLab (Laboratoire Ecologie fonctionnelle et Environnement); ENSATUniversité de ToulouseCastanet-TolosanFrance
  2. 2.CNRS; EcoLab; ENSATCastanet-TolosanFrance
  3. 3.Department of Environmental SciencesCOMSATS Institute of Information TechnologyVehariPakistan
  4. 4.UMR 7618, Laboratoire BioMCoUniversité Pierre et Marie CurieParis CEDEX 05France
  5. 5.Institute of Soil and Environmental SciencesUniversity of Agriculture FaisalabadFaisalabadPakistan

Personalised recommendations