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In situ and ex situ bioremediation of seleniferous soils from northwestern India

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
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Abstract

Purpose

Selenium (Se) toxicity or deficiency disorders are chiefly associated with Se concentration and speciation in soils. Elevated soil Se content may lead to contamination of water bodies and groundwaters due to the leaching caused by rainfall and irrigation. This study is focused on Se removal by in situ (biostimulation and bioaugmentation) and ex situ (soil washing) bioremediation as well as on its recovery.

Materials and methods

In this research, in situ bioremediation of Se-rich soil collected from rice fields in Ludhiana, Northwest India was studied in microcosms. The effect of biostimulation was determined by amending soil with different organic sources (fermentable, non-fermentable, and non-hydrolysable electron donors). The effect of bioaugmentation was determined by adding anaerobic granular sludge to the microcosms. With regard to ex situ bioremediation, the Se-rich soil was leached with water and the resulting leachate was biologically treated in an upflow anaerobic sludge blanket (UASB) reactor using lactate as electron donor. The UASB reactor was operated for 78 days in different conditions of lactate (electron donor) dosing to achieve maximum Se removal and recovery as elemental Se(0) on the granular sludge. The effluent of the UASB reactor was regularly analyzed to determine Se removal efficiencies.

Results and discussion

The effect of biostimulation and bioaugmentation showed no significant difference in terms of Se reduction profiles in the microcosms. This suggested that the indigenous Se-reducing microorganisms and oxidizable organic carbon present in the soil are sufficient for in situ soil bioremediation. During treatment of soil leachate in the UASB reactor, 90% Se removal was achieved irrespective of the lactate dosing and mineral salt medium composition of the reactor influent. Analysis of the granular sludge using scanning electron microscopy coupled with energy dispersive X-ray spectroscopy (SEM-EDS) and powder X-ray diffraction (P-XRD) confirmed the presence of elemental Se on the granular sludge. The total Se concentration in the anaerobic granular sludge amounted to 43.5 (± 0.7) μg Se per gram of granular sludge.

Conclusions

In situ bioremediation achieved Se reduction in the Se-rich soil investigated. However, risk of Se re-oxidation and leaching into groundwater after in situ remediation cannot be disregarded. In contrast, during ex situ treatment, effluent from the UASB reactor contained less than the USEPA guideline value 5 μg L−1 Se. This study showed biological treatment of Se-rich soils is suitable for cleaning the soil, Se recovery, and environmentally acceptable effluent discharge of the soil washing leachate treatment.

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References

  • APHA/AWWA/WEF (2012) Standard methods for the examination of water and wastewater, 22nd edn. Standard Methods. American Public Health Association, American Water Works Association, Water Environment Federation, Washington

    Google Scholar 

  • Ashworth DJ, Shaw G (2006) Soil migration, plant uptake and volatilisation of radio-selenium from a contaminated water table. Sci Total Environ 370(2–3):506–514

    Article  CAS  Google Scholar 

  • Basuvaraj M, Fein J, Liss SN (2015) Protein and polysaccharide content of tightly and loosely bound extracellular polymeric substances and the development of a granular activated sludge floc. Water Res 82:104–117

    Article  CAS  Google Scholar 

  • Cassidy J, Frunzo L, Lubberding HJ, Villa-Gomez DK, Esposito G, Keesman KJ, Lens PNL (2017) Role of microbial accumulation in biological sulphate reduction using lactate as electron donor in an inversed fluidized bed bioreactor: operation and dynamic mathematical modelling. Int Biodeterior Biodegrad 121:1–10

    Article  CAS  Google Scholar 

  • Cennamo P, Montuori N, Trojsi G, Fatigati G, Moretti A (2016) Biofilms in churches built in grottoes. Sci Total Environ 543:727–738

    Article  CAS  Google Scholar 

  • Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation—emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37(24):5701–5710

    Article  CAS  Google Scholar 

  • De La Riva DG, Vindiola BG, Castañeda TN, Parker DR, Trumble JT (2014) Impact of selenium on mortality, bioaccumulation and feeding deterrence in the invasive argentine ant, Linepithema humile (Hymenoptera: Formicidae). Sci Total Environ 481:446–452

    Article  CAS  Google Scholar 

  • Dermont G, Bergeron M, Mercier G, Richer-Laflèche M (2008) Soil washing for metal removal: a review of physical/chemical technologies and field applications. J Hazard Mater 152(1):1–31

    Article  CAS  Google Scholar 

  • Dhillon SK, Dhillon KS, Kohli A, Khera KL (2008) Evaluation of leaching and runoff losses of selenium from seleniferous soils through simulated rainfall. J Plant Nutr Soil Sci 171(2):187–192

