Abstract
For remediating polluted soils, phytoextraction of metals received considerable attention in recent years, although slow removal of metals remained a major constraint in this approach. We, therefore, studied the effect of selected organic and inorganic amendments on the solubility of zinc (Zn), cadmium (Cd), and lead (Pb) in polluted soil and enhancing the efficacy of phytoextraction of these metals by Indian mustard (Brassica juncea cv. Pusa Vijay). For this purpose, a greenhouse experiment was conducted using a metal-polluted soil to evaluate the effect of amendments, viz. green manure (T2), EDTA (T3), sulfur (S)+S oxidizing bacteria (Thiobacillus spp.) (T4), metal-solubilizing bacteria (Pseudomonas spp.) (T5), and green manure + metal-solubilizing bacteria (T6), on solubility and bioavailability of Zn, Cd, and Pb. Distribution of metals in different soil fractions revealed that Cd content in water soluble + exchangeable fraction increased to the extent of 34.1, 523, 133, 123, and 75.8% in T2, T3, T4, T5, and T6 treatments, respectively, over control (T1). Cadmium concentrations in soil solution as extracted by Rhizon sampler were recorded as 3.78, 88.1, 11.2, 6.29, and 4.27 μg L−1in T2, T3, T4, T5, and T6, respectively, whereas soil solution concentration of Cd in T1 was 0.99 μg L−1. Activities of Cd (pCd2+) in Baker soil extract were 12.2, 10.9, 6.72, 7.74, 7.67, and 7.05 for T1, T2, T3, T4, T5, and T6, respectively. Cadmium contents in shoot were recorded as 2.74, 3.12, 4.03, 4.55, 4.68, and 4.63 mg kg−1 in T1, T2, T3, T4, T5, and T6 treatments, respectively. Similar trend in Zn and Pb content with different magnitude was also observed across the different amendments. Cadmium uptake by shoot of mustard was enhanced to the extent of 125, 62.5, 175, 175, and 212% grown on T2-, T3-, T4-, T5-, and T6-treated soil, respectively, over T1. By and large, free ion activity of metals as measured by Baker soil test proved to be the most effective index for predicting Zn, Cd, and Pb content in shoot of mustard, followed by EDTA and DTPA. Among the metal fractions, only water soluble + exchangeable metal contributed positively towards plant uptake, which explained the variation in shoot Zn, Cd, and Pb content to the extent of 74, 81, and 87%, respectively, along with other soil metal fractions. Risk to human health for intake of metals through the consumption of leafy vegetable (mustard) grown on polluted soil in terms of hazard quotient (HQ) ranged from 0.64 to 1.10 for Cd and 0.11 to 0.34 for Pb, thus rendering mustard unfit for the human consumption. Novelty of the study mainly consisted of the use of natural means and microorganisms for enhancing solubility of metals in soil with the ultimate aim of hastening the phytoremediation.
Similar content being viewed by others
References
Abhilash PC, Powell JR, Singh HB, Singh BK (2012) Plant-microbe interactions: novel applications for exploitation in multipurpose remediation technologies. Trends Biotechnol 30:416–420
Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. South Afr J Bot 108:393–406
Baker DE, Amacher MC (1981) The development and interpretation of a diagnostic soil-testing program. Pennsylvania Agric Exp Sta Bull 826. University Park PA 20 page
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyper accumulate metal elements: a review of their distribution, ecology and phytochemistry. Biorecov 1:181–186
Bareen FE, Tahira SA (2010) Efficiency of seven different cultivated plant species for phytoextraction of toxic metals from tannery effluent contaminated soil using EDTA. Soil Sediment Contam 19:160–173
Barman M, Datta SP, Rattan RK (2014) Identification of the solid phase in relation to the solubility of nickel in alluvial soils. J Environ Biol 35:901–906
Barman M, Datta SP, Rattan RK, Meena MC (2015) Chemical fractions and bioavailability of nickel in alluvial soils. Plant Soil Environ 61:17–22
Bernal MP, Mcgrath SP, Miller AJ, Baker AJM (1994) Comparison of the chemical changes in the rhizosphere of the nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus. Plant Soil 164:251–259
Blaylock MJ (2000) Field demonstrations of phytoremediation of Pb contaminated soils. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, pp 1–12
Blaylock MJ, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Salt DE, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865
Bouyoucos GJ (1962) Hydrometer method improved for making particle size analysis of soils. Agron 54:464–465
