Skip to main content
SpringerLink
Log in

Nitrogen removal enhancement reinforced by nitritation/anammox in an anaerobic/oxic/anoxic system with integrated fixed biofilm activated sludge

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

The enhancement of nitrogen removal was reinforced by nitritation/anammox in an anaerobic/oxic/anoxic (AOA) system of integrated fixed biofilm activated sludge. Nitritation was first attained by the method of free nitrous acid (FNA) inhibition with ammonia residues, and anaerobic ammonia oxidizing bacteria (AnAOB) were then added into the system, which enabled the occurrence of nitritation coupled with anaerobic ammonia oxidation (anammox). The results indicated that nitrogen removal was enhanced by the nitritation/anammox pathway with an efficiency of 88.9%. A microbial analysis showed that the ammonia oxidizing bacterium (AOB) Nitrosomonas was enriched on the biofilm (5.98%) and in the activated sludge (2.40%), and the AnAOB Candidatus Brocadia was detected on the biofilm with a proportion of 0.27%. Nitritation/anammox was attained and maintained due to the accumulation of functional bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data will be made available on request.

References

  1. Gurung K, Tang WZ, Sillanpää M (2018) Unit energy consumption as benchmark to select energy positive retrofitting strategies for Finnish wastewater treatment plants (WWTPs): a case study of Mikkeli WWTP. Environ Process 5:667–681

    Article  CAS  Google Scholar 

  2. Vaccari M, Foladori P, Nembrini S, Vitali F (2018) Benchmarking of energy consumption in municipal wastewater treatment plants—a survey of over 200 plants in Italy. Water Sci Technol 77:2242–2252

    Article  CAS  PubMed  Google Scholar 

  3. Zhao W, Huang Y, Wang M, Pan C, Li X, Peng Y, Li B (2018) Post-endogenous denitrification and phosphorus removal in an alternating anaerobic/oxic/anoxic (AOA) system treating low carbon/nitrogen (C/N) domestic wastewater. Chem Eng J 339:450–458

    Article  CAS  Google Scholar 

  4. Zhao W, Wang M, Li J, Yu H, Li B (2018) Optimization of denitrifying phosphorus removal in a pre-denitrification anaerobic/anoxic/post-aeration+ nitrification sequence batch reactor (pre-A2NSBR) system: nitrate recycling, carbon/nitrogen ratio and carbon source type. Front Environ Sci Eng 12:81–810

    Article  Google Scholar 

  5. Yang Q, Peng YZ, Liu XH, Zeng W, Mino T, Satoh H (2007) Nitrogen removal via nitrite from municipal wastewater at low temperatures using real-time control to optimize nitrifying communities. Environ Sci Technol 41:8159–8164

    Article  CAS  PubMed  Google Scholar 

  6. Ma B, Wang S, Cao S, Miao Y, Jia F, Du R, Peng Y (2016) Biological nitrogen removal from sewage via anammox: recent advances. Bioresour Technol 200:981–990

    Article  CAS  PubMed  Google Scholar 

  7. Van de Graaf AAV (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61:1246–1251

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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 57:383–388

    Article  CAS  PubMed  Google Scholar 

  9. Kartal B, Kuenen JG, Loosdrecht M (2010) Sewage treatment with anammox. Science 328:702–703

    Article  CAS  PubMed  Google Scholar 

  10. Molinuevo B, García M, Karakashev D, Angelidaki I (2009) Anammox for ammonia removal from pig manure effluents: effect of organic matter content on process performance. Bioresour Technol 99:2171–2175

    Article  Google Scholar 

  11. Xh A, Sz B, Sy C, Liang ZC, Ypa C (2020) Full-scale partial nitritation/anammox (PN/A) process for treating sludge dewatering liquor from anaerobic digestion after thermal hydrolysis. Bioresour Technol 297:122380

    Article  Google Scholar 

  12. Li J, Peng Y, Zhang L, Liu J, Wang X, Gao R, Pang L, Zhou Y (2019) Quantify the contribution of anammox for enhanced nitrogen removal through metagenomic analysis and mass balance in an anoxic moving bed biofilm reactor. Water Res 160:178–187

    Article  CAS  PubMed  Google Scholar 

  13. Miao Y, Zhang L, Yu D, Zhang J, Zhang W, Ma G, Zhao X, Peng Y (2022) Application of intermittent aeration in nitrogen removal process: development, advantages and mechanisms. Chem Eng J 430:133184

    Article  CAS  Google Scholar 

  14. Zhao W, Peng Y, Wang M, Huang Y, Li X (2019) Nutrient removal and microbial community structure variation in the two-sludge system treating low carbon/nitrogen domestic wastewater. Bioresour Technol 294:122161

    Article  CAS  PubMed  Google Scholar 

  15. AHS, BHC, CWT, DXZ, BHY, AFZ, AYZ (2021) Effects of influent immigration and environmental factors on bacterial assembly of activated sludge microbial communities

