Waste and Biomass Valorization

, Volume 10, Issue 10, pp 2907–2914 | Cite as

Precipitation of Copper (II) in a Two-Stage Continuous Treatment System Using Sulfate Reducing Bacteria

  • Ayla BilginEmail author
  • Peter R. Jaffé
Original Paper


Biologically driven precipitation of dissolved copper and other trace metals has been used to treat contaminated aqueous streams. However, high dissolved trace metal concentrations can lead to toxicity, and their bioremediation difficult. Furthermore sorption of trace metals onto biomass might result in large amounts of contaminated byproducts. The aim of this work was to develop and test a two-stage reactor to bypass the toxic effects on the bacteria and chemically precipitate copper without contaminating the bulk of the biomass. Hence, copper removal using a sulfate reducing bacteria culture was investigated in a two-stage continuous treatment system. The first reactor was a sand-filled biological reactor in which the sulfate is reduced, followed by a second reactor/clarifier where the chemical precipitation and sedimentation of a CuS phase occurs. The influent Cu2+ concentration was varied systematically between 15 and 600 mg/L, and the precipitation of Cu2+ metal as CuS was achieved in the second reactor, resulting in complete (within detection limits) Cu2+ removal. EDS analysis on the solid phase collected from the second reactor confirmed the presence of Cu and S in the precipitate. EDS analysis on the solid phase collected from the second reactor confirmed the presence of Cu and S in the precipitate, and a CuS phase with minimal biomass was obtained. This configuration avoids toxicity effects of heavy metals in the biological reactor, as well as the contamination of biomass with the trace metal. Furthermore, the biomass free CuS precipitates can be easily disposed or even used to recover the trace metal.


Heavy metal Copper Cooper sulfide Anaerobic treatment Sulfate reducing bacteria 



This study has been supported by 2219 Post-doctoral program and the authors present their thanks to the institution of The Scientific and Technological Research Council of Turkey (TUBITAK). At the same time, the authors are thankful for the support and assistance during the process of working with Environmental Biogeochemistry Research Group of Princeton University: Melany Ruiz Urigüen, Shan Huang, Arianna Sherman, Weitao Shuai, Il Han.


