Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 15, pp 6713–6723 | Cite as

Abundance and diversity of anammox bacteria in a mainstream municipal wastewater treatment plant

  • Ali Nejidat
  • Damiana Diaz-Reck
  • Nedal Massalha
  • Adi Arbiv
  • Anwar Dawas
  • Carlos Dosoretz
  • Isam Sabbah
Environmental biotechnology

Abstract

Among the factors that obstruct the application of anammox-based technology for nitrogen removal from mainstream municipal wastewater is the water’s high organic loads. We hypothesized that some anammox species can adapt and grow in mainstream wastewater in which a minimal temperature of 13–15 °C is maintained. Using the AMX368F and AMX820R PCR-primers, anammox bacteria were detected in influent wastewater (COD/N ratio > 13) and in the anaerobic, anoxic, and aerobic chambers of a full-scale municipal wastewater treatment plant, reaching 107 copies/g VSS of the16S rRNA gene. Furthermore, anammox activity was demonstrated by 15N-isotopic tracing. The DNA sequences of clones randomly selected from a clone library were mainly clustered with Candidatus Brocadia flugida in addition to Ca. Brocadia sinica, Ca. Jettenia asiatica, and Ca. Anammoxoglobus propionicus. However, Ca. Brocadia was the only genus detected by high-throughput next-generation sequencing and denaturing gradient gel electrophoresis. The nitrite producers, ammonia-oxidizing archaea and bacteria, were both detected in the influent wastewater and the other chambers, while the nitrite consumers, Nitrospira nitrite oxidizers and the nirS-type denitrifiers, dominated all chambers. The results indicate the occurrence and potential activity of anammox bacteria in mainstream wastewater under certain conditions (proper temperature). The dominance of Brocadia flugida and Anammoxoglobus propionicus suggests a role for volatile fatty acids in selecting the anammox community in wastewater.

Keywords

Anammox abundance Anammox diversity Mainstream wastewater 

Notes

Acknowledgments

The authors thank Prof. Zeev Ronen for his help in performing the N-isotopes experiments.

Funding information

This research was funded by a grant from the Ministry of Science, Technology and Space of the State of Israel (grant no. 3-11871).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2018_9126_MOESM1_ESM.pdf (618 kb)
ESM 1 (PDF 618 kb)

