Bioremediation of copper-contaminated soils by bacteria

  • Jean-Yves Cornu
  • David Huguenot
  • Karine Jézéquel
  • Marc Lollier
  • Thierry LebeauEmail author


Although copper (Cu) is an essential micronutrient for all living organisms, it can be toxic at low concentrations. Its beneficial effects are therefore only observed for a narrow range of concentrations. Anthropogenic activities such as fungicide spraying and mining have resulted in the Cu contamination of environmental compartments (soil, water and sediment) at levels sometimes exceeding the toxicity threshold. This review focuses on the bioremediation of copper-contaminated soils. The mechanisms by which microorganisms, and in particular bacteria, can mobilize or immobilize Cu in soils are described and the corresponding bioremediation strategies—of varying levels of maturity—are addressed: (i) bioleaching as a process for the ex situ recovery of Cu from Cu-bearing solids, (ii) bioimmobilization to limit the in situ leaching of Cu into groundwater and (iii) bioaugmentation-assisted phytoextraction as an innovative process for in situ enhancement of Cu removal from soil. For each application, the specific conditions required to achieve the desired effect and the practical methods for control of the microbial processes were specified.


Bacteria Bioremediation Bioaugmentation Copper Fungi Pollution Phytoremediation Soil 



We would like to thank Laetitia Pinson-Gadais very much for her help in the design of the figure.


  1. Achal V, Pan X, Zhang D (2011) Remediation of copper-contaminated soil by Kocuria flava CR1 based on microbially induced calcite precipitation. Ecol Eng 37:1601–1605CrossRefGoogle Scholar
  2. Albarracín VH, Amoroso MJ, Abate CM (2005) Isolation and characterization of indigenous copper-resistant actinomycete strains. Chemie der Erde Geochem 65:145–156CrossRefGoogle Scholar
  3. Albarracín VH, Winik B, Kothe E, Amoroso MJ, Abate CM (2008) Copper bioaccumulation by the actinobacterium Amycolatopsis sp. AB0. J Basic Microbiol 48:323–330CrossRefGoogle Scholar
  4. Anbu P, Kang CH, Shin YJ, Jae-Seong So JS (2016) Formations of calcium carbonate minerals by bacteria and its multiple applications. SpringerPlus 5:250CrossRefGoogle Scholar
  5. Aouad G, Crovisier JL, Geoffroy VA, Meyer JM, Stille P (2006) Microbially mediated glass dissolution and sorption of metals by Pseudomonas aeruginosa cells and biofilm. J Hazard Mater 136:889–895CrossRefGoogle Scholar
  6. Ariyakanon N, Winaipanich B (2006) Phytoremediation of copper contaminated soil by Brassica juncea (L.). Czern and Bidens alba (L.) DC. Var. radiata. J Sci Res Chula Univ 31:49–56Google Scholar
  7. ASPITET (2000) Teneurs totales en « métaux lourds » dans les sols français résultats généraux du programme ASPITET. Courrier de l’environnement de l’INRA n°39, février 2000. Accessed 26 August 2016
  8. Bakhtiari F, Atashi H, Zivdar M, Seyedbagheri S, Fazaelipoor MH (2011) Bioleaching kinetics of copper from copper smelters dust. J Ind Eng Chem 17:29–35CrossRefGoogle Scholar
  9. Balasubramanian R, Rosenzweig AC (2008) Copper methanobactin: a molecule whose time has come. Curr Opin Chem Biol 12:245–249CrossRefGoogle Scholar
  10. Barton LL, Fauque GD (2009) Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 68:41–98CrossRefGoogle Scholar
  11. Berti WWR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals—using plants to clean up the environment. Wiley, New York, pp 71–88Google Scholar
  12. Bes C, Mench M (2008) Remediation of copper-contaminated topsoils from a wood treatment facility using in situ stabilization. Environ Pollut 156:1128–1138CrossRefGoogle Scholar
  13. Bourrelier PH, Berthelin J (1998) Contamination des sols par les éléments en traces : les risques et leur gestion. Académie des Sciences. Rapport n°42. Tec & Doc, Paris, Lavoisier.Google Scholar
  14. Brandl H, Faramarzi MA (2006) Microbe–metal-interactions for the biotechnological treatment of metal-containing solid waste. Chin Particuol 4:93–97CrossRefGoogle Scholar
  15. Braud A, Jézéquel K, Vieille E, Tritter A, Lebeau T (2006) Cr and Pb bioavailability from a polycontaminated soil using bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Wat Air Soil Poll 6:261–279CrossRefGoogle Scholar