  1. 1.
    Vimala, R., Das, N.: Biosorption of cadmium (II) and lead (II) from aqueous solution using mushrooms: a comparative study. J. Hazard. Mater. 168, 376–382 (2009)CrossRefGoogle Scholar
  2. 2.
    Li, Y., Wu, Y., Wang, Q., Wang, C., Wang, P.: Biosorption of copper, manganese, cadmium, and zinc by Pseudomonas putida isolated from contaminated sediments. Desalination Water Treat. 52(37–39), 7218–7224 (2014)CrossRefGoogle Scholar
  3. 3.
    Zhang, Z.Z., Deng, R., Cheng, Y.F., Zhou, Y.H., Buayi, X., Zhang, X., Wang, H.Z., Jin, R.C.: Behavior and fate of copper ions in an anammox granular sludge reactor and strategies for remediation. J. Hazard. Mater. 30(300), 838–846 (2015)CrossRefGoogle Scholar
  4. 4.
    Ochoa-Herrera, V., Leon, G., Banihani, Q., Field, J.A., Sierra-Alvarez, R.: Toxicity of copper(II) ions to microorganisms in biological wastewater treatment systems. Sci. Total Environ. 412–413, 380–385 (2011)CrossRefGoogle Scholar
  5. 5.
    Radziemska, M., Jeznach, J., Mazur, Z., Fronczyk, J., Bilgin, A.: Assessment of the effect of reactive materials on the content of selected elements in Indian mustard grown in Cu-contaminated soils. J. Water Land Dev. 28, 53–60 (2016)CrossRefGoogle Scholar
  6. 6.
    Fronczyk, J., Radziemska, M., Mazur, Z.: Copper removal from contaminated groundwater using natural and engineered limestone sand in permeable reactive barriers. Fresenius Environ. Bull. 24(1a), 228–234 (2015)Google Scholar
  7. 7.
    Lasat, M.M.: Phytoextraction of toxic metals: a review of biological mechanisms. J. Environ. Qual. 31, 109–120 (2002)CrossRefGoogle Scholar
  8. 8.
    Kumar, R.N., Nagendran, R.: Changes in nutrient profile of soil subjected to bioleaching for removal of heavy metals using Acidithiobacillus thiooxidans. J. Hazard. Mater. 156, 102–107 (2008)CrossRefGoogle Scholar
  9. 9.
    Das, C., Bhowal, A., Datta, S.: Bioremediation of copper-contaminated soil by co-application of bioaugmentation and biostimulation with organic nutrient. Bioremediat. J. 15(2), 90–98 (2011)CrossRefGoogle Scholar
  10. 10.
    Mata, Y.N., Blazquez, M.L., Ballester, A., Gonzalez, F., Munoz, J.A.: Sugar-beet pulp pectin gels as biosorbent for heavy metals: preparation and determination of biosorption and desorption characteristics. Chem. Eng. J. 150, 289–301 (2009)CrossRefGoogle Scholar
  11. 11.
    Perez-Marin, A.B., Ballester, A., Gonzalez, F., Blazquez, M.L., Munoz, J.A., Saez, J., Meseguer Zapata, V.: Study of cadmium, zinc, and lead biosorption by orange wastes using the subsequent addition method. Bioresour. Technol. 99, 8101–8106 (2008)CrossRefGoogle Scholar
  12. 12.
    Peters, R.W., Ku, Y., Batthacharyya, D.: Evaluation of recent treatment techniques for removal of heavy metals from industrial wastewaters. Paper Presented at AIChE Meeting, Philadelphia, PA, 19–22: (1984)Google Scholar
  13. 13.
    Patterson, J.W.: Metals control technology; past, present and future. Separation and recovery. In: Patterson, J.W., Passino, R., (eds.) Metals Speciation, Separation, and Recovery. Proceedings of the Second International Symposium on Metals Speciation, Separation, and Recovery, Rome, Italy, May 14–19, 1989. Lewis Publishers, Chelsea (1990)Google Scholar
  14. 14.
    Veeken, A.H.M., de Vries, S., Van der Mark, A., Rulkens, W.H.: Selective precipitation of heavy metals as controlled by a sulfide-selective electrode. Sep. Sci. Technol. 38(1), 1–19 (2003)CrossRefGoogle Scholar
  15. 15.
    Gallegos-Garcia, M., Celis, L.B., Rangel-Mendez, R., Razo-Flores, E.: Precipitation and recovery of metal sulfides from metal containing acidic wastewater in a sulfidogenic down-flow fluidized bed reactor. Biotechnol. Bioeng. 102, 91–99 (2009)CrossRefGoogle Scholar
  16. 16.
    Tsukamoto, T.K., Killion, H.A., Miller, G.C.: Column experiments for microbiological treatment of acid mine drainage: low-temperature, low-pH and matrix investigations. Water Res. 38, 1405–1418 (2004)CrossRefGoogle Scholar
