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Evaluation of inhibitory effects of heavy metals on anaerobic ammonium oxidation (anammox) by continuous feeding tests

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Abstract

To facilitate the application of anaerobic ammonium oxidation (anammox) to a nitrogen removal process, the effects of heavy metals (Ni, Cu, Co, Zn, and Mo) on anammox bacteria entrapped in gel carriers were examined by conducting continuous feeding tests for each metal. The results show that all anammox activities decreased by more than 10 % when influent concentrations of Ni, Cu, Co, Zn, and Mo were 5, 5, 5, 10, and 0.2 mg/L, respectively. It was observed that the effects of Ni, Cu, Co, and Zn on anammox activity were reversible and that of Mo on anammox activity was irreversible. Anammox activity was not affected when influent containing mixed Ni, Cu, Co, and Zn (0.5 mg/L) was fed into the reactor.

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References

  • Çeçen F, Semerci N, Geyik AG (2010) Inhibition of respiration and distribution of Cd, Pb, Hg, Ag and Cr species in a nitrifying sludge. J Hazard Mater 178:619–627. doi:10.1016/j.jhazmat.2010.01.130

    Article  PubMed  Google Scholar 

  • Dapana-Mora A, Fernadez I, Campos JL, Mosquera-Corral A, Mendez R, Jetten MSM (2007) Evaluation of activity and inhibitory effects on anammox process by batch tests based on the nitrogen gas production. Enzyme Microb Technol 40:859–865. doi:10.1016/j.enzmictec.2006.06.018

    Article  Google Scholar 

  • Date Y, Isaka K, Ikuta H, Sumino T, Kaneko N, Yoshie S, Tsuneda S, Inamori Y (2009) Microbial diversity of anammox bacteria enriched from different types of seed sludge in an anaerobic continuous-feeding cultivation reactor. J Biosci Bioeng 107:281–286. doi:10.1016/j.jbiosc.2008.11.015

    Article  CAS  PubMed  Google Scholar 

  • Furukawa K, Rouse JD, Bhatti ZI, Imajo U, Nakamura K, Ishida H (2002) Characterization of microbial community in an anaerobic ammonium-oxidizing biofilm cultured on a nonwoven biomass carrier. J Biosci Bioeng 94:87–94. doi:10.1016/S1389-1723(02)80218-3

    Article  Google Scholar 

  • Grunditz C, Gumaelius L, Dalhammar G (1998) Comparison of inhibition assays using nitrogen removing bacteria application to industrial wastewater. Water Res 32:2995–3000. doi:10.1016/S0043-1354(98)00050-5

    Article  CAS  Google Scholar 

  • Guven D, Depana A, Kartal B, Schamid MC, Maas B, van de Pas-Schoonen K, Sozen S, Mendez R, Op den Camp HJM, Jetten MSM, Strous M, Schmidt I (2005) Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl Environ Microbiol 71:1066–1071. doi:10.1128/AEM.71.2.1066-1071.2005

    Article  PubMed Central  PubMed  Google Scholar 

  • Henze M, Harremoes P, Jansen JLC, Arvin E (2002) Wastewater treatment: biological and chemical processes (environmental engineering). Springer, Berlin

    Book  Google Scholar 

  • 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. doi:10.1016/j.watres.2004.06.025

    Article  CAS  PubMed  Google Scholar 

  • Isaka K, Date Y, Sumino T, Yoshie S, Tsuneda S (2006) Growth characteristic of anaerobic ammonium-oxidizing (anammox) bacteria in an anaerobic biological filtrated (ABF) reactor. Appl Microbiol Biotechnol 70:47–52. doi:10.1007/s00253-005-0046-2

    Article  CAS  PubMed  Google Scholar 

  • Isaka K, Date Y, Sumino T, Tsuneda S (2007) Ammonium removal performance of anaerobic ammonium-oxidizing bacteria immobilized in polyethylene glycol gel carrier. Appl Microbiol Biotechnol 76:1457–1495. doi:10.1007/s00253-008-1739-0

    Article  CAS  PubMed  Google Scholar 

  • Isaka K, Suwa Y, Kimura Y, Yamagishi T, Sumino T, Tsuneda S (2008) Anaerobic ammonium oxidation (anammox) irreversibly inhibited by methanol. Appl Microbiol Biotechnol 81:379–385. doi:10.1007/s00253-008-1739-0

