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Bioaugmentation-Assisted Phytoextraction Applied to Metal-Contaminated Soils: State of the Art and Future Prospects

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Microbes and Microbial Technology

Abstract

Bioaugmentation-assisted phytoextraction is a promising method for accelerating the cleanup rate of soils contaminated by metals. On average, bioaugmentation increases metal accumulated by plant shoots by factors of about two (metal concentration) and five, as a result of higher bioaccessibility of metals in soils, with few obvious differences between effects by bacteria or fungi (e.g., plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi). Metal bioaccessibility is always controlled by microbial siderophores as well as organic acids and surfactants. In cases of excess concentrations, fungi immobilize metals, in contrast to bacteria. Unfortunately, the typically low inoculant survival rate may impair bioaugmentation efficiency. In this chapter, microbial inoculant formulations and management are addressed, as well as strategies for selecting the most relevant plant–microorganism couples for optimum phytoextraction of soil metals. In environments subject to variable conditions, ecological engineering approaches may help in attaining maximal efficiency. Experiments at field-scale are reported, and environmental effects of the technique are discussed. Finally, future prospects are addressed with the main question being how maximal concentrations and amounts of metals in plants can be attained.

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References

  • Abbott, L. K. and Robson, A. D. 1991. Factors influencing the occurrence of vesicular-arbuscular mycorrhizas. Agric. Ecosyst. Environ. 35:121–150.

    Article  Google Scholar 

  • Abollino, O., Aceto, M., Malandrino, M., Mentasti, E., Sarzanini, C., and Petrella, F. 2002. Heavy metals of agricultural soils from Piedmont Italy. Distribution, speciation and chemometric data treatment. Chemosphere 46:545–557.

    Article  Google Scholar 

  • Abou-Shanab, R. A. I., Angle, J. S., and Chaney, R. L. 2006. Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol. Biochem. 38:2882–2889.

    Article  CAS  Google Scholar 

  • Achouak, W., Conrod, S., Cohen, V., and Heulin, T. 2004. Phenotypic variation of Pseudomonas brassicacearum as a plant root-colonization strategy. Mol. Plant Microbe Interact. 17:872–879.

    Article  CAS  Google Scholar 

  • Adriano, D. C. 1986. Trace element in the terrestrial environment. New York: Springer Verlag.

    Google Scholar 

  • Allen, H. E. 1997. Importance of speciation of metals in natural waters and soils to risk assessment. Report of International Workshop on Risk Assessment of Metals and their Inorganic Compounds, International Council on Metals and the Environment, pp. 141–157.

    Google Scholar 

  • Almas, A. R., Lombnaes, P., Sogn, T. A., and Mulder, J. 2006. Speciation of Cd and Zn in contaminated soils assessed by DGT-DIFS, and WHAM/Model VI in relation to uptake by spinach and ryegrass. Chemosphere 62:1647–1655.

    Article  CAS  Google Scholar 

  • Andrade, S. A. L., Gratão, P. L., Azevedo, R. A., Silveira, A. D. P., Schiavinato, M. A., and Mazzafera, P. 2010. Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ. Exp. Bot. 68:198–207.

    Article  CAS  Google Scholar 

  • Audet, P. and Charest, C. 2007a. Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ. Pollut. 147:609–614.

    Article  CAS  Google Scholar 

  • Audet, P. and Charest, C. 2007b. Heavy metal phytoremediation from a metal-analytical perspective. Environ. Pollut. 147:231–237.

    Article  CAS  Google Scholar 

  • Awad, F. and Romheld, V. 2000. Mobilization of heavy metals from contaminated calcareous soils by plant born, microbial and synthetic chelators and their uptake by wheat plants. J. Plant Nutr. 23:1847–1855.

    Article  CAS  Google Scholar 

  • Azcón, R., Medina, A., Roldán, A., Biró, B., and Vivas, A. 2009. Significance of treated agrowaste residue and autochthonous inoculates (Arbuscular mycorrhizal fungi and Bacillus cereus) on bacterial community structure and phytoextraction to remediate soils contaminated with heavy metals. Chemosphere 75:327–334.

    Article  CAS  Google Scholar 

  • Badri, D. V., Weir, T. L., van der Lelie, D. and Vivanco, J. M. 2009. Rhizosphere chemical ­dialogues: plant–microbe interactions. Curr. Opin. Biotechnol. 20:642–650.

    Article  CAS  Google Scholar 

  • Baker, A. J. M., McGrath, S. P., Sidoli, C. M. D., and Reeves, R. D. 1994. The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resour. Conserv. Recycl. 11:41–49.

    Article  Google Scholar 

  • Baker, A. J. M., McGrath, S. P., Reeves, R. D., and Smith, J. A. C. 2000. Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Phytoremediation of contaminated soil and water, eds. N. Terry and G. Banuelos. Boca Raton: Lewis Publisher, pp. 85–107.

    Google Scholar 

  • Banuelos, G. S. 2006. Phyto-products may be essential for sustainability and implementation of phytoremediation. Environ. Pollut. 144:19–23.

    Article  CAS  Google Scholar 

  • Barazani, O., Dudai, N., Khadka, U. R., and Golan-Goldhirsh, A. 2004. Cadmium accumulation in Allium schoenoprasum L. grown in an aqueous medium. Chemosphere 57:1213–1218.

    Article  CAS  Google Scholar 

  • Bar-Ness, E., Hadar, Y., Chen, Y., Shanzer, A., and Libman, J. 1992. Iron uptake by plants from microbial siderophores: a study with 7-nitrobenz-2 Oxa-1,3-diazole-desferrioxamine as fluorescent ferrioxamine B analog. Plant Physiol. 99:1329–1335.

    Article  CAS  Google Scholar 

  • Barona, A., Aranguiz, I., and Elias, A. 2001. Metal associations in soils before and after EDTA extractive decontamination: implications for the effectiveness of further clean-up procedures. Environ. Pollut. 113:79–85.

    Article  CAS  Google Scholar 

  • Baum, C., Hrynkiewicz, K., Leinweber, P., and Meissner, R. 2006. Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix × dasyclados). J. Plant Nutr. Soil Sci. 169:516–522.

    Article  CAS  Google Scholar 

  • Belimov, A. A., Safronova, V. I., Sergeyeva, T. A., Egorova, T. N., Matveyeva, V. A., Tsyganov, V. E., Borisov, A. Y., and Tikhonovich, I. A. 2001. Characterization of plant growth-promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 47:642–652.

    Article  CAS  Google Scholar 

  • Belimov, A. A., Kunakova, A. M., Safronova, V. I., Stepanok, V. V., Yudkin, L. Y., Alekseev, Y. V., and Kozhemyakov, A. P. 2004. Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiology 73:99–106.

    Article  CAS  Google Scholar 

  • Benizri, E., Schoeny, A., Picard, C., Courtade, A., and Guckert, A. 1997. External and internal root colonization of maize by two Pseudomonas strains: enumeration by enzyme-linked immunosorbent assay (ELISA). Curr. Microbiol. 34:297–302.

    Article  CAS  Google Scholar 

  • Bennett, L. E., Bennett, L. E., Burkhead, J. L., Hale, K. L., Terry, N., Pilon, M., and Pilon-Smits, E. A. H. 2003. Analysis of transgenic Indian mustard plants for phytoremediation of metal-contaminated mine tailings. J. Environ. Qual. 32:432–440.

    Article  CAS  Google Scholar 

  • Bianco, F. and Defez, R. 2009. Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J. Exp. Bot. 60:3097–3107.