  17. 17.
    Kieu, H.T., Müller, E., Horn, H.: Heavy metal removal in anaerobic semi-continuous stirred tank reactors by a consortium of sulfate-reducing bacteria. Water Res. 45(13), 3863–3870 (2011)CrossRefGoogle Scholar
  18. 18.
    Jalali, K., Baldwin, S.A.: The role of sulphate reducing bacteria in copper removal from aqueous sulphate solutions. Water Res. 34(3), 797–806 (2000)CrossRefGoogle Scholar
  19. 19.
    Rossi, G.: Environmental applications. Biohydrometallurgy, ch. 6. McGraw Hill, Hamburg (2000)Google Scholar
  20. 20.
    Villa Gómez, D.K.: Simultaneous sulfate reduction and metal precipitation in an inverse fluidized bed reactor. PhD thesis, UNESCO-IHE Institute for Water Education, Delft, The Netherlands (2013)Google Scholar
  21. 21.
    Remoudaki, E., Hatzikioseyian, A., Kousi, P., Tsezos, M.: The mechanism of metals precipitation by biologically generated alkalinity in biofilm reactors. Water Res. 37, 3843–3854 (2003)CrossRefGoogle Scholar
  22. 22.
    Picavet, M., Dijkman, H., Buisman, C.: Development of a novel efficient bioreactor for sulphate reduction. Electron. J. Environ. Agric. Food Chem. 2(2), 297–302 (2003)Google Scholar
  23. 23.
    Sampaio, R.M.M., Timmers, R.A., Xu, Y., Keesman, K.J., Lens, P.N.L.: Selective precipitation of Cu from Zn in a pS controlled continuously stirred tank reactor. J. Hazard. Mater. 165, 256–265 (2009)CrossRefGoogle Scholar
  24. 24.
    Hulshof, A.H.M., Blowes, D.W., Gould, W.D.: Evaluation of in situ layers for treatment of acid min drainage: a field comparison. Water Res. 40, 1816–1826 (2006)CrossRefGoogle Scholar
  25. 25.
    Neculita, C.M., Zagury, G.J., Bussiere, B.: Passive treatment of acid mine drainage in bioreactors using sulfate-reducing bacteria: critical review and research needs. J. Environ. Qual. 36, 1–16 (2007)CrossRefGoogle Scholar
  26. 26.
    Odom, J.M., Singleton, R.: The Sulfate-Reducing Bacteria: Contemporary Perspectives. Springer, New York (1993)CrossRefGoogle Scholar
  27. 27.
    Karnachuk, O.V., Sasaki, K., Gerasimchuk, A.L., Sukhanova, O., Ivasenko, D.A., Kaksonen, A.H., Puhakka, J.A., Tuovinen, O.H.: Precipitation of Cu-sulfides by copper-tolerant Desulfovibrio isolates. Geomicrobiol. J. 25(5), 219–227 (2008)CrossRefGoogle Scholar
  28. 28.
    Luptakova, A., Kusnierova, M.: Bioremediation of acid mine drainage contaminated by SRB. Hydrometallurgy, 77, 97–102 (2005)Google Scholar
  29. 29.
    Hao, O.J.: Metal effects on sulfur cycle bacteria and metal removal by sulfate reducing bacteria. In: Lens, P.N.L., Hulshoff Pol, L. (eds.) Environmental Technologies to Treat Sulfur Pollution: Principles and Engineering, pp. 393–414. IWA Publishing, London (2000)Google Scholar
  30. 30.
    Johnson, D.B., Hallberg, K.B.: Acid mine drainage: remediation options. Sci. Total Environ. 338, 3–14 (2005)CrossRefGoogle Scholar
  31. 31.
    Tabak, H.H., Scharp, R., Burckle, J., Kawahara, F.K., Govind, R.: Advances in biotreatment of acid mine drainage and biorecovery of metals: 1. Metal precipitation for recovery and recycle. Biodegradation 14(6), 423–436 (2003)CrossRefGoogle Scholar
  32. 32.
    Al-Tarazi, M., Heesink, A.B.M., Versteeg, G.F., Azzam, M.O.J., Azzam, K.: Precipitation of CuS and ZnS in a bubble column reactor. AIChE J. 51(1), 235–246 (2005)CrossRefGoogle Scholar
  33. 33.
    Foucher, S., Battaglia-Brunet, F., Ignatiadis, I., Morin, D.: Treatment by sulfate-reducing bacteria of Chessy acid-mine drainage and metals recovery. Chem. Eng. Sci. 56(4), 1639–1645 (2001)CrossRefGoogle Scholar
  34. 34.
    Gramp, P.J., Sasaki, K., Binghman, J.M., Karnachuk, O.V., Tuovinen, O.H.: Formation of covellite (CuS) under biological sulfate-reducing conditions. Geomicrobiol. J. 23(8), 613–619 (2006)CrossRefGoogle Scholar
  35. 35.
    Esposito, G., Veeken, A., Weijma, J., Lens, P.N.L.: Use of biogenic sulfide for ZnS precipitation. Sep. Purif. Technol. 51(1), 31–39 (2006)CrossRefGoogle Scholar
  36. 36.