    Article  CAS  Google Scholar 

  • Dhillon KS, Dhillon SK, Dogra R (2010) Selenium accumulation by forage and grain crops and volatilization from seleniferous soils amended with different organic materials. Chemosphere 78(5):548–556

    Article  CAS  Google Scholar 

  • El-Ramady H, Abdalla N, Alshaal T, Domokos-Szabolcsy É, Elhawat N, Prokisch J, Sztrik A, Fári M, El-Marsafawy S, Shams MS (2015) Selenium in soils under climate change, implication for human health. Environ Chem Lett 13(1):1–19

    Article  CAS  Google Scholar 

  • Emenike CU, Liew W, Fahmi MG, Jalil KN, Pariathamby A, Hamid FS (2017) Optimal removal of heavy metals from leachate contaminated soil using bioaugmentation process. Clean-Soil, Air, Water 45(2):1500802

    Article  CAS  Google Scholar 

  • Fabbricino M, Ferraro A, Luongo V, Pontoni L, Race M (2018) Soil washing optimization, recycling of the solution, and ecotoxicity assessment for the remediation of Pb-contaminated sites using EDDS. Sustainability 10(3):636

    Article  CAS  Google Scholar 

  • Fellowes JW, Pattrick RAD, Boothman C, Al Lawati WMM, van Dongen BE, Charnock JM, Lloyd JR, Pearce CI (2013) Microbial selenium transformations in seleniferous soils. Eur J Soil Sci 64(5):629–638

    Article  CAS  Google Scholar 

  • Ferraro A, Fabbricino M, van Hullebusch ED, Esposito G (2017) Investigation of different ethylenediamine-N,N′-disuccinic acid-enhanced washing configurations for remediation of a cu-contaminated soil: process kinetics and efficiency comparison between single-stage and multi-stage configurations. Environ Sci Pollut Res 24(27):21960–21972

    Article  CAS  Google Scholar 

  • Flury M, Frankenberger WT Jr, Jury WA (1997) Long-term depletion of selenium from Kesterson dewatered sediments. Sci Total Environ 198:259–270

    Article  Google Scholar 

  • Frankenberger WT Jr, Amrhein C, Fan TWM, Flaschi D, Glater J, Kartinen E Jr, Kovac K, Lee E, Ohlendorf HM, Owens L, Terry N, Toto A (2004) Advanced treatment technologies in the remediation of seleniferous drainage waters and sediments. Irrig Drain Syst 18(1):19–42

    Article  Google Scholar 

  • Fujita M, Ike M, Nishimoto S, Takahashi K, Kashiwa M (1997) Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1. J Ferment Bioeng 83(6):517–522

    Article  CAS  Google Scholar 

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11(3):271–279

    Article  CAS  Google Scholar 

  • Hagarova I, Zemberyova M, Bajcan D (2003) Sequential and single step extraction procedures for fractionation of selenium in soil samples. Chem Pap 59(2):93–98

    Google Scholar 

  • Huguenot D, Mousset E, van Hullebusch ED, Oturan MA (2015) Combination of surfactant enhanced soil washing and electro-Fenton process for the treatment of soils contaminated by petroleum hydrocarbons. J Environ Manag 153:40–47

    Article  CAS  Google Scholar 

  • Hunter WJ (2014) A Rhizobium selenitireducens protein showing selenite reductase activity. Curr Microbiol 68(3):311–316

    Article  CAS  Google Scholar 

  • Isoyama M, Wada SI (2007) Remediation of Pb-contaminated soils by washing with hydrochloric acid and subsequent immobilization with calcite and allophanic soil. J Hazard Mater 143(3):636–642

    Article  CAS  Google Scholar 

  • Jain R, Jordan N, Weiss S, Foerstendorf H, Heim K, Kacker R, Hubner R, Kramer H, Van Hullebusch ED, Farges F, Lens PNL (2015) Extracellular polymeric substances govern the surface charge of biogenic elemental selenium nanoparticles. Environ Sci Technol 49(3):1713–1720

    Article  CAS  Google Scholar 

  • Jang M, Jung SH, Sang IC, Jae KP (2005) Remediation of arsenic-contaminated soils and washing effluents. Chemosphere 60(3):344–354

    Article  CAS  Google Scholar 

  • Kabata-pendias A, Pendias H (2001) Trace elements in soils and plants trace elements in soils and plants, 3rd edn. CRC press LLC, Boca Raton

    Google Scholar 

  • Lenz M, Lens PNL (2009) The essential toxin: the changing perception of selenium in environmental sciences. Sci Total Environ 407(12):3620–3633

