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Effects of plant growth-promoting bacteria on EDTA-assisted phytostabilization of heavy metals in a contaminated calcareous soil

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Abstract

The objective of this research was to determine the combined effects of ethylenediaminetetraacetic acid (EDTA) and plant growth-promoting rhizobacteria (PGPR) on the phytostabilization of Cd, Pb, and Zn by corn and chemical fractionation of these elements in soil. Three heavy metal-resistant bacteria (P18, P15, and P19) were selected. All strains, belonging to the fluorescent pseudomonads, exhibited plant growth-promoting properties, including phosphorus solubilization and production of siderophore, indole acetic acid, and 1-aminocyclopropane-1-carboxylic acid deaminase. Applying EDTA individually or in combination with bacterial strains (P18 and P15) significantly increased shoot biomass. The highest dry shoot biomass was recorded in the combined treatment of EDTA and P15-inoculated pots. Application of EDTA in PGPR-inoculated pots increased concentrations of heavy metals in corn shoots and roots compared to the control. The highest concentration of Zn in corn root and shoot was observed in P15 + EDTA treatment, which were 2.0-fold and 1.3-fold higher than those in the untreated soil. Results of chemical speciation showed that the co-application of EDTA and fluorescent pseudomonads strains increased the bioavailability of Zn, Pb, and Cd by their redistribution from less soluble fractions to water-soluble forms. It was concluded that bacterial inoculation could improve the efficiency of EDTA in phytostabilization of heavy metals from multi-metal contaminated soils.

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References

  • Abbaszadeh-Dahaji, P., Saleh-Rastin, N., Asadi-Rahmani, H., Khavazi, K., Soltani, A., Shoary-Nejati, A. R., et al. (2018). Correction to: Plant growth-promoting activities of fluorescent pseudomonads, isolated from the Iranian soils. Acta Physiologiae Plantarum,40, 26.

    Google Scholar 

  • Agnello, A. C., Huguenot, D., van Hullebusch, E. D., & Esposito, G. (2016). Citric acid- and Tween® 80-assisted phytoremediation of a co-contaminated soil: Alfalfa (Medicago sativa L.) performance and remediation potential. Environmental Science and Pollution Research,23, 9215–9226.

    CAS  Google Scholar 

  • Akhgar, A. R., Arzanlou, M., Bakker, P. A. H. M., & Hamidpour, M. (2014). Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-containing Pseudomonas spp. in the Rhizosphere of salt-stressed canola. Pedosphere,24, 461–468.

    Google Scholar 

  • Amico, E. D., Cavalca, L., & Andreoni, V. (2005). Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiology Ecology,52, 153–162.

    Google Scholar 

  • Babu, A. G., Shim, J., Bang, K. S., Shea, P. J., & Oh, B. T. (2014). Trichoderma virens PDR-28: A heavy metal-tolerant and plant growth-promoting fungus for remediation and bioenergy crop production on mine tailing soil. Journal of Environmental Management,132, 129–134.

    CAS  Google Scholar 

  • Campbell, C. R., & Plank, C. O. (1998). Preparation of plant tissue for laboratory analysis. In Y. P. Kalra (Ed.), Handbook of reference methods for plant analysis (pp. 37–49). Boca Raton: CRC Press.

    Google Scholar 

  • Chander, K., & Joergensen, R. G. (2011). Soil microorganisms and the growth of Lupinus albus on a high metal soil in the presence of EDTA. Archives of Agronomy and Soil Science,57, 115–126.

    CAS  Google Scholar 

  • Chigbo, C., & Batty, L. (2015). Chelate-assisted phytoremediation of Cu-pyrene-contaminated soil using Z. mays. Water, Air, and Soil Pollution,226, 74.

    Google Scholar 

  • Cornu, J. Y., Dépernet, C., Garnier, C., Lenoble, V., Braud, A., & Lebeau, T. (2017). How do low doses of desferrioxamine B and EDTA affect the phytoextraction of metals in sunflower? Science of the Total Environment,592, 535–545.

    CAS  Google Scholar 

  • Estefan, G., Sommer, R., & Ryan, J. (2013). Methods of soil, plant and water analysis: A manual for the West Asia and North Africa Region. Beirut: ICARDA.

    Google Scholar 

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

    CAS  Google Scholar 

  • FOEFL (Swiss Federal Office of Environment, Forest and Landscape). (1987). Commentary on the ordinance relating to pollutants in soils (VSBo of June 9, 1986), Bern.

  • Guo, X., Zhao, G., Zhang, G., He, Q., Wei, Z., Zheng, W., et al. (2018). Effect of mixed chelators of EDTA, GLDA, and citric acid on bioavailability of residual heavy metals in soils and soil properties. Chemosphere,209, 776–782.

    CAS  Google Scholar 

  • Hadi, F., Bano, A., & Fuller, M. P. (2010). The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): The role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere,80, 457–462.