    Ma, X., Hua, Y.: Cd2+ removal from wastewater by sulfate reducing bacteria with an anaerobic fluidized bed reactor. J. Environ. Sci. 9, 366–371 (1997)Google Scholar
  37. 37.
    Steed, V.S., Suidan, M.T., Gupta, M., Miyahara, T., Acheson, C.M., Sayles, G.D.: Development of a sulfate-reducing biological process to remove heavy metals from acid mine drainage. Water Environ. Res. 72, 530–535 (2000)CrossRefGoogle Scholar
  38. 38.
    Kaksonen, A., Puhakka, J.: Sulfate reduction based bioprocesses for the treatment of acid mine drainage and the recovery of metals. Eng. Life 6, 541–564 (2007)CrossRefGoogle Scholar
  39. 39.
    Dijkman, H., Buisman, C.J.N., Bayer, H.G.: Biotechnology in the mining and metallurgical industries: cost savings through selective precipitation of metal sulfides. In: Proceedings of the Copper 99—Cobre 99 International Conference, Phoenix, Arizona, USA, October 10–13, 1999, Vol. IV: Hydrometallurgy of Copper (Eds: S. K. Young, D. B. Dreisinger, R. P. Hackl, D. G. Dixon), The Minerals, Metals & Materials Society, Warrandale, PA (USA), 113–126 (1999)Google Scholar
  40. 40.
    Vegt, A.L., Krol, J., Buisman, C.J.N.: Biological sulfate removal and metal recovery from mine waters. In: Proceedings of the International Biohydrometallurgy Symposium IBS97, BIOMINE 97, Sydney, Australia, August 4–6, 1997, Australian Mineral Foundation, Glenside, South Australia, 1–10 (1997)Google Scholar
  41. 41.
    Alvarez, M.T., Crespo, C., Mattiasson, B.: Precipitation of Zn(II), Cu(II) and Pb(II) at bench-scale using biogenic hydrogen sulfide from the utilization of volatile fatty acids. Chemosphere 66, 1677–1683 (2007)CrossRefGoogle Scholar
  42. 42.
    Prasad, D., Wai, M., Berube, P., Henry, J.G.: Evaluating substrates in the biological treatment of acid mine drainage. Environ. Technol. 20(5), 449–458 (1999)CrossRefGoogle Scholar
  43. 43.
    Prasad, D., Henry, J.G.: Removal of sulphates acidity and iron from acid mine drainage in a bench scale biochemical treatment system. Environ. Technol. 30(2), 151–160 (2009)CrossRefGoogle Scholar
  44. 44.
    APHA; AWWA. Standard Methods for Water and Wastewater Examinations, 21st edn.; American Public Health Association (APHA); American Water Works Association (AWWA): Washington, DC (2005)Google Scholar
  45. 45.
    Metcalf and Eddy. Wastewater Engineering: Treatment, Disposal, and Reuse, 3rd edn.; McGraw-Hill, Inc.: New York, NY (1991)Google Scholar
  46. 46.
    Grady, C.P.L., Daigger, G.T., Lim, H.C.: Biological Wastewater Treatment, 2nd edn.; Marcel Dekker Inc.: New York, NY (1999)Google Scholar
  47. 47.
    Isa, Z., Grusenmeyer, S., Verstraete, W.: Sulfate reduction relative to methane production in high-rate anaerobic digestion: microbiological aspects. Appl. Environ. Microbiol. 51(3), 580–587 (1986)Google Scholar
  48. 48.
    Goble, R.J.: The leaching of copper from anilite and the production of a metastable copper sulfide structure. Can. Miner. 19, 583–591 (1981)Google Scholar
  49. 49.
    Tezuka, K., Sheets, W.C., Kurihara, R., Shan, Y.J., Imoto, H., Marks, T.J., Poeppelmeier, K.R.: Synthesis of covellite (CuS) from the elements. Solid State Sci. 9(1), 95–99 (2007)CrossRefGoogle Scholar
  50. 50.
    Cao, J., Zhang, G., Mao, Z., Fang, Z., Yang, C.: Precipitation of valuable metals from bioleaching solution by biogenic sulfides. Miner. Eng. 22, 289–295 (2009)CrossRefGoogle Scholar
  51. 51.
    McNeil, M.B., Jones, J.M., Little, B.J.: Mineralogical fingerprints for corrosion processes induced by sulfate reducing bacteria. NACE Annual Conference, Paper 580:1–16: (1991)Google Scholar
  52. 52.
    Baas-Becking, L.G.M., Moore, D.: Biogenic sulfides. Econ. Geol. 56, 259–272 (1961)CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental EngineeringArtvin Coruh UniversityArtvinTurkey
  2. 2.Department of Civil and Environmental EngineeringPrinceton UniversityPrincetonUSA

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