Skip to main content
SpringerLink
Log in

Optimization of a bioremediation system of soluble uranium based on the biostimulation of an indigenous bacterial community

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

High concentrations of uranium(VI) in the Witwatersrand Basin, South Africa from mining leachate is a serious environmental concern. Treatment systems are often ineffective. Therefore, optimization of a bioremediation system that facilitates the bioreduction of U(VI) based on biostimulation of indigenous bacterial communities can be a viable alternative. Tolerance of the indigenous bacteria to high concentrations of U and the amount of citric acid required for U removal was optimized. Two bioreactor studies which showed effective U(VI) removal more than 99 % from low (0.0037 mg L−1) and high (10 mg L−1) concentrations of U to below the limit allowed by South African National Standards for drinking water (0.0015 mg L−1). The second bioreactor was able to successfully adapt even with increasing levels of U(VI) feed water up to 10 mg L−1, provided that enough electron donor was available. Molecular biology analyses identified Desulfovibrio sp. and Geobacter sp. among known species, which are known to reduce U(VI). The mineralogical analysis determined that part of the uranium precipitated intracellularly, which meant that the remaining U(VI) was precipitated as U(IV) oxides and TEM-EDS also confirmed this analysis. This was predicted with the geochemical model from the chemical data, which demonstrated that the treated drainage was supersaturated with respect to uraninite > U4O9 > U3O8 > UO2(am). Therefore, the tolerance of the indigenous bacterial community could be optimized to remediate up to 10 mg L−1, and the system can thus be upscaled and employed for remediation of U(VI) impacted sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allison JD, Brown DS, Novo-Gradac KJ (1991) MINTEQA2/PRODEFA2, A geochemical assessment model for environmental systems. Version 3.0 User’s Manual, Environmental Research Laboratory, Office of Research and Development, US Environmental Protection Agency, EPA/600/3-911021, Athens, Georgia

  • Asikainen M (1981) State of disequilibrium between 238-U, 234-U, 226-Ra and 222-Rn in groundwater from bedrock. Geochim Cosmochim Acta 45(2):201–206

    Article  CAS  Google Scholar 

  • Au WW, Wilkinson GS, Tyning SK, Legator MS, Al Zein R, Hallberg L, Heo MY (1996) Monitoring populations for DNA repair deficiency and for cancer susceptibility. Environ Health Perspect 104(3):579–584

    Article  CAS  Google Scholar 

  • Betcher RN, Gascoyne M, Brown D (1988) Uranium in groundwater of southeastern Manitoba, Canada. Can J Earth Sci 25(12):2089–2103

    Article  CAS  Google Scholar 

  • Beyenal H, Sani RK, Peyton BM, Dohnalkova AC, Amonette JE, Lewandowski Z (2004) Uranium immobilization by sulfate-reducing biofilms. Environ Sci Technol 38:2067–2074

    Article  CAS  Google Scholar 

  • Cason ED, Piater LA, van Heerden E (2012) Reduction of U(VI) by the deep surface bacterium, Thermus scotoductus SA-01, and the involvement of the ABC transporter protein. Chemosphere 86(6):572–577

    Article  CAS  Google Scholar 

  • Cho H, Lee J, Choi Y (2003) The genetic diversity of the bacterial community in groundwater by denaturing gradient gel electrophoresis (DGGE). J Microbiol 41(4):327–334

    CAS  Google Scholar 

  • Coetzee H, Winde F, Wade PW (2006) An assessment of sources, pathways, mechanisms and risks of current and potential future pollution of water and sediments in gold-mining areas of the Wonderfonteinspruit catchment. Report No. 1214/06. Water Research Commission, Pretoria

  • Department of Water Affairs (2011) South African national standard—drinking water. Part 1: microbiological, physical, aesthetic and chemical determinants

  • Dong H, Onstott TC, DeFlaun MF, Fuller ME, Gillespie KM, Fredrickson JK (1999) Development of radiographic and microscopic techniques for the characterization of bacterial transport in intact sediment cores from Oyster, Virginia. J Microbiol Methods 3:139–154

    Article  Google Scholar 

  • Durand JF (2012) The impact of gold mining on the Witwatersrand on the rivers and karst system of Gauteng and North West province, South Africa. J Afr Earth Sci 68:24–43

    Article  Google Scholar 

  • Finneran KT, Housewright ME, Lovley DR (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4(9):510–516

    Article  CAS  Google Scholar 

  • Fuller ME, Dong H, Mailloux BJ, Onstott TC, DeFlaun MF (2000) Examining bacterial transport in intact cores from Oyster, Virginia: effect of sedimentary facies type on bacterial breakthrough and retention. Water Resour Res 36(9):2417–2431

    Article  CAS  Google Scholar 

  • Islam E, Dhal PK, Kazy SK, Sar P (2011) Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: a comparative study. J Environ Sci Health 46:271–280

    Article  CAS  Google Scholar 

  • Kalin M, Wheeler WN, Meinrath G (2005) The removal of uranium from mining waste water using algal/microbial biomass. J Environ Radioact 78:151–177