    Article  CAS  PubMed  Google Scholar 

  • Isaka K, Itokawa H, Kimura Y, Noto K, Murakami T (2011) Novel autotrophic nitrogen removal system using gel entrapment technology. Bioresource Technol 102:7720–7726. doi:10.1007/s00253-007-1106-6

    Article  CAS  Google Scholar 

  • 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 hazardous materials 100:271–283. doi:10.1016/S0304-3894(03)00116-X

    Article  CAS  Google Scholar 

  • Kimura Y, Isaka K, Kazama F, Sumino T (2010) Effects of nitrite inhibition on anaerobic ammonium oxidation. Appl Microbiol Biotechnol 86:359–365. doi:10.1007/s00253-009-2359-Z

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Isaka K, Kazama F (2011a) Tolerance level of dissolved oxygen to feed into anaerobic ammonium oxidation (anammox) reactor. J Water Environ Technol 9:169–178. doi:10.2965/jwet.2011.169

    Article  Google Scholar 

  • Kimura Y, Isaka K, Kazama F (2011b) Effects of inorganic carbon limitation on anaerobic ammonium oxidation (anammox) activity. Bioresource Technol 102:4390–4394. doi:10.1016/j.biortech.2010.12.101

    Article  CAS  Google Scholar 

  • Kimura Y, Itokawa H, Noto K, Murakami T, Isaka K (2013) Stability of autotrophic nitrogen removal system under four non-steady operations. Bioresource Technol 137:196–201. doi:10.1016/j.biortech.2013.03.130

    Article  CAS  Google Scholar 

  • Liao D, Li X, Yang Q, Zeng G, Guo L, Yoe X (2008) Effect of inorganic carbon on anaerobic ammonium oxidation enriched in sequencing batch reactor. J Environ Sci 20:940–944. doi:10.1016/S1001-0742(08)62190-7

    Article  CAS  Google Scholar 

  • Liu C, Yamamoto T, Nishiyama T, Fujii T, Furukawa K (2009) Effect of salt concentration in anammox treatment using non-woven biomass carrier. J Biosci Bioeng 107:519–523. doi:10.1016/j.jbiosc.2009.01.020

    Article  CAS  PubMed  Google Scholar 

  • Lotti T, Cordola M, Kleerebezem R, Caffaz S, Lubello C, van Loosdrecht MCM (2012) Inhibition effect of swine wastewater heavy metals and antibiotics on anammox activity. Water Sci Technol 66:1519–1526. doi:10.2166/wst.2012.344

    Article  CAS  PubMed  Google Scholar 

  • Mulder A, van de Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–184. doi:10.1016/0168-6496(94)00081-7

    Article  CAS  Google Scholar 

  • Semerci N, Çeçen F (2007) Importance of cadmium speciation in nitrification inhibition. J hazardous materials 147:503–512. doi:10.1016/j.jhazmat.2007.01.041

    Article  CAS  Google Scholar 

  • Strous M, van Gerven 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 31:1955–1962. doi:10.1016/S0043-1354(97)00055-9

    Article  CAS  Google Scholar 

  • Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999a) Missing lithotroph identified as new planctomycete. Nature 400:446–449. doi:10.1038/22749

    Article  CAS  PubMed  Google Scholar 

  • Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1999b) Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol 65:3248–3250

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sumino T, Noto T, Ogasawara T, Hashimoto N, Suwa Y (1997) Nitrification of high concentration ammonium nitrogen using immobilized nitrifying bacteria. In Proceeding of WEFTEC 70th Annual Conference and Exposition, USA, pp.165-172

  • van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiol 142:2187–2196. doi:10.1099/13500872-142-8-2187

    Article  Google Scholar 

  • You SJ, Tsai YP, Huang RY (2009) Effect of heavy metals on nitrification performance in different activated sludge processes. J hazardous materials 165:987–994. doi:10.1016/j.jhazmat.2008.10.112

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by the New Energy and Industrial Technology Development Organization, Japan.

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Correspondence to Yuya Kimura.

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Kimura, Y., Isaka, K. Evaluation of inhibitory effects of heavy metals on anaerobic ammonium oxidation (anammox) by continuous feeding tests. Appl Microbiol Biotechnol 98, 6965–6972 (2014). https://doi.org/10.1007/s00253-014-5735-2

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  • DOI: https://doi.org/10.1007/s00253-014-5735-2

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