Bower CA, Reitemeier RF, Fireman M (1952) Exchangeable cation analysis of saline and alkali soils. Soil Sci 73:251–262
Brennan D, Coulter B, Mullen G, Courtney R (2008) Evaluation of Mehlich 3 for extraction of copper and zinc from Irish grassland soils and for prediction of herbage content. Commun Soil Sci Plant Anal 39:1943–1962
Chauhan JS, Rai JPN (2009) Phytoextraction of soil cadmium and zinc by microbes inoculated Indian mustard (Brassica juncea). J Plant Interact 4:279–287
Chen Y, Li XD, Shen ZG (2004) Leaching and uptake of heavy metals by ten different species of plants during an EDTA-assisted phytoextraction process. Chemosphere 57:187–196
Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390
Cui Y, Dong Y, Li H, Wang Q (2004) Effect of elemental sulphur on solubility of soil heavy metals and their uptake by maize. Environ Int 30:323–328
Datta SP, Young SD (2005) Predicting metal uptake and risk to the human food chain from leaf vegetables grown on soils amended by long-term application of sewage sludge. Water Air Soil Pollut 163:119–136
Datta SP, Meena BL, Rattan RK (2013) Development of a computer program for calculating metal ion activity using Baker soil test. J Indian Soc Soil Sci 61:47–50
Datta SP, Golui D, Sanyal SK (2017) Assessing potential threats of soil pollutant elements in relation to food-chain contamination with suggested remedial measures. In: Souvenir of 82nd Annual Convention and National Seminar of Indian Society of Soil Science, New Delhi at Amity University Kolkata, New Town, Kolkata, West Bengal 11-14 December 2017 pp 137–150
do Nascimento CWA, Xing B (2006) Phytoextraction: a review on enhanced metal availability and plant accumulation. Sci Agric 63:299–311
Do Nascimento CWA, Amarasiriwardena D, Xing B (2006) Comparison of natural organic acids and synthetic chelates at enhancing phytoextraction of metals from a multi-metal contaminated soil. Environ Pollut 140:114–123
Evangelou MWH, Ebel M, Schaeffer A (2006) Evaluation of the effect of small organic acids on phytoextraction of Cu and Pb from soil with tobacco Nicotianatabacum. Chemosphere 63:996–1004
Gandois L, Probst A, Dumat C (2010) Modeling trace metal extractability and solubility in French forest soils by using soil properties. Eur J Soil Sci 61:271–286
Golui D (2018) Assessing bioavailbility of metals in contaminated soils. Thesis, ICAR-Indian Agricultural Research Institute
Golui D, Datta SP, Rattan RK, Dwivedi BS, Meena MC (2014) Predicting bioavailability of metals from sludge amended soils. Environ Monit Assess 186:8541–8553
Golui D, Guha Mazumder DN, Sanyal SK, Datta SP, Ray P, Patra PK, Sarkar S, Bhattacharya K (2017) Safe limit of arsenic in soil in relation to dietary exposure of arsenicosis patients from Malda district, West Bengal- a case study. Ecotoxicol Environ Saf 144:227–235
Goswamia S, Das S (2015) A study on cadmium phytoremediation potential of Indian mustard, Brassica juncea. Int J Phytoremediation 17:583–588
Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. II: local root exudation of organic acids as a response to P starvation. Plant Soil 113:61–165
IRIS (2019) Integrated risk information system-database. US Environmental Protection Agency
Iwasaki K, Yoshikawa G (1990) Fractionation of copper and zinc in greenhouse soils. Trans. 14th International Congress on Soil Science 11:363–364
Jackson ML (1973) Soil chemical analysis. Prentice Hall of India Private Limited, New Delhi
Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1783
Kos B, Greman H, Lestan D (2003) Phytoextraction of lead, zinc and cadmium from soil by selected plants. Plant Soil Environ 49:548–553
Lindsay WL (1979) Chemical equilibrium in soils. Wiley, New York
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428
Liphadzi MS, Kirkham MB (2006) Chelate-assisted heavy metal removal by sunflower to improve soil with sludge. J Crop Improv 16:153–172
McLaren RG, Crawford DV (1973) Studies on soil copper I. The fractionation of copper in soils. J Soil Sci 24:172–181
Meena R, Datta SP, Golui D, Dwivedi BS, Meena MC (2016) Long term impact of sewage irrigation on soil properties and assessing risk in relation to transfer of metals to human food chain. Environ Sci Pollut Res 23:14269–14283
Meers E, Lesage E, Lamsal S, Hopgood M, Vervaeke P, Tack FMG, Verloo MG (2005) Enhanced phytoextraction. I. Effect of EDTA and citric acid on heavy metal mobility in a calcareous soil. Int J Phytoremediation 7:129–142
Miller WP, Martens DC, Zelazny LW, Kornegay ET (1986) Forms of solid phase copper in copper-enriched swine manure. J Environ Qual 15:69–72