    Article  CAS  Google Scholar 

  • Lenz M, van Hullebusch ED, Hommes G, Corvini PFX, Lens PNL (2008) Selenate removal in methanogenic and sulfate-reducing upflow anaerobic sludge bed reactors. Water Res 42(8–9):2184–2194

    Article  CAS  Google Scholar 

  • Lindblom SD, Fakra SC, Landon J, Schulz P, Tracy B, Pilon-Smits EAH (2014) Inoculation of selenium hyperaccumulator Stanleya pinnata and related non-accumulator Stanleya elata with hyperaccumulator rhizosphere fungi—investigation of effects on Se accumulation and speciation. Physiol Plant 150(1):107–118

    Article  CAS  Google Scholar 

  • Luo Q, Tsukamoto TK, Zamzow KL, Miller GC (2008) Arsenic, selenium, and sulfate removal using an ethanol-enhanced sulfate-reducing bioreactor. Mine Water Environ 27(2):100–108

    Article  CAS  Google Scholar 

  • Luongo V, Ghimire A, Frunzo L, Fabbricino M, d’Antonio G, Pirozzi F, Esposito G (2017) Photofermentative production of hydrogen and poly-β-hydroxybutyrate from dark fermentation products. Bioresour Technol 228:171–175

    Article  CAS  Google Scholar 

  • Makino T, Maejima Y, Akahane I, Kamiya T, Takano H, Fujitomi S, Ibaraki T, Kunhikrishnan A, Bolan N (2016) A practical soil washing method for use in a Cd-contaminated paddy field, with simple on-site wastewater treatment. Geoderma 270:3–9

    Article  CAS  Google Scholar 

  • Mal J, Nancharaiah YV, van Hullebusch ED, Lens PNL (2016) Effect of heavy metal co-contaminants on selenite bioreduction by anaerobic granular sludge. Bioresour Technol 206:1–8

    Article  CAS  Google Scholar 

  • Mal J, Nancharaiah YV, Bera S, Maheshwari N, van Hullebusch ED, Lens PNL (2017a) Biosynthesis of CdSe nanoparticles by anaerobic granular sludge. Environ Sci Nano 4:824–833

    Article  CAS  Google Scholar 

  • Mal J, Nancharaiah YV, Maheshwari N, van Hullebusch ED, Lens PNL (2017b) Continuous removal and recovery of tellurium in an upflow anaerobic granular sludge bed reactor. J Hazard Mater 327:79–88

    Article  CAS  Google Scholar 

  • Misra S, Boylan M, Selvam A, Spallholz J, Björnstedt M (2015) Redox-active selenium compounds - from toxicity and cell death to cancer treatment. Nutrients 7(5):3536–3556

    Article  CAS  Google Scholar 

  • Moreno RG, Burdock R, Cruz M, Álvarez D, Crawford JW (2013) Managing the selenium content in soils in semiarid environments through the recycling of organic matter. Appl Environ Soil Sci 2013:283468

    Google Scholar 

  • Mousset E, Huguenot D, van Hullebusch ED, Oturan N, Guibaud G, Esposito G, Oturan MA (2016) Impact of electrochemical treatment of soil washing solution on PAHdegradation efficiency and soil respirometry. Environ Pollut 211:354–362

    Article  CAS  Google Scholar 

  • Oldfield JE (2002) Se World atlas. Selenium-tellurium development association, Grimbergen

    Google Scholar 

  • Pociecha M, Lestan D (2012) Recycling of EDTA solution after soil washing of Pb, Zn, Cd and As contaminated soil. Chemosphere 86(8):843–846

    Article  CAS  Google Scholar 

  • Pontoni L, van Hullebusch ED, Pechaud Y, Fabbricino M, Esposito G, Pirozzi F (2016) Colloidal mobilization and fate of trace heavy metals in semi-saturated artificial soil (OECD) irrigated with treated wastewater. Sustainability 8(12):1257

    Article  CAS  Google Scholar 

  • Roest K, Heilig HG, Smidt H, de Vos WM, Stams AJ, Akkermans AD (2005) Community analysis of a full-scale anaerobic bioreactro treating paper mill wastewater. Syst Appl Microbiol 28(2):175–185

    Article  CAS  Google Scholar 

  • Satyro S, Race M, Di Natale F, Erto A, Guida M, Marotta R (2016) Simultaneous removal of heavy metals from field-polluted soils and treatment of soil washing effluents through combined adsorption and artificial sunlight-driven photocatalytic processes. Chem Eng J 283(1):1484–1493