    Article  CAS  Google Scholar 

  • Bingemann, C. W., Varner, J. E., and Martin, W. P. 1953. The effect of the addition of organic materials on the decomposition of an organic soil. Proc. Soil Sci. Soc. Am. 17:34–38.

    Article  Google Scholar 

  • Bossier, P., Hofte, M., and Verstraete, W. 1988. Ecological significance of siderophores in soil. Adv. Microb. Ecol. 10:385–414.

    CAS  Google Scholar 

  • Braud, A., Jezequel, K., and Lebeau, T. 2006a. Siderophore production by using free and immobilized cells of two pseudomonads cultivated in a medium enriched with Fe and/or toxic metals (Cr, Hg, Pb). Biotechnol. Bioeng. 94:1080–1088.

    Article  CAS  Google Scholar 

  • Braud, A., Jezequel, K., Vieille, E., Tritter, A., and Lebeau, T. 2006b. Changes in extractability of Cr and Pb in a polycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut. Focus 6:261–279.

    Article  CAS  Google Scholar 

  • Braud, A., Jezequel, K., and Lebeau, T. 2007. Impact of substrates and cell immobilization on siderophore activity by Pseudomonads in a Fe and/or Cr, Hg, Pb containing-medium. J. Hazard. Mater. 144:229–239.

    Article  CAS  Google Scholar 

  • Braud, A., Hoegy, F., Jezequel, K., Lebeau, T., and Schalk, I. J. 2009a. New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ. Microbiol. 11:1079–1091.

    Article  CAS  Google Scholar 

  • Braud, A., Jézéquel, K., Bazot, S., and Lebeau, T. 2009b. Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286.

    Article  CAS  Google Scholar 

  • Brenner, K., You, L., and Arnold, F. H. 2008. Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol. 26:483–489.

    Article  CAS  Google Scholar 

  • Brooks, R. R. and Robinson, B. H. 1998. The potential use of hyperaccumulators and other plants for phytomining. In: Plants that hyperaccumulate heavy metals: their role in archaeology, microbiology, mineral exploration, phytomining and phytoremediation, ed R. R. Brooks. Wallingford: CAB International, pp. 27–48.

    Google Scholar 

  • Brown, S. L., Chaney, R. L., Angle, J. S., and Baker, A. J. M. 1994. Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc-contaminated and cadmium-contaminated soil. J. Environ. Qual. 23:1151–1157.

    Article  CAS  Google Scholar 

  • Burd, G. I., Dixon, D. G., and Glick, B. R. 1998. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol. 64:3663–3668.

    CAS  Google Scholar 

  • Castro, I. M., Fietto, J. L. R., Vieira, R. X., Tropia, M. J. M., Campos, L. M. M., Paniago, E. B., and Brandao, R. L. 2000. Bioleaching of zinc and nickel from silicates using Aspergillus niger cultures. Hydrometallurgy 57:39–49.

    Article  CAS  Google Scholar 

  • Cattani, I., Fragoulis, G., Boccelli, R., and Capri, E. 2006. Copper bioavailability in the rhizopshere of maize (Zea mays L.) grown in two Italian soils. Chemosphere 64:1972–1979.

    Article  CAS  Google Scholar 

  • Chaudhry, Q., Blom-Zandstra, M., Gupta, S., and Joner E. J. 2005. Utilising the synergy between plants and rhizosphere microorganisms to enhance breakdown of organic pollutants in the environment. Environmental Science Pollution Research 12:34–48.

    Article  CAS  Google Scholar 

  • Chauhan, A. and Jain, R. 2010. Biodegradation: gaining insight through proteomics. Biodegradation 21:861–879.

    Article  CAS  Google Scholar 

  • Checkai, R. T., Corey, R. B., and Helmke, P. A. 1987. Effect of ionic and complexed metal concentrations on plant uptake of cadmium and micronutrient cations from solution. Plant Soil 99:335–345.

    Article  CAS  Google Scholar 

  • Chen, H. and Cutright, T. 2001. EDTA and HEDTA effects on Cd, Cr, and Ni uptake by Helianthus annuus. Chemosphere 45:21–28.

    Article  CAS  Google Scholar 

  • Chen, B. D., Li, X. L., Tao, H. Q., Christie, P., and Wong, M. H. 2003. The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846.

    Article  CAS  Google Scholar 

  • Chen, B., Shen, H., Li, X., Feng, G., and Christie, P. 2004a. Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant Soil 261:219–229.

    Article  CAS  Google Scholar 

  • Chen, Y., Shen, Z., and Li, X. 2004b. The use of vetiver grass (Vetiveria zizanioides) in the phytoremediation of soils contaminated with heavy metals. Appl. Geochem. 19:1553–1565.

    Article  CAS  Google Scholar 

  • Chen, B. D., Zhu, Y. G., and Smith, F. A. 2006. Effects of arbuscular mycorhizal inoculation uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from a uranium mining-impacted soil. Chemosphere 62:1464–1473.

    Article  CAS  Google Scholar 

  • Citterio, S., Prato, N., Fumagalli, P., Aina, R., Massa, N., Santagostino, A., Sgorbati, S., and Berta, G. 2005. The arbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes in Cannabis sativa L. Chemosphere 59:21–29.

    Article  CAS  Google Scholar 

  • Clemens, S., Palmgren, M. G., and Kramer, U. 2002. A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7:309–315.

    Article  CAS  Google Scholar 

  • Corbisier, P., van der Lelie, D., Borremans, B., Provoost, A., de Lorenzo, V., Brown, N. L., Lloyd, J. R., Hobman, J. L., Csoregi, E., Johansson, G., and Mattiasson, B. 1999. Whole cell- and protein-based biosenors for the detection of bioavailable heavy metals in environmental samples. Anal. Chim. Acta 387:235–244.

    Article  CAS  Google Scholar 

  • Crecchio, G., Gelsomino, A., Ambrosoli, R., Minati, J. L., and Ruggiero, P. 2004. Functional and molecular responses of soil microbial communities under differing soil management practices. Soil Biol. Biochem. 36:1873–1883.

    Article  CAS  Google Scholar 

  • Crowley, D., Römheld, V., Marschner, H., and Szaniszlo, P. 1992. Root-microbial effects on plant iron uptake from siderophores and phytosiderophores. Plant Soil 142:1–7.

    CAS  Google Scholar 

  • Csillag, J., Partay, G., Lukacs, A., Bujtas, K., and Nemeth, T. 1999. Extraction of soil solution for environmental analysis. Int. J. Environ. Anal. Chem. 74:305–324.

    Article  CAS  Google Scholar 

  • Curl, E. A. and Truelove, B. 1986. The rhizosphere. Berlin: Springer-Verlag.

    Google Scholar 

  • De Leij, F., Sutton, E. J., Whipps, J. M., Fenlon, J. S., and Lynch, J. M. 1995. Impact of field release of genetically modified Pseudomonas fluorescens on indigenous microbial populations of wheat. Appl. Environ. Microbiol. 61:3443–3453.

    Google Scholar 

  • de Souza, M. P., Chu, D., Zhao, M., Zayed, A. M., Ruzin, S. E., Schichnes, D., and Terry, N. 1999. Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol. 119:565–574.

    Article  Google Scholar 

  • Dejonghe, W., Boon, N., Seghers, D., Top, E. M., and Verstraete, W. 2001. Bioaugmentation of soils by increasing microbial richness: missing links. Environ. Microbiol. 3:649–657.

    Article  CAS  Google Scholar 

  • Dennis, P., Edwards, E. A., Liss, S. N., and Fulthorpe, R. 2003. Monitoring gene expression in mixed microbial communities by using DNA microarrays. Appl. Environ. Microbiol. 69:769–778.