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture Circular No. 939. Banderis A D, Barter DH, Anderson K. Agricultural and Advisor
Phillips I, Chappie L (1995) Assessment of a heavy metals-contaminated site using sequential extraction, TCLP, and risk assessment techniques. Soil Sediment Contam 4:311–325
Purakayastha TJ, Viswanath T, Bhadraray S, Chhonkar PK, Adhikari PP, Suribabu K (2008) Phytoextraction of zinc, copper, nickel and lead from a contaminated soil by different species of Brassica. Int J Phytoremediation 10:61–72
Quartacci MF, Baker AJM, Navari-Izzo F (2005) Nitriloacetate-and citric acid assisted phytoextraction of cadmium by Indian mustard (Brassica juncea (L.) Czernj, Brassicaceae). Chemosphere 59:1249–1255
Quevauviller PH (1998) Operationally defined extraction procedures for soil and sediment analysis. Trends Anal Chem 17:289–298
Rang Zan N, Datta SP, Rattan RK, Dwivedi BS, Meena MC (2013) Prediction of the solubility of zinc, copper, nickel, cadmium, and lead in metal contaminated soils. Environ Monit Assess 185:10015–10025
Rattan RK, Datta SP, Chhonkar PK, Suribabu K, Singh AK (2005) Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater– a case study. Agric Ecosyst Environ 109:310–322
Rattan RK, Datta SP, Sanyal SK (2009) Pollutants elements and human health. In: Soil quality for human health (Narayanasamy G, Rattan RK, Ganeshamurthy AN Eds.) Bull Ind Soc Soil Sci 27:103–123
Ray P, Datta SP (2016) Solid phase speciation of Zn and Cd in zinc smelter effluent-irrigated soils. Chem Speciat Bioavailab 29:6–14
Ray P, Singhal SK, Datta SP, Rattan RK (2013) Evaluation of suitability of chemical extractants for assessing available zinc in acid and alkaline soils amended with farmyard manure and sludge. Agrochimica 4:348–362
Rieuwerts JS, Thornton I, Farago ME, Ashmore MR (1998) Factors influencing metal bioavailability in soils: preliminary investigation for the development of a critical loads approach for metals. Chem Speciat Bioavailab 10:61–75
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668
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 60:182–194
Shi P, Zhu K, Zhang Y, Chai T (2016) Growth and cadmium accumulation of Solanum nigrum L. seedling were enhanced by heavy metal-tolerant strains of Pseudomonas aeruginosa. Water Air Soil Pollut 227:459
Sinegani AAS, Khalilikhah F (2010) Effects of EDTA, sheep manure extract, and their application time on Cd uptake by Helianthus annuus from a calcareous mine soil. Soil Sediment Contam 19:378–390
Singh S, Zacharias M, Kalpana S, Mishra S (2012) Heavy metals accumulation and distribution pattern in different vegetable crops. J Environ Chem Ecotoxicol 4:75–81
Snedecor GW, Cochran WG (1967) Statistical Methods, 7th edn. The Lowa State University. Press America, Iowa
Subbiah BV, Asija GL (1956) A rapid procedure for the estimation of available nitrogen in soils. Curr Sci 25:259–260
Tandy S, Schulin R, Nowack B (2006) Uptake of metals during chelant-assisted phytoextraction with EDDS related to the solubilized metal concentration. Environ Sci Technol 40:2753–2758
Tessier A, Campbell PG, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851
Tye AM, Young SD, Crout NMJ, Zhang H, Preston S, Barbosa-Jefferson VL, Davison W, Mcgrath SP, Paton GI, Kilham K, Resende L (2003) Predicting the activity of Cd2+ and Zn2+ in soil pore water from the radio-labile metal fraction. Geochim Cosmochim Acta 67:375–385
USEPA (1991) US Environmental Protection Agency. Annual reports FY 1990. USEPA report540/8-91/067. USEPA, Washington DC
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
Whiting SN, De Souza MP, Terry N (2001) Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ Sci Technol 35:3144–3150
Wuana RA, Mbasugh PA (2013) Response of roselle (Hibiscus sabdariffa) to heavy metals contamination in soils with different organic fertilizations. J Chem Ecol 29:437–447
Funding
This study received financial support in the form of Junior Research Fellowship (JRF) from the Indian Council of Agricultural Research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 13 kb)
Rights and permissions
About this article
Cite this article
Mishra, R., Datta, S.P., Annapurna, K. et al. Enhancing the effectiveness of zinc, cadmium, and lead phytoextraction in polluted soils by using amendments and microorganisms. Environ Sci Pollut Res 26, 17224–17235 (2019). https://doi.org/10.1007/s11356-019-05143-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05143-9