    Article  CAS  Google Scholar 

  • Kilincarslan A, Akylin S (2005) Uranium adsorption characteristic and thermodynamic behavior of clinoptilolite zeolite. J Radioanal Nucl Chem 264(3):541–548

    Article  CAS  Google Scholar 

  • Kumar A, Rout S, Narayanan U, Mishra MK, Tripathi RM, Singh J, Kumar S, Kushwaha HS (2011) Geochemical modelling of uranium speciation in the subsurface aquatic environment of Punjab State in India. J Geol Min Res 3(5):137–146

    Google Scholar 

  • Langmuir D (1978) Uranium solution-mineral equilibria at low temperatures with applications to sedimentary ore deposits. Geochim Cosmochim Acta 42:547–569

    Article  CAS  Google Scholar 

  • Lee LM, Herbert BE (2001) A GIS survey of arsenic and other trace metals in groundwater resources of Texas. Geological society of america 2001, annual meeting. Abstr Programs Geol Soc Am 5(33):53

    Google Scholar 

  • Lee SY, Baik MH, Cho H, Jung EC, Jeong JT, Choi JW, Lee YB, Lee YJ (2013) Abiotic reduction of uranium by mackinawite (FeS) biogenerated under sulfate-reducing condition. J Radioanal Nucl Chem 296:1311–1319

    Article  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1992) Bioremediation of uranium contamination with enzymatic uranium reduction. Environ Sci Technol 26:2228–2234

    Article  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1994) Reduction of chromate by Desulfovibrio vulgaris and its c 3 cytochrome. Appl Environ Microbiol 60(2):726–728

    CAS  Google Scholar 

  • Lovley DR, Roden EE, Phillips EJP, Woodward JC (1993a) Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar Geol 113:41–53

    Article  CAS  Google Scholar 

  • Lovley DR, Widman PK, Woodward JC, Phillips EJP (1993b) Reduction of uranium by cytochrome c 3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59(11):3572–3576

    CAS  Google Scholar 

  • Manders P (2009) Acid mine drainage in South Africa, Briefing Note 2009/02, CSIR. <http://www.csir.co.za/nre/docs/BriefingNote2009_2_AMD_draft.pdf> (accessed 06.06.11)

  • Martinez RJ, Beazley MJ, Taillefert M, Arakaki AK, Skolnick J, Sobecky PA (2007) Aerobic uranium(VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide-and metal-contaminated subsurfaces soils. Environ Microbiol 9(12):3122–3133

    Article  CAS  Google Scholar 

  • Merroun ML, Nedelkova M, Ojeda JJ, Reitz T, Fernandez ML, Arias JM, Romero-Gonzalez M, Selenska-Pobell S (2011) Bio-precipitation of uranium by two bacterial isolates recovered from extreme environments as estimated by potentiometric titration, TEM and X-ray absorption spectroscopic analyses. J Hazard Mater 197:1–10

    Article  CAS  Google Scholar 

  • Muyzer G, De Waal E, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700

    CAS  Google Scholar 

  • Naicker K, Cukrowska E, McCarthy TS (2003) Acid mine drainage arising from gold mining activity in Johannesburg, South Africa and environs. Environ Pollut 122:29–40

    Article  CAS  Google Scholar 

  • National Nuclear Regulator (2007) Radiological impacts of the mining activities to the public in the Wonderfontein Catchment area. Report No. TR-RRD-07-0006

  • Nevin KP, Finneran KT, Lovley DR (2003) Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69(6):3672–3675

    Article  CAS  Google Scholar 

  • Nikie Z, Kovacevic J, Radosevic B (2002) Uranium content in groundwater in Stara Planina Triassic sediments. In: Merkel BJ, Planer-Fiedrich B, Wolkersdorfer C (eds) Uranium in the aquatic environment: proceedings of the International Conference Uranium Mining and Hydrogeology III and the International Mine Water Association Symposium, Freiberg, Germany, September 15–21. SpringerSpringer-Verlag, Berlin, pp 99–106

    Google Scholar 

  • Parkhurst DL, Appelo CAJ (2005) PHREEQC-2 version 2.12: A hydrochemical transport model. http://wwwbrr.cr.usgs.gov

  • Payne RB, Gentry DM, Rapp-Giles BJ, Casalot L, Wall JD (2002) Uranium reduction by Desulfovibrio desulfuricans strain G20 and a cytochrome c 3 mutant. Appl Environ Microbiol 68(6):3129–3132

    Article  CAS  Google Scholar 

  • Porcelli D, Andersson PS, Baskaran M, Wasserburg GJ (2001) Transport of U- and Th-series nuclides in a Baltic shield watershed and the Baltic sea. Geochim Cosmochim Acta 65(15):2439–2459

    Article  CAS  Google Scholar 

  • Ray AE, Bargar JR, Sivaswamy V, Dohnalkova AC, Fujita Y, Peyton BM, Magnuson TS (2011) Evidence for multiple mode of uranium immobilization by anaerobic bacterium. Geochim Cosmochim Acta 75:2684–2695

