Biodegradation

, Volume 23, Issue 5, pp 751–762 | Cite as

Inhibitory effects of free ammonia on Anammox bacteria

  • Cigdem Kalkan Aktan
  • Kozet Yapsakli
  • Bulent Mertoglu
Original Paper

Abstract

Anammox bacteria can effectively treat high ammonia and nitrite concentrations under anoxic environments. However, the presence of high ammonia and nitrite concentrations may cause free ammonia and nitrous acid inhibition at high pH and temperature environments. In this study, the inhibitory effect of free ammonia on Anammox bacteria was investigated in a lab-scale upflow fixed-bed reactor with Kaldnes biofilm carriers. Results of continuous operation showed that inhibition was not observed in the Anammox reactor when the free ammonia concentration gradually increased up to 150 mg/L. However, Anammox activity suddenly dropped to 10 % when the free ammonia concentration reached to 190 mg/L. Nevertheless, high influent ammonia and nitrite concentrations up to 1,500 and 500 mg/L, respectively, did not noticeably inhibit the Anammox activity. Gradually decreasing Anammox activity was also supported by fluorescent in situ hybridization (FISH) analysis. FISH and 16S rRNA gene analysis results revealed that main Anammox organisms were phylogenetically related to Candidatus Kuenenia stuttgartiensis, Candidatus Jettenia asiatica and Candidatus Brocadia anammoxidans.