  16. Zhao W, Wang M, Bai M, Tian Z, Wang S, Wang Z (2022) Nitrogen removal improvement by denitrifying ammonium oxidation in anoxic/oxic-sequence batch biofilm reactor system. J Environ Chem Eng 10:107022

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  18. Vadivelu VM, Keller J, Yuan Z (2007) Free ammonia and free nitrous acid inhibition on the anabolic and catabolic processes of nitrosomonas and nitrobacter. Water Sci Technol 56:89–97

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  20. Wang Q, Ye L, Jiang G, Hu S, Yuan Z (2014) Side-stream sludge treatment using free nitrous acid selectively eliminates nitrite oxidizing bacteria and achieves the nitrite pathway. Water Res 55:245–255

    Article  CAS  PubMed  Google Scholar 

  21. Vadivelu VM, Yuan Z, Fux C, Keller J (2006) The inhibitory effects of free nitrous acid on the energy generation and growth processes of an enriched nitrobacter culture. Environ Sci Technol 40:4442–4448

    Article  CAS  PubMed  Google Scholar 

  22. Chen YZ, Peng CY, Wang JH, Ye L, Zhang LC, Peng YZ (2011) Effect of nitrate recycling ratio on simultaneous biological nutrient removal in a novel anaerobic/anoxic/oxic (A(2)/O)-biological aerated filter (BAF) system. Bioresour Technol 102:5722–5727

    Article  CAS  PubMed  Google Scholar 

  23. Wang X, Wang S, Xue T, Li B, Dai X, Peng Y (2015) Treating low carbon/nitrogen (C/N) wastewater in simultaneous nitrification-endogenous denitrification and phosphorous removal (SNDPR) systems by strengthening anaerobic intracellular carbon storage. Water Res 77:191–200

    Article  CAS  PubMed  Google Scholar 

  24. AJW, ACH, BMCMVL, bJP (2016) Selection of ammonium oxidizing bacteria (AOB) over nitrite oxidizing bacteria (NOB) based on conversion rates. Chem Eng J 304:953–961

  25. Jin P, Li B, Mu D, Li X, Peng Y (2019) High-efficient nitrogen removal from municipal wastewater via two-stage nitritation/anammox process: long-term stability assessment and mechanism analysis. Bioresour Technol 271:150–158

    Article  CAS  PubMed  Google Scholar 

  26. Miao Y, Zhang L, Li B, Zhang Q, Wang S, Peng Y (2017) Enhancing ammonium oxidizing bacteria activity was key to single-stage partial nitrification-anammox system treating low-strength sewage under intermittent aeration condition. Bioresour Technol 231:36–44

    Article  CAS  PubMed  Google Scholar 

  27. Regmi P, Miller MW, Holgate B, Bunce R, Park H, Chandran K, Wett B, Murthy S, Bott CB (2014) Control of aeration, aerobic SRT and COD input for mainstream nitritation/denitritation. Water Res 57:162–171

    Article  CAS  PubMed  Google Scholar 

  28. Poot V, Hoekstra M, Geleijnse MAA, Loosdrecht MV, Pérez J (2016) Effects of the residual ammonium concentration on NOB repression during partial nitritation with granular sludge. Water Res 106:518–530

    Article  CAS  PubMed  Google Scholar 

  29. Qiao S, Yamamoto T, Misaka M, Isaka K, Sumino T, Bhatti Z, Furukawa K (2010) High-rate nitrogen removal from livestock manure digester liquor by combined partial nitritation–anammox process. Biodegradation 21:11

    Article  PubMed  Google Scholar 

  30. Zhao W, Zhang Y, Lv D, Wang M, Peng Y, Li B (2016) Advanced nitrogen and phosphorus removal in the pre-denitrification anaerobic/anoxic/aerobic nitrification sequence batch reactor (pre-A2NSBR) treating low carbon/nitrogen (C/N) wastewater. Chem Eng J 302:296–304

    Article  CAS  Google Scholar 

  31. Ye L, Shao MF, Tong Z, Tong A, Si L (2011) Analysis of the bacterial community in a laboratory-scale nitrification reactor and a wastewater treatment plant by 454-pyrosequencing. Water Res 45:4390–4398

    Article  CAS  PubMed  Google Scholar 

  32. Muszyński A, Tabernacka A, Miłobędzka A (2015) Long-term dynamics of the microbial community in a full-scale wastewater treatment plant. Int Biodeterior Biodegrad 100:44–51

    Article  Google Scholar 

  33. Miura Y, Watanabe Y, Okabe S (2007) Significance of chloroflexi in performance of submerged membrane bioreactors (MBR) treating municipal wastewater. Environ Sci Technol 41:7787–7794