    Article  CAS  Google Scholar 

  • Dhankher, O. P., Li, Y., Rosen, B. P., Shi, J., Salt, D., Senecoff, J. F., Sashti, N. A., and Meagher, R. B. 2002. Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat. Biotechnol. 20:1140–1145.

    Article  CAS  Google Scholar 

  • Di Gregorio, S., Barbafieri, M., Lampis, S., Sanangelantoni, A. M., Tassi, E., and Vallini, G. 2006. Combined application of Triton X-100 and Sinorhizobium sp. Pb002 inoculum for the improvement of lead phytoextraction by Brassica juncea in EDTA amended soil. Chemosphere 63:293–299.

    Article  CAS  Google Scholar 

  • Di Simine, C. D., Sayer, J. A., and Gadd, G. M. 1998. Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from a forest soil. Biol. Fertil. Soils 28:87–94.

    Article  Google Scholar 

  • Diels, L., De Smet, M., Hooyberghs, L., and Corbisier, P. 1999. Heavy metals bioremediation of soil. Mol. Biotechnol. 12:154–158.

    Article  Google Scholar 

  • Diez Lazaro, J., Kidd, P. S., and Monterroso Martinez, C. 2006. A phytogeochemical study of the Tras-os-Montes region (NE Portugal): possible species for plant-based soil remediation technologies. Sci. Total Environ. 354:265–277.

    Article  CAS  Google Scholar 

  • Dimkpa, C. O., Merten, D., Svato, A., Büchel, G., and Kothe, E. 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107:1687–1696.

    Article  CAS  Google Scholar 

  • Dubbin, W. E. and Ander, L. E. 2003. Influence of microbial hydroxamate siderophores on Pb(II) desorption from α-FeOOH. Appl. Geochem. 18:1751–1756.

    Article  CAS  Google Scholar 

  • Duffy, B. K. and Defago, G. 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65:2429–2438.

    CAS  Google Scholar 

  • Duijff, B. J., Bakker, P. A. H. M., and Schippers, B. 1991. Influence of pseudobactin-358 on the iron nutrition of plants. 6th Int. Fe Symp. 31.

    Google Scholar 

  • Duponnois, R., Kisa, M., Assigbetse, K., Prin, Y., Thioulouse, J., Issartel, M., Moulin, P., and Lepage, M. 2006. Fluorescent pseudomonads occuring in Macrotermes subhyalinus mound structures decrease Cd toxicity and improve its accumulation in sorghum plants. Sci. Total Environ. 370:391–400.

    Article  CAS  Google Scholar 

  • Duquène, L., Vandenhove, H., Tack, F., Van Hees, M., and Wannijn, J. 2010. Diffusive gradient in thin FILMS (DGT) compared with soil solution and labile uranium fraction for predicting uranium bioavailability to ryegrass. J. Environ. Radioact. 101:140–147.

    Article  CAS  Google Scholar 

  • Duquenne, P., Chenu, C., Richard, G., and Catroux, G. 1999. Effect of carbon source supply and its location on competition between inoculated and established bacterial strains in sterile soil microcosm. FEMS Microbiol. Ecol. 29:331–339.

    Article  CAS  Google Scholar 

  • Duss, F., Mozafar, A., Oertli, J. J., and Jaeggi, W. 1986. Effect of bacteria on the iron uptake by axenically-cultured roots of Fe-efficient and Fe-inefficient tomatoes (Lycopersicon esculentum mill.). J. Plant Nutr. 9:587–598.

    Article  Google Scholar 

  • El Fantroussi, S. and Agathos, S. N. 2005. Is bioaugmentation a feasible strategy for pollutant removal and site remediation? Curr. Opin. Microbiol. 8:268–275.

    Article  CAS  Google Scholar 

  • El-Kherbawy, M., Angle, J. S., Heggo, A., and Chaney, R. L. 1989. Soil pH, rhizobia, and vesicular-arbuscular mycorrhizae inoculation effects on growth and heavy metal uptake of alfalfa (Medicago sativa L.). Biol. Fertil. Soils 8:61–65.

    Article  CAS  Google Scholar 

  • Epelde, L., Mijangos, I., Becerril, J. M., and Garbisu, C. 2009. Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol. Biochem. 41:1788–1794

    Article  CAS  Google Scholar 

  • Evangelou, M. W. H., Ebel, M., and Schaeffer, A. 2007. Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68:989–1003.

    Article  CAS  Google Scholar 

  • Evans, K. M., Katherine, M., Gatehouse, J. A., Lindsay, W. P., Shi, J., Tommey, A. M., and Robinson, N. J. 1992. Expression of the pea metallothionein-like gene PsMTA in Escherichia coli and Arabidopsis thaliana and analysis of trace metal ion accumulation: implications for PsMTA function. Plant Mol. Biol. 20:1019–1028.

    Article  CAS  Google Scholar 

  • Farwell, A. J., Vesely, S., Nero, V., Rodriguez, H., McCormack, K., Shah, S., Dixon, D. G., and Glick, B. R. 2007. Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ. Pollut. 147:540–545.

    Article  CAS  Google Scholar 

  • Feng, M. H., Shan, X. Q., Zhang, S. Z., and Wen, B. 2005. Comparison of a rhizosphere-based method with other one-step extraction methods for assessing the bioavailability of soil metals to wheat. Chemosphere 59:939–949.

    Article  CAS  Google Scholar 

  • Filgueiras, A. V., Lavilla, I., and Bendicho, C. 2002. Chemical sequential extraction for metals partitioning in environmental solid samples. J. Environ. Monit. 4:823–857.

    Article  CAS  Google Scholar 

  • Forstner, U. 1995. Land contamination by heavy metals: global scope and magnitude of problem. In: Metal speciation and contamination of soils, ed. H. E. Allen. Boca Raton: Lewis Publishers, pp. 1–33.

    Google Scholar 

  • Gadd, G. M. 1993. Microbial formation and transformation of organometallic and organometalloid compounds. FEMS Microbiol. Rev. 11:297–316.

    Article  CAS  Google Scholar 

  • Gadd, G. M. 2001. Microbial metal transformation. J. Microbiol. 39:83–88.

    CAS  Google Scholar 

  • Gadd, G. M. 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119.

    Article  CAS  Google Scholar 

  • Gadd, G. M. and White, C. 1993. Microbial treatment of metal pollution – a working biotechnology? Trends Biotechnol. 11:353–359.

    Article  CAS  Google Scholar 

  • Gentry, T. J., Rensing, C., and Pepper, I. L. 2004. New approaches for bioaugmentation as a remediation technology. Crit. Rev. Environ. Sci. Technol. 34:447–494.

    Article  CAS  Google Scholar 

  • Gisbert, C., Ros, R., De Haro, A., Walker, D. J., Pilar Bernal, M., Serrano, R., and Navarro-Avino, J. 2003. A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem. Biophys. Res. Commun. 303:440–445.

    Article  CAS  Google Scholar 

  • Gleba, D., Borisjuk, N. V., Borisjuk, L. G., Kneer, R., Poulev, A., Skarzhinska, M., Dushenkov, S., Logendra, S., Gleba, Y. Y., and Raskin, L. 1999.Use of plant roots for phytoremediation and molecular farming. Proc. Natl Acad. Sci. 96:5973–5977.

    Article  CAS  Google Scholar 

  • Glick, B. R. 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41:109–117.

    Article  CAS  Google Scholar 

  • Glick, B. R. 2003. Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol. Adv. 21:383–393.