References

  1. APHA (1989) Standard methods for the examination of water and wastewater, 17th edn. American Public Health Association, Washington, DCGoogle Scholar
  2. Ali M, Okabe S (2015) Anammox-based technologies for nitrogen removal: advances in process start-up and remaining issues. Chemosphere 141:144–153CrossRefPubMedGoogle Scholar
  3. Chamchoi N, Nitisoravut S (2007) Anammox enrichment from different conventional sludges. Chemosphere 66:2225–2232CrossRefPubMedGoogle Scholar
  4. Chamchoi N, Nitisoravut S, Schmidt JE (2008) Inactivation of anammox communities under concurrent operation of anaerobic ammonium oxidation (ANAMMOX) and denitrification. Bioresour Technol 99:3331–3336CrossRefPubMedGoogle Scholar
  5. Dapena-Mora A, Fern’andez I, Campos JL, Mosquera-Corral A, M’endez R, MSM J (2007) Evaluation of activity and inhibition effects on Anammox process by batch tests based on the nitrogen gas production. Enzym Microb Technol 40:859–865CrossRefGoogle Scholar
  6. Dosta J, Fernández I, Vázquez-Padín JR, Mosquera-Corral A, Campos JL, Mata-Álvarez J, Méndez R (2008) Short- and long-term effects of temperature on the Anammox process. J Hazard Mater 154:688–693CrossRefPubMedGoogle Scholar
  7. Ge S, Wang S, Yang X, Qiu S, Li B, Peng Y (2015) Detection of nitrifiers and evaluation of partial nitrification for wastewater treatment: a review. Chemosphere 140:85–98CrossRefPubMedGoogle Scholar
  8. Henze M (1992) Characterization of wastewater for modelling of activated sludge processes. Water Sci Technol 25:1–15CrossRefGoogle Scholar
  9. Henze M, Comeau Y (2008) Wastewater characterization. In: Biological wastewater treatment: principles modelling and design. Edited by M. Henze, M.C.M. van Loosdrecht, G.A. Ekama and D. Brdjanovic. ISBN: 9781843391883, pp. 33-52. IWA Publishing, London, UKGoogle Scholar
  10. Hoekstra M, de Weerd FA, Kleerebezem R, van Loosdrecht MCM (2018) Deterioration of the anammox process at decreasing temperatures and long SRTs. Environ Technol, 39, 658, 668Google Scholar
  11. Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J 4:450–454CrossRefPubMedGoogle Scholar
  12. Jetten MSM., Logemann S, Muyzer G, Robertson LA, deVries S, van Loosdrecht MCM, Kuenen JG (1997a) Novel principles in the microbial conversion of nitrogen compounds. Anton Leeuw 71: 75–93Google Scholar
  13. Jetten MSM, Horn SJ, van Loosdrecht MCM (1997b) Towards a more sustainable municipal wastewater treatment system. Water Sci Technol 35:171–180CrossRefGoogle Scholar
  14. Jenni S, Vlaeminck SE, Morgenroth E, Udert KM (2014) Successful application of nitritation/anammox to wastewater with elevated organic carbon to ammonia ratios. Water Res 49:316–326CrossRefPubMedGoogle Scholar
  15. Joss A, Salzgeber D, Eugster J, Konig R, Rottermann K, Burger S, Fabijan P, Leumann S, Mohn J, Siegrist H (2009) Full-scale nitrogen removal from digester liquid with partial nitritation and anammox in one SBR. Environ Sci Technol 43:5301–5306CrossRefPubMedGoogle Scholar
  16. Kalvelage T, Jensen MM, Conteras S, Revsbech NP, Lam P, Gunter M, La Roche J, Lavik G, Kuypers MMM (2011) Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS One 6:e29299CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerstc JA, Damste JS, Jetten MSM, Strous M (2007) CandidatusAnammoxoglobus propionicus” a new propionate-oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49Google Scholar
  18. Kartal B, van Niftrik LA, Rattray J, van deVossenberg J, Schmid MC, Damsté JS, Jetten MSM, Strous M (2008) CandidatusBrocadia fulgida’: an auto fluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63: 46–55Google Scholar
  19. Kartal B, Kuenen JG, van Loosdrecht MCM (2010) Sewage treatment with Anammox. Science 328:702–703CrossRefPubMedGoogle Scholar
  20. Kartal B, Geerts W, Jetten MSM (2011a) Cultivation, detection, and ecophysiology of anaerobic ammonium-oxidizing bacteria. Methods Enzymol 486:89–105CrossRefPubMedGoogle Scholar
  21. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJM, Harhangi HR, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011b) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127–132CrossRefPubMedGoogle Scholar
  22. Kuenen JG (2008) Anammox bacteria: from discovery to application. Nature Rev/Microbiology 6:320–326Google Scholar
  23. Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, Mark CM, van Loosdrecht MCM (2014) Full-scale partial nitritation/anammox experience—an application survey. Water Res 55:292–303CrossRefPubMedGoogle Scholar
  24. Lackner S, Thoma K, Gilbert EM, Wolfgang Gander W, Schreff D, Horn H (2015) Start-up of a full-scale deammonification SBR-treating effluent from digested sludge dewatering. Water Sci Technol 71:553–559CrossRefPubMedGoogle Scholar
  25. Lee KH, Wang YF, Zhang GX, Gu JD (2014) Distribution patterns of ammonia-oxidizing bacteria and anammox bacteria in the freshwater marsh of Honghe wetland in Northeast China. Ecotoxicology 23:1930–1942CrossRefPubMedGoogle Scholar
  26. Lotti T, Kleerebezem R, van Loosdrecht MCM (2015) Effect of temperature change on anammox activity. Biotechnol Bioeng 112:98–103CrossRefPubMedGoogle Scholar
  27. Lotti T, Kleerebezem R, van Erp Taalman Kip C, Hendrickx TLG, Kruit J, Hoekstra M, van Loosdrecht MCM (2014) Anammox growth on pretreated municipal wastewater. Environ Sci Technol 48: 7874–7880Google Scholar
  28. Lotti T, van der Star WRL, Kleerebezem R, Lubello C, van Loosdrecht MCM (2012) The effect of nitrite inhibition on the anammox process. Water Res 46:2559–2569CrossRefPubMedGoogle Scholar
  29. Meng H, Yang Y, Lin JG, Denecke M, Gu JD (2017) Occurrence of anammox bacteria in a traditional full-scale wastewater treatment plant and successful inoculation for new establishment. Int Biodeterior Biodegrad 120:224–231CrossRefGoogle Scholar
  30. Morales N, Val del Rio A, Vazquez-Padin JR, Mendez R, Mosquera-Corral A, Campos JL (2015) Integration of the anammox process to the rejection water and mainstream lines of WWTPs. Chemosphere 140:99–105CrossRefPubMedGoogle Scholar
