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Investigation of copper inhibition of nitrifying moving bed biofilm (MBBR) reactors during long term operations

Abstract

Copper, a prevalent heavy metal in industrial mining wastewaters, has been shown to inhibit nitrification in wastewater treatment systems. Biofilm treatment systems have an inherent potential to reduce inhibition. This study investigated the effects of copper concentration on nitrifying biofilms in moving bed biofilm reactor (MBBR) systems across long term operation using influent ammonia concentrations representative of gold mining wastewater. Conventional isotherm models did not adequately model the attachment of copper to the biofilm. Long term nitritation was shown to be uninhibited at influent copper concentrations between 0.13 and 0.61 mg Cu/L. Nitratation was inhibited with influent copper concentrations of 0.28–0.61 mg Cu/L. There was no statistical difference in biofilm characteristics, including biofilm thickness, mass and density, across all copper concentrations tested, however, changes in biofilm morphology were observed. The demonstrated resistance of the nitrifying biofilm to copper inhibition makes the MBBR system a promising technology for treating ammonia in mining wastewaters.

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References

  1. 1.

    Mineral commodity summaries (2016) U.S. Geological Survey, Virginia. https://doi.org/10.3133/70140094. Accessed 10 June 2017

  2. 2.

    Wastewater systems effluent regulations (2012) Canada Gazette, July 18 2012, Part II, vol 146, No. 15. http://www.gazette.gc.ca/rp-pr/p2/2012/index-eng.html. Accessed February 2017

  3. 3.

    Environmental code for practice of metal mines (2009) Environment Canada, Ottawa. https://www.ec.gc.ca/lcpe-cepa/documents/codes/mm/mm-eng.pdf. Accessed 20 April 2017

  4. 4.

    Canadian Fisheries Act: Metal Mining Effluent Regulations (2002) Retrieved from the Justice Laws website: http://laws-lois.justice.gc.ca/eng/regulations/SOR-2002-222/page-1.html. Accessed 20 April 2017

  5. 5.

    U.S. Clean Water Act, 33 U.S.C. § 1251 et seq. (1972) U.S Environmental Protections Agency, Washington. https://www.epa.gov/laws-regulations/summary-clean-water-act. Accessed February 2017

  6. 6.

    Skinner FA, Walker N (1961) Growth of Nitrosomonas europaea in batch and continuous culture. Archiv für Mikrobiologie 38:339–349

  7. 7.

    Cenci G, Morozzi G (1979) The validity of the TTC-test for dehydrogenase activity of activated sludge in the presence of chemical inhibitors. Zentralbl Bakteriol B 169:320–330

  8. 8.

    Çeçen F, Semerci N, Geyik AG (2010) Inhibitory effects of Cu, Zn, Ni, and Co on nitrification and relevance of speciation. J Chem Technol Biotechnol 85:520–528

  9. 9.

    Sato C, Leung SW, Schnoor JL (1988) Toxic response of Nitrosomonas europaea to copper in inorganic medium and wastewater. Water Res 22:1117–1127

  10. 10.

    Gerardi MH (2002) Nitrification and denitrification in the activated sludge process. Environmental protection magazine series. Wiley, New York

  11. 11.

    Juliastuti SR, Baeyens J, Creemers C, Bixio D, Lodewyckx E (2003) The inhibitory effects of heavy metals and organic compounds on the net maximum specific growth rate of the autotrophic biomass in activated sludge. J Hazard Mater B100:271–283

  12. 12.

    Ochoa-Herrera V, Leon G, Baniban Q, Afield J, Sierra-Alvares R (2011) Toxicity of copper (II) ions to microorganisms in biological wastewater treatment systems. Sci Total Environ 412–413:380–385

  13. 13.

    Sterrit RM, Lester JN (1980) Interactions of heavy metals with bacteria. Sci Total Environ 14:5–17

  14. 14.