    Article  CAS  Google Scholar 

  • Glick, B. R. 2010. Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 28:367–374.

    Article  CAS  Google Scholar 

  • Gonzaga, M., Ma, L., and Santos, J. 2007. Effects of plant age on arsenic hyperaccumulation by Pteris vittata L. Water Air Soil Pollut. 186:289–295.

    Article  CAS  Google Scholar 

  • González-Chávez, M. C., Carrillo-González, R., Wright, S. F., and Nichols, K. A. 2004. The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ. Pollut. 130:317–323.

    Article  CAS  Google Scholar 

  • Grichko, V. P., Filby, B., and Glick, B. R. 2000. Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb, and Zn. J. Biotechnol. 81:45–53.

    Article  CAS  Google Scholar 

  • Gries, D., Brunn, S., Crowley, D. E., and Parker, D. R. 1995. Phytosiderophore release in relation to micronutrient metal deficiencies in barley. Plant Soil 172:299–308.

    Article  CAS  Google Scholar 

  • Groleau-Renaud, V., Plantureux, S., Tubeileh, A., and Guckert, A. 2000. Influence of microflora and composition of root bathing solution on root exudation of maize plants. J. Plant Nutri. 23:1283–1301.

    Article  CAS  Google Scholar 

  • Guo, Y., George, E., and Marschner, H. 1996. Contribution of an arbuscular mycorrhizal fungus to the uptake of cadmium and nickel in bean and maize plants. Plant Soil 184:195–205.

    Article  CAS  Google Scholar 

  • Gupta, R. and Aten, R. 1993. Comparison and evaluation of extraction media and their suitability in a simple model to predict the biological relevance of heavy metal concentrations in contaminated soils. Int. J. Envir. Anal. Chem. 51:25–46.

    Article  CAS  Google Scholar 

  • Gupta, A. K. and Sinha, S. 2006a. Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants. Chemosphere 64:161–173.

    Article  CAS  Google Scholar 

  • Gupta, A. K. and Sinha, S. 2006b. Role of Brassica juncea (L.) Czern. (var. Vaibhav) in the phytoextraction of Ni from soil amended with fly ash: selection of extractant for metal bioavailability. J. Hazard. Mater. 136:371–378.

    Article  CAS  Google Scholar 

  • Halstead, R. L., Finn, B. J., and McLean, A. J. 1969. Extractability of nickel added to the soils and its concentration in plants. Can. J. Soil Sci. 49:335–342.

    Article  CAS  Google Scholar 

  • Hammer, D. and Keller, C. 2002. Changes in the rhizosphere of metal-accumulating plants evidenced by chemical extractants. J. Environ. Qual. 31:1561–1569.

    Article  CAS  Google Scholar 

  • Haynes, R. J. 1990. Active ion uptake and maintenance of cation–anion balance: a critical examination of their role in regulating rhizosphere pH. Plant Soil 126:247–264.

    Article  CAS  Google Scholar 

  • Hazen, T. C. and Stahl, D. A. 2006. Using the stress response to monitor process control: pathways to more effective bioremediation. Curr Opin. Biotechnol. 17:285–290.

    Article  CAS  Google Scholar 

  • Heggo, A., Angle, J. S., and Chaney, R. L. 1990. Effects of vesicular-arbuscular mycorrhizal fungi on heavy metal uptake by soybeans. Soil Biol. Biochem. 22:865–869.

    Article  CAS  Google Scholar 

  • Hinchman, R. R., Negri, M. C., and Gatliff, E. G. 1998. Phytoremediation: using green plants to cleanup contaminated soil, groundwater and wastewater. Argonne, IL: Argonne National Laboratory.

    Google Scholar 

  • Hinsinger, P., Plassard, C., Tang, C., and Jaillard, B. 2003. Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59.

    Article  CAS  Google Scholar 

  • Höflich, G. and Metz, R. 1997. Interactions of plant–microorganism associations in heavy metal containing soils from sewage farms. Die Bodenkultur 48:239–247.

    Google Scholar 

  • Höfte, M., Buysens, S., Koedam, N., and Cornelis, P. 1993. Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals 6:85–91.

    Article  Google Scholar 

  • Hovsepyan, A. and Greipsson, S. 2004. Effect of arbuscular mycorrhizal fungi on phytoextraction by corn (Zea mays) of lead-contaminated soil. Int. J. Phytoremed. 6:305–321.

    Article  CAS  Google Scholar 

  • Huang, J. W. and Cunningham, S. D. 1996. Lead phytoextraction: species variation in lead uptake and translocation. New Phytol. 134:75–84.

    Article  CAS  Google Scholar 

  • Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W. W., and Sessitsch, A. 2004. Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl. Environ. Microbiol. 70:2667–2677.

    Article  CAS  Google Scholar 

  • Imsande, J. 1998. Iron, sulfur, and chlorophyll deficiencies: a need for an integrative approach in plant physiology. Physiol. Plant. 103:139–144.

    Article  CAS  Google Scholar 

  • Iwamoto, T. and Nasu, M. 2001. Current bioremediation practice and perspective. J. Biosci. Bioeng. 92:1–8.

    Article  CAS  Google Scholar 

  • James, B. R. and Bartlett, R. J. 1984. Plant–soil interactions of chromium. J. Environ. Qual. 13:67–70.

    Article  CAS  Google Scholar 

  • Jankong, P., Visoottiviseth, P., and Khokiattiwong, S. 2007. Enhanced phytoremediation of arsenic contaminated land. Chemosphere 68:1906–1912.

    Article  CAS  Google Scholar 

  • Jansson, J. K. 2003. Marker and reporter genes: illuminating tools for environmental microbiologists. Curr. Opin. Microbiol. 6:310–316.

    Article  CAS  Google Scholar 

  • Jiang, C. Y., Sheng, X. F., Qian, M., and Wang, Q. Y. 2008. Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164.

    Article  CAS  Google Scholar 

  • Jing, Y. D., He, Z. L., and Yang, X. E. 2007. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. Sci. B 8:192–207.

    Article  CAS  Google Scholar 

  • Joner, E. J. and Leyval, C. 1997. Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol. 135:353–360.

    Article  CAS  Google Scholar 

  • Jurkevitch, E., Hadar, Y., and Chen, Y. 1988. Involvement of bacterial siderophores in the remedy of lime-induced chlorosis in peanut. Soil Sci. Soc. Am. J. 52:1032–1037.

    Article  CAS  Google Scholar 

  • Kalembkiewicz, J. and Socco, E. 2002. Investigations of sequential extraction of chromium from soil. Polish J. Environ. Stud. 11:245–250.

    CAS  Google Scholar 

  • Kandasamy, S., Loganathan, K., Muthuraj, R., Duraisamy, S., Seetharaman, S., Thiruvengadam, R., Ponnusamy, B., and Ramasamy, S. 2009. Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci. 7:47.

    Article  CAS  Google Scholar 

  • Karenlampi, S., Schat, H., Vangronsveld, J., Verkleij, J. A. C., van der Lelie, D., Mergeay, M., and Tervahauta, A. I. 2000. Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ. Pollut. 107:225–231.

    Article  CAS  Google Scholar 

  • Kayser, G., Korckritz, T., and Markert, B. 2001. Bioleaching for the decontamination of heavy metals. Wasser Boden 53:54–58.

    CAS  Google Scholar 

  • Keller, C. and Hammer, D. 2005. Alternatives for phytoextraction: biomass plants versus hyperaccumulators. Geophys. Res. Abstr. 7.