  31. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141CrossRefPubMedGoogle Scholar
  32. Nnaji CC (2013) A review of the upflow anaerobic sludge blanket reactor. Desalin Water Treat 52(22–24)Google Scholar
  33. Ni SQ, Ni JY, Hu DL, Sung S (2012) Effect of organic matter on the performance of granular anammox process. Bioresour Technol 110:701–705CrossRefPubMedGoogle Scholar
  34. Park G, Takekawa M, Soda S, Ike M, Furukawa K (2017) Temperature dependence of nitrogen removal activity by anammox bacteria enriched at low temperatures. J Biosci Bioeng 123:505–511CrossRefPubMedGoogle Scholar
  35. Pons MN, Spanjers H, Baetens D, Nowak O, Gillot S, Nouwen J, Schuttinga N (2004) Wastewater characteristics in Europe—a survey. Eur Water Manag Online, Official Publication of the European Water Association (EWA), pp. 1–10, www.ewa-online.eu/tl_files/_media/content/documents_pdf
  36. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidizers in soil: The quest for niche specialization and differentiation. Trends Microbiol 20:523–531CrossRefPubMedGoogle Scholar
  37. Oshiki M, Saton H, Okabe S (2016) Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol 18:2784–2796CrossRefPubMedGoogle Scholar
  38. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130–3139CrossRefPubMedGoogle Scholar
  39. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:143–162CrossRefGoogle Scholar
  40. Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S, Revsbech NP (2004) Anaerobic ammonium oxidation in an estuarine sediment. Aquatic Micro Ecol 36:293–304CrossRefGoogle Scholar
  41. Schmidt I, Sliekers O, Schmid M, Bock E, Fuerst J, Kuenen JG, Jetten MSM, Strous M (2003) New concepts of microbial treatment processes for the nitrogen removal in wastewater. FEMS Microbiol Rev 27:481–491CrossRefPubMedGoogle Scholar
  42. Sher Y, Baram S, Dahan O, Ronen Z, Nejidat A (2012) Ammonia transformations and abundance of ammonia oxidizers in a clay soil underlying a manure pond. FEMS Microbiol Ecol 81:145–155CrossRefPubMedGoogle Scholar
  43. Siegrist H, Salzgeber D, Eugster J, Joss A (2008) Anammox brings WWTP closer to energy autarky due to increased biogas production and reduced aeration energy for N-removal. Water Sci Technol 57:383–388CrossRefPubMedGoogle Scholar
  44. Sonthiphand P, Hall MW, Neufeld JD (2014) Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol 5:399.  https://doi.org/10.3389/fmicb.2014.00399 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Strous M, van Gerven E, Kuenen JG, Jetten MSM (1997) Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (anammox) sludge. Appl Environ Microbiol 63:2446–2448PubMedPubMedCentralGoogle Scholar
  46. Strous M, Fuerst JA, Kramer EH, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999a) Missing lithotroph identified as new planctomycete. Nature 400:446–449CrossRefPubMedGoogle Scholar
  47. Strous M, Kuenen JG, Jetten M (1999b) Key physiological parameters of anaerobic ammonium oxidation. Appl Microbiol Biotechnol 65:3248–3250Google Scholar
  48. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molec Biol Evo 24:1596–1599CrossRefGoogle Scholar
  49. Tchobanoglous G, Burton FL, Stensel HD, (2003) Wastewater engineering: treatment and reuse, 4th ed. Metcalf & Eddy, Inc. McGraw-Hill, New York, USAGoogle Scholar
  50. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318CrossRefPubMedPubMedCentralGoogle Scholar
  51. van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON-Anammox process for treatment of ammonium rich wastewater. Water SciTechnol 44:153–160Google Scholar
  52. van Hulle SWH, Vandeweyer HJP, Meesschaert BD, Vanrolleghem PA, Dejans P, Dumoulin A (2010) Engineering aspects and practical application of autotrophic nitrogen removal from nitrogen rich streams. Chem Eng J 162:1–20Google Scholar
  53. Van Lier JB, Mahmoud N, and Zeeman G (2008) Anaerobic wastewater treatment. In: Biological wastewater treatment: principles modelling and design. Edited by: M. Henze, MCM van loosdrecht, GA Ekama and D Brdjanovic. IWA Publishing, London, UKGoogle Scholar
  54. Wang S, Hong Y, Wu J, Xu XR, Bin L, Pan Y, Guan F, Wen J (2015a) Comparative analysis of two 16S rRNA gene-based PCR primer sets provides insight into the diversity distribution patterns of anammox bacteria in different environments. Appl Microbiol Biotechnol 99:8163–8176CrossRefPubMedGoogle Scholar
  55. Wang S, Peng Y, Ma B, Wang S, Zhu G (2015b) Anaerobic ammonium oxidation in traditional municipal wastewater treatment plants with low-strength ammonium loading: widespread but overlooked. Water Res 84:66–75CrossRefPubMedGoogle Scholar
  56. Wett B (2007) Development and implementation of a robust deammonification process. Water Sci Technol 56:81–88CrossRefPubMedGoogle Scholar
  57. Wett B, Omari A, Podmirseg SM, Han M, Akintayo O, Gómez Brandón M, Murthy S, Bott C, Hell M, Takács I, Nyhuis G, O'Shaughnessy M (2013) Going for mainstream deammonification from bench to full scale for maximized resource efficiency. Water Sci Technol 68:283–289CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ali Nejidat
    • 1
  • Damiana Diaz-Reck
    • 1
  • Nedal Massalha
    • 2
  • Adi Arbiv
    • 1
  • Anwar Dawas
    • 3
  • Carlos Dosoretz
    • 3
  • Isam Sabbah
    • 2
    • 4
  1. 1.Department of Environmental Hydrology and Microbiology, Zuckerberg Institute for Water Research, The Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben-GurionIsrael
  2. 2.The Galilee Society Institute of Applied ResearchShefa-AmrIsrael
  3. 3.Division of Environmental, Water and Agricultural Engineering, Faculty of Civil and Environmental EngineeringTechnion - Israel Institute of TechnologyHaifaIsrael
  4. 4.Prof. Ephraim Katzir, Department of Biotechnology EngineeringBraude CollegeKarmielIsrael

Personalised recommendations