    CAS  Google Scholar 

  • Hamidpour, M., Akbari, L., & Shirani, H. (2017). Effects of co-application of zeolites and vermicompost on speciation and phytoavailability of cadmium, lead, and zinc in a contaminated soil. Communications in Soil Science and Plant Analysis,48, 262–273.

    CAS  Google Scholar 

  • Hamidpour, M., Karamooz, M., Akhgar, A., Tajabadipour, A., & Furrer, G. (2019). Adsorption of Cd and Zn onto micaceous minerals—Effect of siderophore desferrioxamine B. Pedosphere. 29, 590–597.

    Google Scholar 

  • Institute SAS. (1999). SAS/STAT user’s guide, version 8. SAS Institute.

  • Jamal, A., Delavar, M. A., Naderi, A., Nourieh, N., Medi, B., & Mahvi, A. H. (2019). Distribution and health risk assessment of heavy metalsin soil surrounding a lead and zinc smelting plant in Zanjan, Iran. Human and Ecological Risk Assessment: An International Journal,25, 1018–1033.

    CAS  Google Scholar 

  • Jiang, C., Sheng, X., Qian, M., & Wang, Q. (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.

    CAS  Google Scholar 

  • Jiang, W., & Liu, D. (2010). Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biology,10, 40.

    Google Scholar 

  • Jing, Y. X., Yan, J. L., He, H. D., Yang, D. J., Xiao, L., Zhong, T., et al. (2014). Characterization of bacteria in the rhizosphere soils of Polygonum Pubescens and their potential in promoting growth and Cd, Pb, Zn Uptake by Brassica napus. International Journal of Phytoremediation,16, 321–333.

    CAS  Google Scholar 

  • Jones, J. B., Jr. (2001). Laboratory guide for conducting soil tests and plant analysis. Boca Raton: CRC Press.

    Google Scholar 

  • Kabata-Pendias, A. (2011). Trace elements in soils and plants. Boca Raton: CRC Press.

    Google Scholar 

  • Khalid, S., Shahid, M., Niazi, N. K., Murtaza, B., Bibi, I., & Dumat, C. (2017). A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration,182, 247–268.

    CAS  Google Scholar 

  • Khan, I., Iqbal, M., Ashraf, M. Y., Ashraf, M. A., & Ali, S. (2016). Organic chelants-mediated enhanced lead (Pb) uptake and accumulation is associated with higher activity of enzymatic antioxidants in spinach (Spinacea oleracea L.). Journal of Hazardous Materials,317, 352–361.

    CAS  Google Scholar 

  • Lafuente, A. L., González, C., Quintana, J. R., Vázquez, A., & Romero, A. (2008). Mobility of heavy metals in poorly developed carbonate soils in the Mediterranean region. Geoderma,145, 238–244.

    CAS  Google Scholar 

  • Leleyter, L., Rousseau, C., Biree, L., & Baraud, F. (2012). Comparison of EDTA, HCl and sequential extraction procedures, for selected metals (Cu, Mn, Pb, Zn), in soils, riverine and marine sediments. Journal of Geochemical Exploration,116–117, 51–59.

    Google Scholar 

  • Li, W. C., & Wong, M. H. (2010). Effects of bacteria on metal bioavailability, speciation, and mobility in different metal mine soils: A column study. Journal of Soils and Sediments,10, 313–325.

    Google Scholar 

  • López, M. L., Peralta-Videa, J. R., Benitez, T., & Gardea-Torresdey, J. L. (2005). Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere,61, 595–598.

    Google Scholar 

  • Luo, C., Wang, S., Wang, Y., Yang, R., Zhang, G., & Shen, Z. (2015). Effects of EDDS and plant-growth-promoting bacteria on plant uptake of trace metals and PCBs from e-waste-contaminated soil. Journal of Hazardous Materials,286, 379–385.

    CAS  Google Scholar 

  • Ma, Y., Prasad, M. N. V., Rajkumar, M., & Freitas, H. (2011). Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances,29, 248–258.

    CAS  Google Scholar 

  • Mingorance, M. D., Leidi, E. O., Valdés, B., & Oliva, S. R. (2012). Evaluation of lead toxicity in Erica andevalensis as an alternative species for revegetation of contaminated soils. International Journal of Phytoremediation,14, 174–185.

    Google Scholar 

  • Mousavi, S. M., Motesharezadeh, B., Hosseini, H. M., Alikhani, H., & Zolfaghari, A. A. (2018). Geochemical fractions and phytoavailability of Zinc in a contaminated calcareous soil affected by biotic and abiotic amendments. Environmental Geochemistry and Health,40, 1221–1235.

    CAS  Google Scholar 

  • Nowack, B., Schulin, R., & Robinson, B. H. (2006). Critical assessment of chelant-enhanced metal phytoextraction. Environmental Science and Technology,40, 5225–5232.