    Google Scholar 

  • Kennedy, I. R., Choudhury, A. T. M. A., and Kecskés, M. L. 2004. Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol. Biochem. 36:1229–1244.

    Article  CAS  Google Scholar 

  • Khan, A. G. 2005. Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J. Trace Elem. Med. Biol. 18:355–364.

    Article  CAS  Google Scholar 

  • Khan, M. R. and Khan, S. M. 2002. Effects of root-dip treatment with certain phosphate solubilizing microorganisms on the fusarial wilt of tomato. Biores. Technol. 85:213–215.

    Article  CAS  Google Scholar 

  • Khan, A. G., Kuek, C., Chaudhry, T. M., Khoo, C. S., and Hayes, W. J. 2000. Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:97–207.

    Article  Google Scholar 

  • Kheboian, C. and Bauer, C. F. 1987. Accuracy of selective extraction procedures for metal speciation in model aquatic sediments. Anal. Chem. 59:417–1423.

    Article  Google Scholar 

  • Kinnersley, A. M. 1993. The role of phytochelates in plant growth and productivity. Plant Growth Regul. 12:207–218.

    Article  CAS  Google Scholar 

  • Krämer, U. and Chardonnens, A. N. 2001. The use of transgenic plants in the bioremediation of soils contaminated with trace elements. Appl. Microbiol. Biotechnol. 55:661–672.

    Article  Google Scholar 

  • Kramer, U., Cotter-Howells, J. D., Charnock, J. M., Baker, A. J. M., and Smith, J. A. C. 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638.

    Article  CAS  Google Scholar 

  • Krotzky, A., Berggold, R., and Werner, D. 1988. Plant characteristics limiting associative N2-fixation (C2H2-reduction) with two cultivars of Sorghum nutans. Soil Biol. Biochem. 20:157–162.

    Article  CAS  Google Scholar 

  • Kuiper, I., Bloemberg, G., and Lugtenberg, B. 2001. Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol. Plant Microbe Interact. 14:1197–1205.

    Article  CAS  Google Scholar 

  • Kuiper, I., Lagendijk, E. L., Bloemberg, G. V., and Lugtenberg, B. J. J. 2004. Rhizoremediation: a beneficial plant–microbe interaction. Mol. Plant Microbe Interact. 17:6–15.

    Article  CAS  Google Scholar 

  • Kumar, P. B. A. N., Dushenkov, V., Motto, H., and Raskin, Y. 1995. Phytoextraction: the use of plants to remove heavy metals from soils. Environ. Sci. Technol. 29:232–1238.

    Article  Google Scholar 

  • Kumar, K. V., Singh, N., Behl, H. M., and Srivastava, S. 2008. Influence of plant growth promoting bacteria and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended soil. Chemosphere 72:678–683.

    Article  CAS  Google Scholar 

  • Kush, A. K. and Dadarwal, K. R. 1981. Root exudates as pre-invasive factors in the modulation of chick pea varieties. Soil Biol. Biochem. 13:51–55.

    Article  CAS  Google Scholar 

  • Labana, S., Pandey, G., Paul, D., Sharma, N. K., Basu, A., and Jain, R. K. 2005. Pot and field studies on bioremediation of p-nitrophenol contaminated soil using Arthrobacter protophormiae RKJ100. Environ. Sci. Technol. 39:3330–3337.

    Article  CAS  Google Scholar 

  • Lampis, S., Ferrari, A., Cunha-Queda, A., Alvarenga, P., Di Gregorio, S., and Vallini, G. 2009. Selenite resistant rhizobacteria stimulate SeO 2−3 phytoextraction by Brassica juncea in bioaugmented water-filtering artificial beds. Environ. Sci. Pollut. Res. Int. 16:663–670.

    Article  CAS  Google Scholar 

  • LaPara, T. M., Zakharova, T., Nakatsu, C. H., and Konopka, A. 2002. Functional and structural adaptations of bacterial communities growing on particulate substrates under stringent nutrient limitation. Microb. Ecol. 44:317–326.

    Article  CAS  Google Scholar 

  • Latour, X., Corberand, T., Laguerre, G., Allard, F., and Lemanceau, P. 1996. The composition of fluorescent Pseudomonad populations associated with roots is influenced by plant and soil type. Appl. Environ. Microbiol. 62:2449–2456.

    CAS  Google Scholar 

  • Latour, X., Delorme, S., Mirleaub, P., and Lemanceau, P. 2003. Identification of traits implicated in the rhizosphere competence of fluorescent pseudomonads: description of a strategy based on population and model strain studies. Agronomie 23:397–405.

    Article  Google Scholar 

  • Lebeau, T. 2010. Bioaugmentation for in situ soil remediation: how to ensure the success of such a process. In: Bioaugmentation, biostimulation and biocontrol, eds. A. Singh, N. Parmar, and R. Kuhad, Chapter 10. “Soil Biology” series, Springer, in press.

    Google Scholar 

  • Lebeau, T., Bagot, D., Jézéquel, K., and Fabre, B. 2002. Cadmium biosorption by free and immobilised microorganisms cultivated in a liquid soil extract medium: effects of Cd, pH and techniques of culture. Sci. Total Environ. 291:73–83.

    Article  CAS  Google Scholar 

  • Lebeau, T., Braud, A., and Jézéquel, K. 2008. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ. Pollut. 153:497–522.

    Article  CAS  Google Scholar 

  • Lee, M. H., Weidhaas, J., Macbeth, T., Swift, D., and Rothermel, J. S. 2009. Fluorescent in situ hybridization (FISH) techniques for remediation, In Situ and on-site bioremediation – 2009: Proc. 10th Intl. In Situ and On-Site Bioremediation Symp. 40.

    Google Scholar 

  • Lewandowski, I., Schmidt, U., Londo, M., and Faaij, A. 2006. The economic value of the phytoremediation function – assessed by the example of cadmium remediation by willow (Salix ssp). Agric. Syst. 89:68–89.

    Article  Google Scholar 

  • Leyval, C., Turnau, K., and Haselwandter, K. 1997. Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153.

    Article  CAS  Google Scholar 

  • Leyval, C., Joner, E. J., del Val, C., and Haselwandter, K. 2002. Potential of arbuscular mycorrhizal fungi for bioremediation. In: Mycorrhizal technology in agriculture, eds S. Gianinazzi, H. Schuepp, J. M. Barea, and K. Haselwandter. Basel: Birkhauser Verlag, pp. 175–186.

    Google Scholar 

  • Li, M. S., Luo, Y. P., and Su, Z. Y. 2007. Heavy metal concentrations in soils and plant accumulation in a restored manganese mineland in Guangxi, South China. Environ. Pollut. 147:68–175.

    Article  CAS  Google Scholar 

  • Liang, H. M., Lin, T. H., Chiou, J. M., and Yeh, K. C. 2009. Model evaluation of the phytoextraction potential of heavy metal hyperaccumulators and non-hyperaccumulators. Environ. Pollut. 157:1945–1952.

    Article  CAS  Google Scholar 

  • Lodewyckx, C., Taghavi, S., Mergeay, M., Vangronsveld, J., Clijsters, H., and Lelie, D. 2001. The effect of recombinant heavy metal-resistant endophytic bacteria on heavy metal uptake by their host plant. Int. J. Phytoremediation 3:173–187.

    Article  CAS  Google Scholar 

  • Magrisso, S., Erel, Y., and Belkin, S. 2008. Microbial reporters of metal bioavailability. Microb. Biotechnol. 1:320–330.