  16. Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286CrossRefGoogle Scholar
  17. Braud A, Hubert M, Gaudin P, Lebeau T (2015) A quick rhizobacterial selection tool to be used in phytoextraction-assisted bioaugmentation of metal contaminated soils. J Appl Microbiol 119:435–445CrossRefGoogle Scholar
  18. Bruins MR, Kapil S, Oehme FW (2000) Microbial Resistance to Metals in the Environment. Ecotoxicol Environ Saf 45:198–207CrossRefGoogle Scholar
  19. Carranza F, Romero R, Mazuelos A, Iglesias N, Forcat O (2009) Biorecovery of copper from converter slags: slags characterization and exploratory ferric leaching tests. Hydrometallurgy 97:39–45CrossRefGoogle Scholar
  20. Carrillo-Castaneda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL (2003) Plant growth-promoting bacteria promote copper and iron translocation from root to shoot in alfalfa seedlings. J Plant Nutr 26:1801–1814CrossRefGoogle Scholar
  21. Cayol JL, Olivier B, Alazard D, Amils R, Godfroy A, Piette F, Prieur D (2015) The extreme conditions of life on the planet and exobiology. In: Bertrand et al (eds) Environmental microbiology: fundamentals and applications. Springer, Berlin, pp 353–394Google Scholar
  22. Chen S, Wu Z, Peng X (2014) Experimental study on weathering of seafloor volcanic glass by bacteria Pseudomonas fluorescens—implications for the contribution of bacteria to the water–rock reaction at the Mid-Oceanic Ridge setting. J Asian Earth Sci 90:15–25CrossRefGoogle Scholar
  23. Clavé G, Garoux L, Boulanger C, Hesemann P, Grison C (2016) Ecological recycling of a bio-based catalyst for Cu click reaction: a new strategy for a greener sustainable catalysis. Chem Select Commun 1:1410–1416Google Scholar
  24. Codex Alimentarius (2015) Codex general standard for contaminants and toxins in food and feed - CODEX STAN 193-1995. Accessed 26 August 2016/
  25. Comte S, Guibaud G, Baudu M (2008) Biosorption properties of extracellular polymeric substances (EPS) towards Cd, Cu and Pb for different pH values. J Hazard Mater 151:185–193CrossRefGoogle Scholar
  26. Cornu JY, Elhabiri M, Ferret C, Geoffroy VA, Jézéquel K, Leva Y, Lollier M, Schalk IJ, Lebeau T (2014) Contrasting effects of pyoverdine on the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere 103:212–219CrossRefGoogle Scholar
  27. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509Google Scholar
  28. Dimkpa CO (2016) Microbial siderophores: Production, detection and application in agriculture and environment. Endocyt Cell Res 27:7–16Google Scholar
  29. Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162CrossRefGoogle Scholar
  30. Dixit R, Wasiullah, Malaviya WD, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: An overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212CrossRefGoogle Scholar
  31. Duplay J, Semhi K, Errais E, Imfeld G, Babcsanyi I, Perrone T (2014) Copper, zinc, lead and cadmium bioavailability and retention in vineyard soils (Rouffach, France): The impact of cultural practices. Geoderma 230–231:318–328CrossRefGoogle Scholar
  32. Fang L, Wei X, Cai P, Huang Q, Chen H, Liang W, Rong X (2011) Role of extracellular polymeric substances in Cu(II) adsorption on Bacillus subtilis and Pseudomonas putida. Bioresour Technol 102:1137–1141CrossRefGoogle Scholar
  33. Fatnassi IC, Chiboub M, Saadani O, Jebara M, Jebara SH (2015) Phytostabilization of moderate copper contaminated soils using co-inoculation of Vicia faba with plant growth promoting bacteria. J Basic Microb 55:303–311CrossRefGoogle Scholar
  34. Ferret C, Sterckeman T, Cornu JY, Gangloff S, Schalk IJ, Geoffroy VA (2014) Siderophore-promoted dissolution of smectite by fluorescent Pseudomonas. Environ Microbiol Rep 6:459–467CrossRefGoogle Scholar
  35. Ferret C, Cornu JY, Elhabiri M, Sterckeman T, Braud A, Jézéquel K, Lollier M, Lebeau T, Schalk IJ, Geoffroy VA (2015) Effect of pyoverdine supply on cadmium and nickel complexation and phytoavailability in hydroponics. Environ Sci Pollut R 22:2106–2116CrossRefGoogle Scholar