    CAS  Google Scholar 

  • Parizanganeh, A., Hajisoltani, P., & Zamani, A. (2010). Concentration, distribution and comparison oftotal and bioavailable metals in top soils and plants accumulation in zanjan zinc industrial Town-Iran. Procedia Environmental Sciences,2, 167–174.

    Google Scholar 

  • Patten, C., & Glick, B. (2002). Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Applied Environmental Microbiology,68, 3795–3801.

    CAS  Google Scholar 

  • Płociniczak, T., Kukla, M., Watroba, R., & Piotrowska-Seget, Z. (2013). The effect of soil bioaugmentation with strains of Pseudomonas on Cd, Zn and Cu uptake by Sinapis alba L. Chemosphere,91, 1332–1337.

    Google Scholar 

  • Pourrut, B., Shahid, M., Dumat, C., Winterton, P., & Pinelli, E. (2011). Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology,213, 113–136.

    CAS  Google Scholar 

  • Rafiq, M., Shahid, M., Abbas, G., Shamshad, S., Khalid, S., Niazi, N. K., et al. (2017). Comparative effect of calcium and EDTA on arsenic uptake and physiological attributes of Pisum sativum. International Journal of Phytoremediation,19, 662–669.

    CAS  Google Scholar 

  • Rizwan, M., Ali, S., Qayyum, M. F., Ok, Y. S., Zia-ur-Rehman, M., Abbas, Z., et al. (2017). Use of maize (Zea mays L.) for phytomanagement of Cd-contaminated soils: A critical review. Environmental Geochemistry and Health,39, 259–277.

    CAS  Google Scholar 

  • Rosas-Castor, J. M., Portugal, L., Ferrer, L., Guzmán-Mar, J. L., Hernández-Ramírez, A., Cerdà, V., et al. (2015). Arsenic fractionation in agricultural soil using an automated three-step sequential extraction method coupled to hydride generation-atomic fluorescence spectrometry. Analytica Chimica Acta,874, 1–10.

    CAS  Google Scholar 

  • Saifullah, E. M., Qadir, M., de Caritat, P., Tack, F. M. G., Du Laing, G., & Zia, M. H. (2009). EDTA-assisted Pb phytoextraction. Chemosphere,74, 1279–1291.

    CAS  Google Scholar 

  • Salbu, B., Krekling, T., & Oughton, D. H. (1998). Characterisation of radioactive particles in the environment. The Analyst,123, 843–850.

    CAS  Google Scholar 

  • Sarwar, N., Imran, M., Shaheen, M. R., Ishaque, W., Kamran, M. A., Matloob, A., et al. (2017). Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere,171, 710–721.

    CAS  Google Scholar 

  • Shafigh, M., Ghasemi-Fasaei, R., & Ronaghi, A. (2016). Influence of plant growth regulators and humic acid on the phytoremediation of lead by maize in a Pb-polluted calcareous soil. Archives of Agronomy and Soil Science,62, 1733–1740.

    CAS  Google Scholar 

  • Shahid, M., Austruy, A., Echevarria, G., Arshad, M., Sanaullah, M., Aslam, M., et al. (2014). EDTA-enhanced phytoremediation of heavy metals: A review. Soil and Sediment Contamination,23, 389–416.

    CAS  Google Scholar 

  • Shahid, M., Dumat, C., Aslama, M., & Pinelli, E. (2012). Assessment of lead speciation by organic ligands using speciation models. Chemical Speciation and Bioavailability,24, 248–252.

    CAS  Google Scholar 

  • Soleimani, M., Hajabbasi, M. A., Afyuni, M., Akbar, S., Jensen, J. K., Holm, P. E., et al. (2010). Comparison of natural humic substances and synthetic ethylenediaminetetraacetic acid and nitrilotriacetic acid as washing agents of a heavy metal–polluted soil. Journal of Environment Quality,39, 855.

    CAS  Google Scholar 

  • Sparks, D. L. (2003). Environmental soil chemistry. Boston: Academic Press.

    Google Scholar 

  • Tessier, A., Campbell, P. G. C., & Bisson, M. (1979). Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry,51, 844–851.

    CAS  Google Scholar 

  • Usman, A. R. A., & Mohamed, H. M. (2009). Effect of microbial inoculation and EDTA on the uptake and translocation of heavy metal by corn and sunflower. Chemosphere,76, 893–899.

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Soil Science, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran

    Mohsen Hamidpour, Hamideh Nemati & Payman Abbaszadeh Dahaji

  2. Department of Horticulture Science, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran

    Hamid Reza Roosta

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  1. Mohsen Hamidpour
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  2. Hamideh Nemati
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Correspondence to Mohsen Hamidpour.

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Hamidpour, M., Nemati, H., Abbaszadeh Dahaji, P. et al. Effects of plant growth-promoting bacteria on EDTA-assisted phytostabilization of heavy metals in a contaminated calcareous soil. Environ Geochem Health 42, 2535–2545 (2020). https://doi.org/10.1007/s10653-019-00422-3

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