    Article  CAS  Google Scholar 

  • Malcova, R., Vosatka, M., and Gryndler, M. 2003. Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaris L. Appl. Soil Ecol. 23:55–67.

    Article  Google Scholar 

  • Martínez, M., Bernal, P., Almela, C., Velez, D., Garcia-Augustin, P., Serrano, R., and Navarro-Avino, J. 2006. An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere 64:478–485.

    Article  CAS  Google Scholar 

  • McGrath, S. P., Shen, Z. G., and Zhao, F. J. 1997. Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159.

    Article  CAS  Google Scholar 

  • McGrath, S. P., Zhao, J., and Lombi, E. 2002. Phytoremediation of metals, metalloids, and radionuclides. Adv. Agron. 75:1–56.

    Article  CAS  Google Scholar 

  • McLaren, R. 1998. Assessment of heavy metal contaminations of soils using sequential fractionations, 16ème Congrès mondial de Science du Sol, Montpellier, 20–26 août, No. 120.

    Google Scholar 

  • Medina, A., Vassileva, M., Barea, J. M., and Azcon, R. 2006. The growth-enhancement of clover by Aspergillus-treated sugar beet waste and Glomus mosseae inoculation in Zn contaminated soil. Appl. Soil Ecol. 33:87–98.

    Article  Google Scholar 

  • Melnitchouck, A., Leinweber, P., Eckhardt, K. U., and Beese, R. 2005. Qualitative differences between day- and night-time rhizodeposition in maize (Zea mays L.) as investigated by pyrolysis-field ionization mass spectrometry. Soil Biol. Biochem. 37:155–162.

    Article  CAS  Google Scholar 

  • Mench, M., Morel, J. L., and Guckert, A. 1987. Metal binding properties of high molecular weight soluble exudates from maize (Zea mays L.) roots. Biol. Fertil. Soils 3:165–169.

    Article  CAS  Google Scholar 

  • Miller, R. M. 1995. Biosurfactant-facilitated remediation of metal-contaminated soils. Environ. Health Perspect. 103:59–62.

    Article  CAS  Google Scholar 

  • Mirabello, S. 2006. Influence of siderophore producing bacteria and organic ligands on phase distribution of cadmium and its uptake by Brassica napus in the presence of goethite. MS thesis. New York: Cornell University.

    Google Scholar 

  • Mitsch, W. J. and Jørgensen, S. E. 2004. Ecological engineering and ecosystem restoration. New York: John Wiley & Sons.

    Google Scholar 

  • Mohan, S. V., Sirisha, K., Rao, R. S., and Sarma, P. N. 2007. Bioslurry phase remediation of chlorpyrifos contaminated soil: process evaluation and optimization by Taguchi design of experimental (DOE) methodology. Ecotoxicol. Environ. Saf. 68:252–262.

    Article  CAS  Google Scholar 

  • Moreno, D. A., Villora, G., Ruiz, J. M., and Romero, L. 2003. Growth conditions, elemental accumulation and induced physiological changes in Chinese cabbage. Chemosphere 52:1031–1040.

    CAS  Google Scholar 

  • Mrozik, A. and Piotrowska-Seget, Z. 2010. Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol. Res. 165:363–375.

    Google Scholar 

  • Mulligan, C. N., Yong, R. N., and Gibbs, B. F. 1999a. Removal of heavy metals from contaminated soil and sediments using the biosurfactant surfactin. J. Soil Contam. 8:231–254.

    Article  CAS  Google Scholar 

  • Mulligan, C. N., Yong, R. N., Gibbs, B. F., James, S., and Bennett, H. P. J. 1999b. Metal removal from contaminated soils and sediments by biosurfactants surfactin. Environ. Sci. Technol. 33:3812–3820.

    Article  CAS  Google Scholar 

  • Nacamulli, C., Bevivino, A., Dalmastri, C., Tabacchioni, S., and Chiarini, L. 1997. Perturbation of maize rhizosphere microflora following seed bacterization with Burkholderia cepacia MCI 7. FEMS Microbiol. Ecol. 23:183–193.

    Article  CAS  Google Scholar 

  • Ngiam, L. S. and Lim, P. E. 2000. Speciation patterns of heavy metals in tropical estuarine anoxic and oxidized sediments by different sequential extraction schemes. Sci. Total Environ. 275:53–61.

    Article  Google Scholar 

  • Odum, H. T. 1962. Ecological tools and their use. Man and the ecosystem. In: Conference of the suburban forest and ecology, eds P. E. Waggoner and J. D. Ovington, pp. 57–75.

    Google Scholar 

  • Pérez, A. L. and Anderson, K. M. 2009. DGT estimates cadmium accumulation in wheat and potato from phosphate fertilizer applications. Sci. Total Environ. 407:5096–5103.

    Article  CAS  Google Scholar 

  • Pilon-Smits, E. 2005. Phytoremediation. Annu. Rev. Plant Biol. 56:15–39.

    Article  CAS  Google Scholar 

  • Plangklang, P. and Reungsang, A. 2009. Bioaugmentation of carbofuran residues in soil using Burkholderia cepacia PCL3 adsorbed on agricultural residues. Int. Biodeterior. Biodegradation 63:515–522.

    Article  CAS  Google Scholar 

  • Pulford, I. D. and Watson, C. 2003. Phytoremediation of heavy metal-contaminated land by trees – a review. Environ. Int. 29:529–540.

    Article  CAS  Google Scholar 

  • Rai, U. N., Pandey, K., Sinha, S., Singh, A., Saxena, R., and Gupta, D. K. 2004. Revegetating fly ash landfills with Prosopis juliflora L.: impact of different amendments and Rhizobium inoculation. Environ. Int. 30:293–300.

    Article  CAS  Google Scholar 

  • Rajkumar, M., Ae, N., and Freitas, H. 2009. Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160.

    Article  CAS  Google Scholar 

  • Rao, R. S., Kumar, C. G., Prakasham, R. S., and Hobbs, P. J. 2008. The Taguchi methodology as a statistical tool for biotechnological applications: a critical appraisal. Biotechnol. J. 3:510–23.

    Article  CAS  Google Scholar 

  • Raskin, I., Kumar, P. B. A. N., Dushenkov, S., and Salt, D. E. 1994. Bioconcentration of heavy metals by plants. Curr. Opin. Biotechnol. 5:285–290.

    Article  CAS  Google Scholar 

  • Rasmussen, L. D., Sorensen, S. J., Turner, R. R., and Barkay, T. 2000. Application of a mer-lux biosensor for estimating bioavailable mercury in soil. Soil Biol. Biochem. 32:639–646.

    Article  CAS  Google Scholar 

  • Reeves, R. D. and Baker, A. J. M. 2000. Mechanisms of metal hyperaccumulation in plants. In: Phytoremediation of toxic metals: using plants to clean-up the environment, eds I. Raskin and B. D. Ensley. New York: John Wiley & Sons, pp. 193–229.

    Google Scholar 

  • Regvar, M., Vogel-Mikus, K., Kugonic, N., Turk, B., and Batic, F. 2006. Vegetational and mycorrhizal successions at a metal polluted site: indications for the direction of phytostabilisation? Environ. Pollut. 144:976–984.

    Article  CAS  Google Scholar 

  • Robinson, B. H., Banuelos, G., Conesa, H. M., Evangelou, M. W. H., and Schulin, R. 2009. The phytomanagement of trace elements in soil. Crit. Rev. Plant Sci. 28:240–266.