  36. Flores-Vélez LM, Ducaroir J, Jaunet AM, Robert M (1996) Study of the distribution of copper in an acid sandy vineyard soil by three different methods. Eur J Soil Sci 47:523–532. doi: 10.1111/j.1365-2389.1996.tb01852.x (review)CrossRefGoogle Scholar
  37. Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14CrossRefGoogle Scholar
  38. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643CrossRefGoogle Scholar
  39. Glass DJ (2000) Economic potential of phytoremediation. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals using plants to clean up the environment. Wiley, New York, pp 15–31Google Scholar
  40. Grandlic CJ, Mendez MO, Chorover J, Machado B, Maier RM (2008) Plant growth-promoting bacteria for phytostabilization of mine tailings. Environ Sci Technol 42:2079–2084CrossRefGoogle Scholar
  41. Grigalaviciene I, Rutkoviene V, Marozas V (2005) The accumulation of heavy metals Pb, Cu and Cd at roadside forest soil. Pol J Environ Stud 14:109–115Google Scholar
  42. Grison C (2015) Combining phytoextraction and ecocatalysis: a novel concept for greener chemistry, an opportunity for remediation. Environ Sci Pollut R 22:5589–5591CrossRefGoogle Scholar
  43. Grybos M, Billard P, Desobry-Banon S, Michot LJ, Lenain JF, Mustin C (2011) Bio-dissolution of colloidal-size clay minerals entrapped in microporous silica gels. J Colloid Interface Sc 362:317–324CrossRefGoogle Scholar
  44. Hammes F, Verstraete W (2002) Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev Environ Sci Biotechnol 1:3–7CrossRefGoogle Scholar
  45. Hazotte AA, Peron O, Abdelouas A, Montavon G, Lebeau T (2016) Microbial mobilization of cesium from illite: the role of organic acids and siderophores. Chem Geol 428:8–14CrossRefGoogle Scholar
  46. Herman DC, Artiola JF, Miller RM (1995) Removal of cadmium, lead, and zinc from soil by a rhamnolipid biosurfactants. Environ Sci Technol 29:2280–2285CrossRefGoogle Scholar
  47. Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59CrossRefGoogle Scholar
  48. Huguenot D, Bois P, Cornu JY, Jézéquel K, Lollier M, Lebeau T (2015) Remediation of sediment and water contaminated by copper in small-scaled constructed wetlands: effect of bioaugmentation and phytoextraction. Environ Sci Pollut R 22:721–732CrossRefGoogle Scholar
  49. Jézéquel K, Lebeau T (2008) Soil bioaugmentation by free and immobilized bacteria to reduce potentially phytoavailable cadmium. Bioresour Technol 99:690–698CrossRefGoogle Scholar
  50. Kabata-Pendias A (2001) Trace elements in Soils and plants, 3rd edn. CRC Press, Boca RatonGoogle Scholar
  51. Kaksonen AH, Lavonen L, Kuusenaho MK, Kolli A, Närhi HM, Vestola EA, Puhakka JA, Tuovinen OH (2011) Bioleaching and recovery of metals from final slag waste of the copper smelting industry. Miner Eng 24:1113–1121CrossRefGoogle Scholar
  52. Kumpiene J, Lagerkvist A, Maurice C (2007) Stabilization of Pb- and Cu-contaminated soil using coal fly ash and peat. Environ Pollut 145:365–373CrossRefGoogle Scholar
  53. Lau PS, Lee HY, Tsang CCK, Tam NFY, Wong YS (1999) Effect of metal interference, pH and temperature on Cu and Ni biosorption by Chlorella vulgaris and Chlorella miniata. Environ Technol 20:953–961CrossRefGoogle Scholar
  54. Lebeau T (2011). Bioaugmentation for in situ soil remediation: how to ensure the success of such a process. In: Singh A, Parmar N, Kuhad RC (eds) Bioaugmentation, biostimulation and biocontrol, Chap. 7. Soil biology, vol 28, Springer, Berlin Heidelberg, pp 129–186Google Scholar
  55. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal-contaminated soils: a review. Environ Pollut 153:497–522CrossRefGoogle Scholar
  56. Li M, Cheng X, Guo H (2013) Heavy metal removal by biomineralization of urease producing bacteria isolated from soil. Int Biodeter Biodegr 76:81–85CrossRefGoogle Scholar
  57. Liu W, Yang C, Shi S, Shu W (2014) Effects of plant growth-promoting bacteria isolated from copper tailings on plants in sterilized and non-sterilized tailings. Chemosphere 97:47–53CrossRefGoogle Scholar
  58. López A, Lázaro N, Priego JM, Marqués AM (2000) Effect of pH on the biosorption of nickel and other heavy metals by Pseudomonas fluorescens 4F39. J Ind Microbiol Biotechnol 24:146–151CrossRefGoogle Scholar