Keywords

Free ammonia Inhibition Kaldnes rings Anammox Molecular tools 

References

  1. Abma WR, Schultz CE, Mulder JW, van der Star WRL, Strous M, Tokutomi T, van Loosdrecht MCM (2007) Full-scale granular sludge Anammox process. Water Sci Technol 55(8–9):27–33. doi:10.2166/wst.2007.238 PubMedGoogle Scholar
  2. Angelidaki I, Molinuevo B, Garcia MC, Karakashev D (2009) Anammox for ammonia removal from pig manure effluents: effect of organic matter content on process performance. Bioresour Technol 100(7):2171–2175. doi:10.1016/j.biortech.2008.10.038 PubMedCrossRefGoogle Scholar
  3. Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG (1976) Inhibition of nitrification by ammonia and nitrous-acid. J Water Pollut Con F 48(5):835–852Google Scholar
  4. APHA (2005) Standard methods for the examination of water and wastewaterGoogle Scholar
  5. Bae W, Park S (2009) Modeling kinetics of ammonium oxidation and nitrite oxidation under simultaneous inhibition by free ammonia and free nitrous acid. Process Biochem 44(6):631–640. doi:10.1016/j.procbio.2009.02.002 CrossRefGoogle Scholar
  6. Bettazzi E, Caffaz S, Vannini C, Lubello C (2010) Nitrite inhibition and intermediates effects on Anammox bacteria: a batch-scale experimental study. Process Biochem 45(4):573–580. doi:10.1016/j.procbio.2009.12.003 CrossRefGoogle Scholar
  7. Calli B, Mertoglu B, Inanc B, Yenigun O (2005) Effects of high free ammonia concentrations on the performances of anaerobic bioreactors. Process Biochem 40(3–4):1285–1292. doi:10.1016/j.procbio.2004.05.008 CrossRefGoogle Scholar
  8. Egli K, Fanger U, Alvarez PJJ, Siegrist H, van der Meer JR, Zehnder AJB (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175(3):198–207PubMedCrossRefGoogle Scholar
  9. Ergas SJ, Yuan X, Kumar A, Sahu AK (2011) Impact of ammonia concentration on Spirulina platensis growth in an airlift photobioreactor. Bioresour Technol 102(3):3234–3239. doi:10.1016/j.biortech.2010.11.019 PubMedCrossRefGoogle Scholar
  10. Fernandez I, Dosta J, Vazquez-Padin JR, Mosquera-Corral A, Campos JL, Mata-Alvarez J, Mendez R (2008) Short- and long-term effects of temperature on the Anammox process. J Hazard Mater 154(1–3):688–693. doi:10.1016/j.jhazmat.2007.10.082 PubMedGoogle Scholar
  11. Gallert C, Winter J (1997) Mesophilic and thermophilic anaerobic digestion of source-sorted organic wastes: effect of ammonia on glucose degradation and methane production. Appl Microbiol Biot 48(3):405–410CrossRefGoogle Scholar
  12. Gaul T, Marker S, Kunst S (2005) Start-up of moving bed biofilm reactors for deammonification: the role of hydraulic retention time, alkalinity and oxygen supply. Water Sci Technol 52(7):127–133Google Scholar
  13. Heinrichs DM, Poggivaraldo HM, Oleszkiewicz JA (1990) Effects of ammonia on anaerobic-digestion of simple organic substrates. J Environ Eng Asce 116(4):698–710CrossRefGoogle Scholar
  14. Hellinga C, Schellen AAJC, Mulder JW, van Loosdrecht MCM, Heijnen JJ (1998) The SHARON process: an innovative method for nitrogen removal from ammonium-rich waste water. Water Sci Technol 37(9):135–142CrossRefGoogle Scholar
  15. Jetten MSM, I C, Kartal B, van Niftrik L, van de Pas-Schoonen KT, Sliekers O, Haaijer S, van der Star W, Schmid M, van de Vossenberg J, I S, Harhangi H, van Loosdrecht M, Kuenen JG, den Camp HO, Strous M (2005) 1994–2004: 10 years of research on the anaerobic oxidation of ammonium. Biochem Soc T 33:119–123Google Scholar
  16. Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen UGJM, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG (1998) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22(5):421–437PubMedCrossRefGoogle Scholar
  17. Jung JY, Kang SH, Chung YC, Ahn DH (2007) Factors affecting the activity of anammox bacteria during start up in the continuous culture reactor. Water Sci Technol 55(1–2):459–468. doi:10.2166/wst.2007.023 PubMedGoogle Scholar
  18. Kartal B, Kuypers MMM, Lavik G, Schalk J, den Camp HJMO, Jetten MSM, Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol 9(3):635–642. doi:10.1111/j.1462-2920.2006.01183.x PubMedCrossRefGoogle Scholar
  19. Kim DJ, Lee DI, Keller J (2006) Effect of temperature and free ammonia on nitrification and nitrite accumulation in landfill leachate and analysis of its nitrifying bacterial community by FISH. Bioresource Technol 97(3):459–468. doi:10.1016/j.biortech.2005.03.032 CrossRefGoogle Scholar
  20. Kim HW, Nam JY, Shin HS (2010) Ammonia inhibition of electricity generation in single-chambered microbial fuel cells. J Power Sources 195(19):6428–6433. doi:10.1016/j.jpowsour.2010.03.091 CrossRefGoogle Scholar
  21. Liu JX, Liang Z (2008) Landfill leachate treatment with a novel process: anaerobic ammonium oxidation (Anammox) combined with soil infiltration system. J Hazard Mater 151(1):202–212. doi:10.1016/j.jhazmat.2007.05.068 PubMedCrossRefGoogle Scholar