    Article  CAS  Google Scholar 

  • Rodrigues, J. L. M., Aiello, M. R., Urbance, J. W., Tsoi, T. V., and Tiedje, J. M. 2002. Use of both 16S rRNA and engineered functional genes with real-time PCR to quantify an engineered, PCB-degrading Rhodococcus in soil. J. Microbiol. Methods 51:181–189.

    Article  CAS  Google Scholar 

  • Salt, D. E. and Kramer, U. 2000. Mechanisms of metal hyperaccumulation in plants. In: Phytoremediation of toxic metals: using plants to clean-up the environment, eds I. Raskin and B. D. Ensley. New York: John Wiley & Sons, pp. 231–246.

    Google Scholar 

  • Sas-Nowosielska, A., Kucharski, R., Malkowski, E., Pogrzeba, M., Kuperberg, J. M., and Krynski, K. 2004. Phytoextraction crop disposal – an unsolved problem. Environ. Pollut. 128:373–379.

    Article  CAS  Google Scholar 

  • Sayer, J. A., Cotter-Howells, J. D., Watson, C., Hillier, S., and Gadd, G. M. 1999. Lead mineral transformation by fungi. Curr. Biol. 9:691–694.

    Article  CAS  Google Scholar 

  • Scheckel, K. G., Ryan, J. A., Allen, D., and Lescano, N. V. 2005. Determining speciation of Pb in phosphate-amended soils: method limitations. Sci. Total Environ. 350:261–272.

    Article  CAS  Google Scholar 

  • Semple, K. T., Doick, K. J., Burauel, P., Craven, A., Jones, K. C., and Harms, H. 2004. Defining bioavailability and bioaccessibility for the risk assessment and remediation of soils and sediment is complicated. Environ. Sci. Technol. 38:209A–212A.

    Article  Google Scholar 

  • Shann, J. R. 1995. The role of plants and plant/microbial systems in the reduction of exposure. Environ. Health Perspect. 103:13–15.

    Article  Google Scholar 

  • Sharma, A. and Johri, B. N. 2003a. Combat of iron-deprivation through a plant growth promoting fluorescent Pseudomonas strain GRP3A in mung bean (Vigna radiata L. Wilzeck). Microbiol. Res. 158:77–81.

    Article  CAS  Google Scholar 

  • Sharma, A. and Johri, B. N. 2003b. Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol. Res. 158:243–248.

    Article  CAS  Google Scholar 

  • Shen, Z. G., Li, X. D., Wang, C. C., Chen, H. M., and Chua, H. 2002. Lead phytoextraction from contaminated soil with high-biomass plant species. J. Environ. Qual. 31:1893–1900.

    Article  CAS  Google Scholar 

  • Sheng, X. F., Xia, J. J. Jiang, C. Y., He, L. Y., and Qian, M. 2008. Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ. Pollut. 156:1164–1170.

    Article  CAS  Google Scholar 

  • Shenker, M., Fan, T. W. M., and Crowley, D. E. 2001. phytosiderophores influence on cadmium mobilization and uptake by wheat and barley plants. J. Environ. Qual. 30:2091–2098.

    Article  CAS  Google Scholar 

  • Singer, A. C., van der Gast, C. J., and Thompson, I. P. 2005. Perspectives and vision for strain selection in bioaugmentation. Trends Biotechnol. 23:74–77.

    Article  CAS  Google Scholar 

  • Singh, O. V., Labana, S., Pandey, G., Budhiraja, R., and Jain, R. K. 2003. Phytoremediation: an overview of metallic ion decontamination from soil. Appl. Microbiol. Biotechnol. 61:405–412.

    CAS  Google Scholar 

  • Singh, B. K., Munro, S., Reid, E., Ord, B., Potts, J. M., Paterson, E., and Millard, P. 2006. Investigating microbial community structure in soils by physiological, biochemical and molecular fingerprinting methods. Eur. J. Soil Sci. 57:72–82.

    Article  CAS  Google Scholar 

  • Sirguey, C., Christophe, S., and Morel, J. L. 2006. Response of Thlaspi caerulescens to nitrogen, phosphorus and sulfur fertilisation. Int. J. Phytoremediation 8:149–161.

    Article  CAS  Google Scholar 

  • Siripattanakul, S., Wirojanagud, W., McEvoy, J. M., Casey, F. X. M., and Khan, E. 2009. A feasibility study of immobilized and free mixed culture bioaugmentation for treating atrazine in infiltrate. J. Hazard. Mater. 168:1373–1379.

    Article  CAS  Google Scholar 

  • Smith, J. A. C., Harper, F. A., Leighton, R. S., Thompson, I. P., Vaughan, D. J., and Baker, A. J. M. 1999. Comparative analysis of metal uptake, transport and sequestration in hyperaccumulator plants. In: Proc. 5th Intl. Conf. on the biogeochemistry of trace elements, Vienna, pp. 22–23.

    Google Scholar 

  • Srivastava, S., Srivastava, S., Prakash, S., and Srivastava, M. M. 1998. Fate of trivalent chromium in presence of organic acids: a hydroponic study on the tomato plant. Chem. Spec. Bioavail. 10:147–150.

    Article  CAS  Google Scholar 

  • Tack, F. M. G., Vossius, H. A. H., and Verloo, M. G. 1996. A comparison between sediment metal fractions, obtained from sequential extraction and estimated from single extractions. Int. J. Environ. Anal. Chem. 63:61–66.

    Article  CAS  Google Scholar 

  • Tani, K., Muneta, M., Nakamura, K., Shibuya, K., and Nasu, M. 2002. Monitoring of Ralstonia eutropha KT1 in groundwater in an experimental bioaugmentation field by in situ PCR. Appl. Environ. Microbiol. 68:412–416.

    Article  CAS  Google Scholar 

  • Thompson, I. P., van der Gast, C. J., Ciric, L., and Singer, A. C. 2005. Bioaugmentation for bioremediation: the challenge of strain selection. Environ. Microbiol. 7:909–915.

    Article  CAS  Google Scholar 

  • Tibazarwa, C., Corbisier, P., Mench, M., Bossus, A., Solda, A., Mergeay, M., Wyns, L., and van der Lelie, D. 2001. A microbial biosensor to predict bioavailable nickel in soil and its transfer to plants. Environ. Pollut. 113:19–26.

    Article  CAS  Google Scholar 

  • Toler, H. D., Morton, J. B., and Cumming, J. R. 2005. Growth and Metal Accumulation of mycorrhizal sorghum exposed to elevated copper and zinc. Water Air Soil Pollut. 164:155–172.

    Article  CAS  Google Scholar 

  • Unge, A., Tombolini, R., Molbak, L., and Jansson, J. K. 1999. Simultaneous monitoring of cell number and metabolic activity of specific bacterial populations with a dual gfp-luxAB marker system. Appl. Environ. Microbiol. 65:813–821.

    CAS  Google Scholar 

  • Valix, M., Usai, F., and Malik, R. 2001. Fungal bio-leaching of low grade laterite ores. Miner. Eng. 14:197–203.

    Article  CAS  Google Scholar 

  • Valls, M. and Lorenzo, V. 2002. Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol. Rev. 26:327–338.

    CAS  Google Scholar 

  • van Ranst, E., Verloo, M., Demeyer, A., and Pauwels, J. M. 1999. Manual for the soil chemistry and fertility laboratory. Gent: Faculty Agricultural and Applied Biological Sciences, Ghent University.

    Google Scholar 

  • van Veen, J. A., van Overbeek, L. S., and van Elsas, J. D. 1997. Fate and activity of microorganisms introduced into soil. Microbiol. Mol. Biol. Rev. 61:121–135.