    Article  CAS  PubMed  Google Scholar 

  34. Wang Y, Ye J, Ju F, Liu L, Boyd JA, Deng Y, Parks DH, Jiang X, Yin X, Woodcroft BJ, Tyson GW, Hugenholtz P, Polz MF, Zhang T (2021) Successional dynamics and alternative stable states in a saline activated sludge microbial community over 9 years. Microbiome 9:199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Goodfellow M, Kampfer P, Busse H-J, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (2012) Bergey’s manual of systematic bacteriology. Springer, New York. https://doi.org/10.1007/978-0-387-68233-4

    Book  Google Scholar 

  36. Pereira AD, Cabezas A, Etchebehere C, Chernicharo CADL, Araujo JCD (2017) Microbial communities in anammox reactors: a review. Environ Technol Rev 6:74–93

    Article  CAS  Google Scholar 

  37. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93–106

    Article  CAS  PubMed  Google Scholar 

  38. Hu BL, Ping Z, Tang CJ, Chen JW, Biezen E, Lei Z, Ni BJ, Jetten M, Jia Y, Yu HQ (2010) Identification and quantification of anammox bacteria in eight nitrogen removal reactors. Water Res 44:5014–5020

    Article  CAS  PubMed  Google Scholar 

  39. Araujo JC, Campos AC, Correa MM, Silva EC, Chernicharo C (2011) Anammox bacteria enrichment and characterization from municipal activated sludge. Water Sci Technol 64:1428

    Article  CAS  PubMed  Google Scholar 

  40. Kartal B, Kuypers M, Lavik G, Schalk J, Camp H, Jetten M, Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ Microbiol 9:635–642

    Article  CAS  PubMed  Google Scholar 

  41. Mark CM, van Loosdrecht H, Horn EM, Gilbert A (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303

    Article  Google Scholar 

  42. Chen G, Zhang Y, Wang X, Chen F, Lin L, Ruan Q, Wang Y, Wang F, Cao W, Chiang P (2020) Optimizing of operation strategies of the single-stage partial nitrification-anammox process. J Clean Prod 256:120667

    Article  CAS  Google Scholar 

  43. Wett B (2006) Solved upscaling problems for implementing deammonification of rejection water. Water Sci Technol 53:121–128

    Article  CAS  PubMed  Google Scholar 

  44. Joss A, Salzgeber DV, Eugster J, Koenig 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 43:5301–5306

    Article  CAS  PubMed  Google Scholar 

  45. Pérez J, Lotti T, Kleerebezem R, Picioreanu C, Loosdrecht MCMV (2014) Outcompeting nitrite-oxidizing bacteria in single-stage nitrogen removal in sewage treatment plants: a model-based study. Water Res 66C:208–218

    Article  Google Scholar 

  46. Hellinga C, Schellen A, Mulder JW, Van LMCM, Heijnen JJ (1998) The SHARON process: an innovative method for nitrogen removal from ammonium-rich waste water. Water Sci Technol 37:135–142

    Article  CAS  Google Scholar 

  47. Hulle SWV, Volcke EI, Teruel JL, Donckels B, Loosdrecht MCV, Vanrolleghem PA (2007) Influence of temperature and pH on the kinetics of the Sharon nitritation process. J Chem Technol Biotechnol 82:471–480

    Article  Google Scholar 

  48. Cao Y, van Loosdrecht MC, Daigger GT (2017) Mainstream partial nitritation-anammox in municipal wastewater treatment: status, bottlenecks, and further studies. Appl Microbiol Biotechnol 101:1365–1383

    Article  CAS  PubMed  Google Scholar 

  49. Zhao W, Bi X, Bai M et al (2023) Research advances of ammonia oxidation microorganisms in wastewater: metabolic characteristics, microbial community, influencing factors and process applications. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-023-02866-

    Article  PubMed  Google Scholar 

  50. Weihua Z, Meng B (2022) Upgrading integrated fixed-biofilm activated sludge (IFAS) system into separated two-sludge denitrifying phosphorus removal system: Nutrient removal and microbial structure. Chemosphere 307(3):135918

    Google Scholar 

  51. Weihua Z, Xuejun B, Yongzhen P, Meng B (2022) Research advances of the phosphorus-accumulating organisms of candidatus accumulibacter, dechloromonas and tetrasphaera: metabolic mechanisms, applications and influencing factors. Chemosphere 307(1):135675

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of Shandong Province, China (Grant Number ZR2020QE230).

Author information

Authors and Affiliations

  1. School of Environmental and Municipal Engineering, Qingdao University of Technology, Huangdao District, Qingdao, 266525, People’s Republic of China

    Weihua Zhao, Yanyan Wang & Meng Bai

  2. School of Marine Science and Technology, Harbin Institute of Technology, Weihai, 264209, People’s Republic of China

    Weihua Zhao

Authors
  1. Weihua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Weihua Zhao.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, W., Wang, Y. & Bai, M. Nitrogen removal enhancement reinforced by nitritation/anammox in an anaerobic/oxic/anoxic system with integrated fixed biofilm activated sludge. Bioprocess Biosyst Eng 46, 1065–1073 (2023). https://doi.org/10.1007/s00449-023-02885-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-023-02885-2

Keywords

Search

Navigation