    Article  CAS  Google Scholar 

  • Sharma S, Bansal A, Dogra R, Dhillon SK, Dhillon KS (2011) Effect of organic amendments on uptake of selenium and biochemical grain composition of wheat and rape grown on seleniferous soils in northwestern India. J Plant Nutr Soil Sci 174(2):269–275

    Article  CAS  Google Scholar 

  • Stams AJM, Grolle KCF, Frijters CTMJ, Van Lier JB (1992) Enrichment of thermophilic propionate-oxidizing bacteria in syntrophy with Methanobacterium thermoautotrophicum or Methanobacterium thermoformicicum. Appl Environ Microbiol 58(1):346–352

    CAS  Google Scholar 

  • Tan LC, Nancharaiah YV, van Hullebusch ED, Lens PNL (2016) Selenium: environmental significance, pollution, and biological treatment technologies. Biotechnol Adv 34(5):886–907

    Article  CAS  Google Scholar 

  • Trellu C, Ganzenko O, Papirio S, Pechaud Y, Oturan N, Huguenot D, van Hullebusch ED, Esposito G, Oturan MA (2016) Combination of anodic oxidation and biological treatment for the removal of phenanthrene and Tween 80 from soil washing solution. Chem Eng J 306:588–596

    Article  CAS  Google Scholar 

  • Tugarova AV, Vetchinkina EP, Loshchinina EA, Burov AM, Nikitina VE, Kamnev AA (2014) Reduction of selenite by Azospirillum brasilense with the formation of selenium nanoparticles. Microb Ecol 68(3):495–503

    Article  CAS  Google Scholar 

  • Wang Q, Zhang J, Zhao B, Xin X, Deng X, Zhang H (2016) Influence of long-term fertilization on selenium accumulation in soil and uptake by crops. Pedosphere 26(1):120–129

    Article  Google Scholar 

  • Williams KH, Wilkins MJ, N’Guessan AL, Arey B, Dodova E, Dohnalkova A, Holmes D, Lovley DR, Long PE (2013) Field evidence of selenium bioreduction in a uranium-contaminated aquifer. Environ Microbiol Rep 5(3):444–452

    Article  CAS  Google Scholar 

  • Winkel LHE, Vriens B, Jones GD, Schneider LS, Pilin-Smits E, Bañuelos GS (2015) Selenium cycling across soil-plant-atmosphere interfaces: a critical review. Nutrients 7:4199–4239

    Article  CAS  Google Scholar 

  • World Health Organization (2011) Selenium in drinking-water. Geneva

  • Wu Y, Yang J, Tang J, Kerr P, Wong PK (2017) The remediation of extremely acidic and moderate pH soil leachates containing Cu (II) and Cd (II) by native periphytic biofilm. J Clean Prod 162:846–855

    Article  CAS  Google Scholar 

  • Yao R, Wang R, Wang D, Su J, Zheng S, Wang G (2014) Paenibacillus selenitireducens sp. nov., a selenite-reducing bacterium isolated from a selenium mineral soil. Int J Syst Evol Microbiol 64(3):805–811

    Article  CAS  Google Scholar 

  • Yasin M, El Mehdawi AF, Jahn CE, Anwar A, Turner MFS, Faisal M, Pilon-Smits EAH (2014) Seleniferous soils as a source for production of selenium-enriched foods and potential of bacteria to enhance plant selenium uptake. Plant Soil 386(1–2):385–394

    Google Scholar 

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Acknowledgements

The authors thank Dr. Paola Cennamo and Dr. Giorgio Triosi from Università degli Studi Suor Orsola Benincasa (Naples, Italy) for SEM-EDS and P-XRD analysis; Dr. Ludovico Pontoni and Dr. Marco Race from University of Naples “Federico II” (Naples, Italy) for laboratory and instrument assistance. The authors would also like to thank the EU for providing financial support through the Erasmus Mundus Joint Doctorate Programme, Environmental Technologies for Contaminated Solids, Soils and Sediments, grant agreement FPA no. 2010-0009 (ETeCoS3), and the Marie Curie International Incoming Fellowship (MC-IIF) Role of biofilm-matrix components in the extracellular reduction and recovery of chalcogens (BioMatch project no. 103922).

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Correspondence to Shrutika L. Wadgaonkar.

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Wadgaonkar, S.L., Ferraro, A., Nancharaiah, Y.V. et al. In situ and ex situ bioremediation of seleniferous soils from northwestern India. J Soils Sediments 19, 762–773 (2019). https://doi.org/10.1007/s11368-018-2055-7

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  • DOI: https://doi.org/10.1007/s11368-018-2055-7

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