    Google Scholar 

  • Vansuyt, G. R., Robin, A. S., Briat, J. F., Curie, C., and Lemanceau, P. 2007. Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol. Plant Microbe Interact. 20:441–447.

    Article  CAS  Google Scholar 

  • Verstraete, W., Wittelbolle, L., Heylen, K., Vanparys, B., de Vos, P., van de Wiele, T., and Boon, N. 2007. Microbial resource management: the road to go for environmental biotechnology. Eng. Life Sci. 7:117–126.

    Article  CAS  Google Scholar 

  • Visca, P., Colotti, G., Serino, L., Verzili, D., Orsi, N., and Chiancone, E. 1992. Metal regulation of siderophore synthesis in Pseudomonas aeruginosa and functional effects of siderophore–metal complexes. Appl. Environ. Microbiol. 58:2886–2893.

    CAS  Google Scholar 

  • Vivas, A., Voros, I., Biro, B., Campos, E., Barea, J. M., and Azcon, R. 2003. Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp. isolated from cadmium polluted soil under increasing cadmium levels. Environ. Pollut. 126:179–189.

    Article  CAS  Google Scholar 

  • Vivas, A., Biro, B., Ruiz-Lozano, J. M., Barea, J. M., and Azcon, R. 2006. Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62:1523–1533.

    Article  CAS  Google Scholar 

  • Vogel, T. M. and Walter, M. V. 2001. Bioaugmentation. In: Manual of environmental microbiology, eds. C. J. Hurst, R. L. Crawford, G. R. Knudsen, M. J. McInerney, and L. D. Stetzenbach. Washington: American Society for Microbiology Press, pp. 952–959.

    Google Scholar 

  • Wang, Y., Brown, H. N., Crowley, D. E., and Szaniszlo, P. J. 1993. Evidence for direct utilization of a siderophore, ferrioxamine B, in axenically grown cucumber. Plant Cell Environ. 16:579–585.

    Article  CAS  Google Scholar 

  • Wang, W. S., Shan, X. Q., Wen, B., and Zhang, S. Z. 2003. Relationship between the extractable metals from soils and metals taken up by maize roots and shoots. Chemosphere 53:523–530.

    Article  CAS  Google Scholar 

  • Wang, F. Y., Lin, X. G., and Yin, R. 2007. Inoculation with arbuscular mycorrhizal fungus Acaulospora mellea decreases Cu phytoextraction by maize from Cu-contaminated soil. Pedobiologia 51:99–109.

    Article  CAS  Google Scholar 

  • Wang, Y. P., Li, Q. B., Shi, J. Y., Lin, Q., Chen, X. C., Wu, W., and Chen, Y. X. 2008. Assessment of microbial activity and bacterial community composition in the rhizosphere of a copper accumulator and a non-accumulator. Soil Biol. Biochem. 40:1167–1177.

    Article  CAS  Google Scholar 

  • Wani, P. A., Khan, M. S., and Zaidi, A. 2007. Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45.

    Article  CAS  Google Scholar 

  • Wasay, S. A., Barrington, S. F., and Tokunaga, S. F. 1998. Using Aspergillus niger to bioremediate soils contaminated by heavy metals. Bioremediat. J. 2:183–190.

    CAS  Google Scholar 

  • Wei, S., Zhou, Q., and Koval, P. V. 2006. Flowering stage characteristics of cadmium hyperaccumulator Solanum nigrum L. and their significance to phytoremediation. Sci. Total Environ. 369:441–446.

    Article  CAS  Google Scholar 

  • Wenzel, W. W., Bunkowski, M., Puschenreiter, M., and Horak, O. 2003. Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ. Pollut. 123:131–138.

    Article  CAS  Google Scholar 

  • Whiting, S. N., de Souza, M. P., and Terry, N. 2001. Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ. Sci. Technol. 35:3144–3150.

    Article  CAS  Google Scholar 

  • Widada, J., Nojiri, H., and Omor, T. 2002. Recent developments in molecular techniques for identification and monitoring of xenobiotic-degrading bacteria and their catabolic genes in bioremediation. Appl. Microbiol. Biotechnol. 60:45–59.

    Article  CAS  Google Scholar 

  • Willaert, R. G. and Baron, G. V. 1996. Gel entrapment and micro-encapsulation: methods, applications and engineering principles. London: Freund Publishing House.

    Google Scholar 

  • Wu, C. H., Wood, T. K., Mulchandani, A., and Chen, W. 2006a. Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl. Environ. Microbiol. 72:1129–1134.

    Article  CAS  Google Scholar 

  • Wu, Q. T., Deng, J. C., Long, X. X., Morel, J. L., and Schwartz, C. 2006b. Selection of appropriate organic additives for enhancing Zn and Cd phytoextraction by hyperaccumulators. J. Environ. Sci. 18:1113–1118.

    Article  CAS  Google Scholar 

  • Yang, C. H. and Crowley, D. E. 2000. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl. Environ. Microbiol. 66:345–351.

    Article  CAS  Google Scholar 

  • Zaidi, S., Usmani, S., Singh, B. R., and Musarrat, J. 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997.

    Article  CAS  Google Scholar 

  • Zemberyova, M., Zwaik, A. A. H., and Farkasovska, I. 1998. Sequential extraction for the speciation of some heavy metals in soils. J. Radioanal. Nucl. Chem. 229:56–71.

    Article  Google Scholar 

  • Zenk, M. H. 1996. Heavy metal detoxification in higher plants – a review. Gene 179:21–30.

    Article  CAS  Google Scholar 

  • Zhang, H., Zhao, F. J., Sun, B., Davison, W., and McGrath, S. 2001. A new method to measure effective soil solution concentration predicts copper availability to plants. Environ. Sci. Technol. 35:2602–2607.

    Article  CAS  Google Scholar 

  • Zhao, F. J., Hamon, R. E., and McLaughlin, M. J. 2001. Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol. 151:613–620.

    Article  CAS  Google Scholar 

  • Zhu, Y. L., Pilon-Smits, E. A. H., Tarun, A. S., Weber, S. U., Jouanin, L., and Terry, N. 1999. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma-glutamylcysteine synthetase. Plant Physiol. 121:1169–1177.

    Article  CAS  Google Scholar 

  • Zhuang, X., Chen, J., Shim, H., and Bai, Z. 2007. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ. Int. 33:406–413.

    Article  Google Scholar 

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Authors and Affiliations

  1. IUT Colmar – Dpt Génie Biologique Equipe Dépollution Biologique des Sols, Plate-Forme Technologique AGROSYSTEMES, Université de Haute-Alsace, 28, rue de herrlisheim, BP 50568, 68 008, Colmar cedex, France

    Thierry Lebeau

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  1. Thierry Lebeau
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  2. Karine Jézéquel
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  3. Armelle Braud
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Correspondence to Thierry Lebeau .

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  1. Fac. Agricultural Sciences, Dept. Agricultural Microbiology, Aligarh Muslim University, Aligarh, 202002, India

    Iqbal Ahmad

  2. of Biomedical Sciences and Research, Department of Microbiology, Sardan Bhagwan Singh Post Graduate Insti, Dehradun, Uttaranchal, India

    Farah Ahmad

  3. , Natural Resources and Environmental Mana, Ball State University, Muncie, 47306, Indiana, USA

    John Pichtel

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Lebeau, T., Jézéquel, K., Braud, A. (2011). Bioaugmentation-Assisted Phytoextraction Applied to Metal-Contaminated Soils: State of the Art and Future Prospects. In: Ahmad, I., Ahmad, F., Pichtel, J. (eds) Microbes and Microbial Technology. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7931-5_10

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