    Hu Z, Chandran K, Grasso D, Smets BF (2003) Impact of metal sorption and internalization on nitrification inhibition. Environ Sci Technol 37:728–734

  15. 15.

    Braam F, Klapwijk A (1981) Effect of copper on nitrification in activated sludge. Water Res 15:1093–1098

  16. 16.

    Lee YW, Tian Q, Ong SK, Sato C, Chung J (2009) Inhibitory effects of copper on nitrifying bacteria in suspended and attached growth reactors. Water Air Soil Pollut 203:17–27

  17. 17.

    Hu Z, Chandran K, Grasso D, Smets BF (2004) Comparison of nitrification inhibition by metals in batch and continuous flow reactors. Water Res 38:3949–3959

  18. 18.

    Özbelge TA, Özbelge HO, Altinten P (2007) Effect of acclimatization of microorganisms to heavy metals on the performance of activated sludge process. J Hazard Mater 142:332–339

  19. 19.

    Şengör SS, Gikas P, Moberly JG, Peyton BM, Ginn TR (2011) Comparison of single and joint effects of Zn and Cu in continuous flow and batch reactors. J Chem Technol Biotechnol 87:374–380

  20. 20.

    Ødegaard H (1999) The moving bed biofilm reactor. Water Environmental Engineering and Reuse of Water, Hokkaido Press, pp 250–305

  21. 21.

    White C, Gadd GM (2000) Copper accumulation by sulfate reducing bacterial biofilms. FEMS Microbiol Lett 183:313–318

  22. 22.

    Hoang V, Delatolla R, Laflamme E, Gadbois A (2014) An investigation of moving bed biofilm reactor nitrification during long-term exposure to cold temperatures. Water Environ Res 86:36–42

  23. 23.

    Delatolla R, Tufenkji N, Comeau Y, Gadbois A, Lamarre D, Berk D (2009) Kinetic analysis of attached growth nitrification in cold climates. Water Sci Technol 60:1173–1184

  24. 24.

    Young B, Delatolla R, Ren B, Kennedy K, Laflamme E, Stintzi A (2016) Pilot-scale tertiary MBBR nitrification at 1 °C: characterization of ammonia removal rate, solids settleability and biofilm characteristics. Environ Technol 37:2124–2132

  25. 25.

    Flemming HC (1993) Biofilms and environmental protection. Water Sci Technol 27:1–10

  26. 26.

    Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “House of Biofilm Cells”. J Bacteriol 189:7945–7947

  27. 27.

    Young B, Banihashemi B, Forrest D, Kennedy K, Stinzi A, Delatolla R (2016) Meso and micro-scale response of post carbon removal nitrifying MBBR biofilm across carrier type and loading. Water Res 91:235–243

  28. 28.

    Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91

  29. 29.

    Harrison JJ, Cerl H, Stremick CA, Turner RJ (2004) Biofilm susceptibility to metal toxicity. Environ Microbiol 6:1220–1227

  30. 30.

    Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69:2313–2320

  31. 31.

    Freundlich H (1906) Über die adsorption in Losungen. Z Phys Chem 57:385–471

  32. 32.

    Langmuir I (1918) The adsorption of gases on plane surfaces of glass, mica and platinum. J Am Chem Soc 40:1361–1403

  33. 33.

    Redlich O, Peterson DL (1959) A useful adsorption isotherm. J Phys Chem 63:1024

  34. 34.

    Tran HN, Hosseini-Bandegharaei A, Chao H-P (2017) Mistakes and inconsistencies regarding adsorption of contaminants from aqueous solutions: a critical review. Water Res 120:88–116

  35. 35.

    Black R, Sartaj M, Mohammadian A, Qiblawey HAM (2014) Biosorption of Pb and Cu using fixed and suspended bacteria. J Environ Chem Eng 2:1663–1671

  36. 36.