  22. Liu ST, Yang FL, Gong Z, Meng FG, Chen HH, Xue Y, Furukawa KJ (2008) Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresource Technol 99(15):6817–6825. doi:10.1016/j.biortech.2008.01.054 CrossRefGoogle Scholar
  23. Mata-Alvarez J, Gali A, Dosta J, van Loosdrecht MCM (2007) Two ways to achieve an anammox influent from real reject water treatment at lab-scale: partial SBR nitrification and SHARON process. Process Biochem 42(4):715–720. doi:10.1016/j.procbio.2006.12.002 CrossRefGoogle Scholar
  24. Mertoglu B, Calli B, Girgin E, Inanc B, Ozturk I (2005) Comparative analysis of nitrifying bacteria in full-scale oxidation ditch and aerated nitrification biofilter by using fluorescent in situ hybridization (FISH) and denaturing gradient gel electrophoresis (DGGE). J Environ Sci Heal A 40(5):937–948. doi:10.1081/Ese-200056115 CrossRefGoogle Scholar
  25. Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16(3):177–183CrossRefGoogle Scholar
  26. Neef A, Amann R, Schlesner H, Schleifer KH (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiol Uk 144:3257–3266CrossRefGoogle Scholar
  27. Schmid MC, Maas B, Dapena A, de Pas-Schoonen KV, de Vossenberg JV, Kartal B, van Niftrik L, Schmidt I, Cirpus I, Kuenen JG, Wagner M, Damste JSS, Kuypers M, Revsbech NP, Mendez R, Jetten MSM, Strous M (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microb 71(4):1677–1684. doi:10.1128/Aem.71.4.1677-1684.2005 CrossRefGoogle Scholar
  28. Speece RE (1996) Anaerobic biotechnology for industrial wastewaters. Archae Press, NashvilleGoogle Scholar
  29. Sprott GD, Patel GB (1986) Ammonia toxicity in pure cultures of methanogenic bacteria. Syst Appl Microbiol 7(2–3):358–363CrossRefGoogle Scholar
  30. Strous M, VanGerven E, Zheng P, Kuenen JG, Jetten MSM (1997) Ammonium removal from concentrated waste streams with the anaerobic ammonium oxidation (anammox) process in different reactor configurations. Water Res 31(8):1955–1962CrossRefGoogle Scholar
  31. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50(5):589–596CrossRefGoogle Scholar
  32. Strous M, Kuenen JG, Jetten MSM (1999) Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol 65(7):3248–3250PubMedGoogle Scholar
  33. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440(7085):790–794. doi:10.1038/nature04647 PubMedCrossRefGoogle Scholar
  34. Sung SW, Liu T (2003) Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere 53(1):43–52. doi:10.1016/S0045-6535(03)00434-X PubMedCrossRefGoogle Scholar
  35. Tang CJ, Zheng P, Mahmood Q, Chen JW (2009) Start-up and inhibition analysis of the Anammox process seeded with anaerobic granular sludge. J Ind Microbiol Biotechnol 36(8):1093–1100. doi:10.1007/s10295-009-0593-0 PubMedCrossRefGoogle Scholar
  36. Tokutomi T, Yamauchi H, Nishimura S, Yoda M, Abma W (2011) Application of the nitritation and anammox process into ınorganic nitrogenous wastewater from semiconductor factory. J Environ Eng Asce 137(2):146–154. doi:10.1061/(Asce)Ee.1943-7870.0000303 CrossRefGoogle Scholar
  37. van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, Van Loosdrecht MCM (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41(18):4149–4163. doi:10.1016/j.watres.2007.03.044 PubMedCrossRefGoogle Scholar
  38. van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM (2008) The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101(2):286–294. doi:10.1002/bit.21891 PubMedCrossRefGoogle Scholar
  39. van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON((R))-Anammox((R)) process for treatment of ammonium rich wastewater. Water Sci Technol 44(1):153–160PubMedGoogle Scholar
  40. van Kempen R, Mulder JW, Uijterlinde CA, Loosdrecht MCM (2001) Overview: full scale experience of the SHARON (R) process for treatment of rejection water of digested sludge dewatering. Water Sci Technol 44(1):145–152PubMedGoogle Scholar
  41. Villaverde S, Fdz-Polanco F, Garcia PA (2000) Nitrifying biofilm acclimation to free ammonia in submerged biofilters. Start-up influence. Water Res 34(2):602–610CrossRefGoogle Scholar
  42. Waki M, Tokutomi T, Yokoyama H, Tanaka Y (2007) Nitrogen removal from animal waste treatment water by anammox enrichment. Bioresour Technol 98(14):2775–2780. doi:10.1016/j.biortech.2006.09.031 PubMedCrossRefGoogle Scholar
  43. Yang J, Zhang L, Hira D, Fukuzaki Y, Furukawa K (2011) High-rate nitrogen removal by the Anammox process at ambient temperature. Bioresour Technol 102(2):672–676. doi:10.1016/j.biortech.2010.08.039 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Cigdem Kalkan Aktan
    • 1
  • Kozet Yapsakli
    • 1
  • Bulent Mertoglu
    • 2
  1. 1.Department of Environmental EngineeringMarmara UniversityGoztepe, IstanbulTurkey
  2. 2.Department of BioengineeringMarmara UniversityGoztepe, IstanbulTurkey

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