    Article  CAS  Google Scholar 

  • Sani RK, Peyton BM, Amonette JE, Geesey GG (2004) Reduction of uranium(VI) under sulfate-reducing conditions in the presence of Fe(III)-(hydr)oxides. Geochim Cosmochim Acta 68(12):2639–2648

    Article  CAS  Google Scholar 

  • Scott R (1995) Flooding of Central and East Rand gold mines—an investigation into controls over the inflow rate, water quality and the predicted impacts of flooded mines. Report No. 486/1/95. Water Research Commission, Pretoria

  • Shelobolina ES, O’Neil K, Finneran KT, Hayes LA, Lovley DR (2003) Potential for in situ bioremediation of a low-pH, high-nitrate uranium-contaminated groundwater. Soil Sediment Contam 12:865–884

    Article  CAS  Google Scholar 

  • Sherman HM, Gierke JS, Anderson CP (2007) Controls on spatial variability of uranium in sandstone aquifers. Ground Water Monit Rem 27(2):106–118

    Article  CAS  Google Scholar 

  • Sinha DK, Shrivastava PK, Hansoti SK, Sharma PK (1997) Uranium and radon concentration in ground water of Deccan Trap country and environmental hazard in Keolari-Nainpur area, Seoni-Mandla District, Madhya Pradesh. Spec Publ Ser Geol Surv India 2(48):115–121

    Google Scholar 

  • Spear JR, Figueroa LA, Honeyman BD (2000) Modeling reduction of uranium U(VI) under variable sulfate concentrations by sulfate-reducing bacteria. Appl Environ Microbiol 66(9):3711–3721

    Article  CAS  Google Scholar 

  • Suzuki Y, Banfield JF (2004) Resistance to, and accumulation of, uranium by bacteria from a uranium-contaminated sites. Geomicrobiol J 21:113–121

    Article  CAS  Google Scholar 

  • Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2005) Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. Appl Environ Microbiol 71(4):1790–1797

    Article  CAS  Google Scholar 

  • Venter AJA (1995) Assessment of the effects of gold-mine effluent on the natural aquatic environment. Unpublished PhD Thesis, Rand Afrikaans University, Johannesburg

  • Viljoen M (2009) The life, death and revival of the central Rand Goldfied. World Gold Conference 2009, The Southern African Institute of Mining and Metallurgy. Department of Geology, University of the Witwatersrand

  • Winde F (2006) Challenges for sustainable water use in dolomitic mining regions of South Africa—a case study of uranium pollution part I: sources and pathways. Phys Geogr 27(4):333–347

    Article  Google Scholar 

  • Winde F (2010) Uranium pollution of the Wonderfonteinspruit, 1997-2008 Part 2: uranium in water—concentrations, loads and associated risks. Water SA 36(3):257–278

    CAS  Google Scholar 

  • Winde F, Wade P, van der Walt IJ (2004) Gold tailings as a source of waterborne uranium contamination of streams—the Koekemoerspruit (Klerksdorp goldfield, South Africa) as a case study part I of III: uranium migration along the aqueous pathway. Water SA 30(2):233–239

    CAS  Google Scholar 

  • Zaire R, Griffin CS, Simpson PJ, Papworth DG, Savage JR, Armstrong S (1996) Analysis of lymphocytes from uranium mine workers in Namibia for chromosomal damage using fluorescence in situ hybridization. Mutat Res 371:109–117

    Article  Google Scholar 

  • Zaire R, Notter M, Riedel W, Thiel E (1997) Unexpected rates of chromosomal instabilities and alterations of hormone levels in Namibian uranium miners. Radiat Res 147:579–584

    Article  CAS  Google Scholar 

  • Zouridakis N, Ochsenkuhn KM, Savidou A (2002) Determination of uranium and radon in potable water samples. J Environ Radioact 61(2):225–232

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Centre of Microscopy, Institution of Groundwater Studies, Steven Lotter, and Prof. Walter Purcell at Department of Chemistry. This study was conducted with financial support from the TIA/UFS Metagenomics Platform and National Research Foundation.

Author information

Authors and Affiliations

  1. TIA/UFS Metagenomics Platform, Department of Microbial, Biochemical and Food Biotechnology, University of the Free State, PO Box 339, Bloemfontein, 9300, South Africa

    Maleke Maleke, Peter Williams, Julio Castillo, Elsabe Botes, Abidemi Ojo & Esta van Heerden

  2. Geosyntec Consultants, Ewing, NJ, USA

    Mary DeFlaun

Authors
  1. Maleke Maleke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julio Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elsabe Botes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abidemi Ojo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mary DeFlaun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Esta van Heerden
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Esta van Heerden.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maleke, M., Williams, P., Castillo, J. et al. Optimization of a bioremediation system of soluble uranium based on the biostimulation of an indigenous bacterial community. Environ Sci Pollut Res 22, 8442–8450 (2015). https://doi.org/10.1007/s11356-014-3980-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3980-7

Keywords

Search

Navigation