    U.S. Ore mining and dressing effluent regulations, 40 C.F.R § 440 (1988) U.S Environmental Protections Agency, Washington. https://www.epa.gov/eg/ore-mining-and-dressing-effluent-guidelines. Accessed April 20 2017

  37. 37.

    Water Environment Federation, American Society of Civil Engineers (2009) Design of municipal wastewater treatment plants, MoP8, 5th edn. WEF Press, McGraw Hill, New York

  38. 38.

    Acheampong MA, Paksirajan K, Lens PNL (2013) Assessment of the effluent quality from a gold mining industry in Ghana. Environ Sci Pollut Res 20:3799–3811

  39. 39.

    APHA, AWWA, WEF (1989) Standard methods for examination of water and wastewater, 17th edn. American Public Health Association, Washington, D.C

  40. 40.

    Forrest D, Delatolla R, Kennedy K (2008) Carrier effects on tertiary nitrifying moving bed biofilm reactor: an examination of performance, biofilm and biologically produced solids. Environ Technol 37:662–671

  41. 41.

    Bryers JD (1987) Biologically active surfaces: processes governing the formation and persistence of biofilms. Biotechnol Prog 3:57–68

  42. 42.

    Lee LY, Ong SL, Ng HY, Hu JY, Koh YN (2008) Simultaneous ammonia-nitrogen and copper removal and copper recovery using nitrifying biofilm from the ultra-compact biofilm reactor. Biores Technol 99:6614–6620

  43. 43.

    Vasanth Kumar K, Sivanesan S (2006) Equilibrium data, isotherm parameters and process design for partial and complete isotherm of methylene blue onto activated carbon. J Haz Mater 134:237–244

  44. 44.

    Do DD (1998) Adsorption analysis: equilibrium and kinetics. Imperial College Press, London

  45. 45.

    Scullion J, Winson M, Matthews R (2007) Inhibition and recovery in a fixed microbial film leachate treatment system subject to shock loadings of copper and zinc. Water Res 41:4129–4138

  46. 46.

    Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG (1976) Inhibition of nitrification by ammonia and nitrous acid. J Water Pollut Control Fed 48:835–852

  47. 47.

    Keenan JD, Steiner RL, Fangarol AA (1979) Substrate inhibition of nitrification. J Environ Sci Health A14:377–397

  48. 48.

    Bjornberg C, Lin W, Zimmerman RA (2009) Effect of temperature on biofilm growth dynamics and nitrification in a full-scale MBBR system. In: Proceedings of the Water Environment Federation, WEFTEC 2009: Session 61 through 70, pp 4407–4426

  49. 49.

    De Beer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43:1131–1138

  50. 50.

    Schramm A, Larsen LH, Revsbech NP, Ramsing NB, Amann R, Schleifer KH (1996) Structure and function of a nitrifying biofilm as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol 62:4641–4647

  51. 51.

    Blackburne R, Vadivelu VM, Yuan Z, Keller J (2007) Kinetic characterisation of an enriched Nitrospira culture with comparison to Nitrobacter. Water Res 41:3033–3042

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Acknowledgements

The authors would like to acknowledge Veolia Water Technologies Canada for technical support and in kind donations. In addition, the authors would like the thank Dr. Nimal Desilva for his assistance in analyzing copper concentrations, and Meghan Thompson for laboratory assistance.

Funding

This study was partially funded by the NSERC CREATE in Technologies for Microbiome Science and Engineering (TECHNOMISE CREATE 497995-2017).

Author information

Correspondence to Robert Delatolla.

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The authors declare that they have no conflict of interest.

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Schopf, A., Delatolla, R., Mathew, R. et al. Investigation of copper inhibition of nitrifying moving bed biofilm (MBBR) reactors during long term operations. Bioprocess Biosyst Eng 41, 1485–1495 (2018). https://doi.org/10.1007/s00449-018-1976-2

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Keywords

  • Biofilm
  • Copper
  • Long term operation
  • Moving bed biofilm reactor (MBBR)
  • Nitrification