  59. Mackie KA, Müller T, Kandeler E (2012) Remediation of copper in vineyards: A mini review. Environ Pollut 167:16–26CrossRefGoogle Scholar
  60. Müller D, Groves D (2000) Potassic igneous rocks and associated gold-copper mineralization. Springer, BerlinCrossRefGoogle Scholar
  61. Neubauer U, Nowack B, Furrer G, Schulin R (2000) Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ Sci Technol 34:2749–2755CrossRefGoogle Scholar
  62. Neubauer U, Furrer G, Schulin R (2002) Heavy metal sorption on soil minerals affected by the siderophore desferrioxamine B: the role of Fe(III) (hydr)oxides and dissolved Fe(III). Eur J Soil Sci 53:45–55CrossRefGoogle Scholar
  63. Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232CrossRefGoogle Scholar
  64. Perez A, Rossano S, Trcera N, Huguenot D, Fourdrin C, Verney-Carron A, van Hullebusch ED, Guyot F (2016) Bioalteration of synthetic Fe(III)-, Fe(II)-bearing basaltic glasses and Fe-free glass in the presence of heterotrophic bacteria strain Pseudomonas aeruginosa: impact of siderophores. Geochim Cosmochim Acta 118:147–162CrossRefGoogle Scholar
  65. Potysz A, Lens PNL, van de Vossenberg J, Rene ER, Grybos M, Guibaud G, Kierczak J, van Hullebusch ED (2016) Comparison of Cu, Zn and Fe bioleaching from Cu-metallurgical slags in the presence of Pseudomonas fluorescens and Acidithiobacillus thiooxidans. Appl Geochem 68:39–52CrossRefGoogle Scholar
  66. Rajkumar M, Lee KJ, Lee WH, Banu JR (2005) Growth of Brassica juncea under chromium stress: Influence of siderophores and indole 3 acetic acid producing rhizosphere bacteria. J Environ Biol 26:693–699Google Scholar
  67. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149CrossRefGoogle Scholar
  68. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194CrossRefGoogle Scholar
  69. Shutcha MN, Faucon MP, Kissi CK, Colinet G, Mahy G, Luhembwe MN, Visser M, Meerts P (2015) Three years of phytostabilisation experiment of bare acidic soil extremely contaminated by copper smelting using plant biodiversity of metal-rich soils in tropical Africa (Katanga, DR Congo). Ecol Eng 82:81–90CrossRefGoogle Scholar
  70. Smith SR (2009) A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. Environ Int 35:142–156CrossRefGoogle Scholar
  71. Solioz M, Vulpe C (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241CrossRefGoogle Scholar
  72. Su DC, Wong JWC (2004) Chemical speciation and phytoavailability of Zn, Cu, Ni and Cd in soil amended with fly ash-stabilized sewage sludge. Environ Int 29:895–900CrossRefGoogle Scholar
  73. Vestola EA, Kuusenaho MK, Närhi HM, Tuovinen OH, Puhakka JA, Plumb JJ, Kaksonen AH (2010) Acid bioleaching of solid waste materials from copper, steel and recycling industries. Hydrometallurgy 103:74–79CrossRefGoogle Scholar
  74. Viera M, Pogliani C, Donati E (2007) Recovery of zinc, nickel, cobalt and other metals by bioleaching. In: Donati R, Sand S (eds) Microbial processing of metal sulfides. Springer, Berlin, pp 103–119Google Scholar
  75. Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250CrossRefGoogle Scholar
  76. Wang T, Sun H, Jiang C, Mao H, Zhang Y (2014) Immobilization of Cd in soil and changes of soil microbial community by bioaugmentation of UV-mutated Bacillus subtilis 38 assisted by biostimulation. Eur J Soil Biol 65:62–69CrossRefGoogle Scholar
  77. Wilson-Corral V, Anderson C, Rodriguez M, Lopez-Perez J (2011) Phytoextraction of gold and copper from mine tailings with Helianthus annuus L. and Kalanchoe serrata L. Miner Eng 24:1488–1494CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Jean-Yves Cornu
    • 1
  • David Huguenot
    • 2
  • Karine Jézéquel
    • 3
  • Marc Lollier
    • 3
  • Thierry Lebeau
    • 4
    Email author
  1. 1.ISPA, INRA, Bordeaux Sciences AgroVillenave d’OrnonFrance
  2. 2.Université Paris-Est, Laboratoire Géomatériaux et Environnement (EA 4508), UPEMMarne-la-ValléeFrance
  3. 3.Université de Haute Alsace, EA 3991 LVBE (Laboratoire Vigne Biotechnologies et Environnement), Equipe Dépollution Biologique des SolsColmar cedexFrance
  4. 4.Université de Nantes, UMR 6112 LPG-Nantes (Laboratoire de Planétologie et Géodynamique de Nantes)Nantes cedex 3France

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