Skip to main content
SpringerLink
Log in

Research advances of ammonia oxidation microorganisms in wastewater: metabolic characteristics, microbial community, influencing factors and process applications

  • Critical Review
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Ammonia oxidation carried out by ammonia-oxidizing microorganisms (AOMs) is a central step in the global nitrogen cycle. Aerobic AOMs comprise conventional ammonia-oxidizing bacteria (AOB), novel ammonia-oxidizing archaea (AOA), which could exist in complex and extreme conditions, and complete ammonia oxidizers (comammox), which directly oxidize ammonia to nitrate within a single cell. Anaerobic AOMs mainly comprise anaerobic ammonia-oxidizing bacteria (AnAOB), which can transform NH4+-N and NO2−-N into N2 under anaerobic conditions. In this review, the unique metabolic characteristics, microbial community of AOMs and the influencing factors are discussed. Process applications of nitrification/denitrification, nitritation/denitrification, nitritation/anammox and partial denitrification/anammox in wastewater treatment systems are emphasized. The future development of nitrogen removal processes using AOMs is expected, enrichment of comammox facilitates the complete nitrification performance, inhibiting the activity of comammox and NOB could achieve stable nitritation, and additionally, AnAOB conducting the anammox process in municipal wastewater is a promising development direction.

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

Similar content being viewed by others

Data availability

Data will be made available on request.

References

  1. Monteiro M, Seneca J, Magalhaes C (2014) The history of aerobic ammonia oxidizers: from the first discoveries to today. J Microbiol 52:537–547

    Article  CAS  PubMed  Google Scholar 

  2. Zhao WH, Wang MX, Bai M, Tian ZS, Wang SY, Wang ZW (2022) Nitrogen removal improvement by denitrifying ammonium oxidation in anoxic/oxic-sequence batch biofilm reactor system. J Environ Chem Eng 10:8

    Google Scholar 

  3. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  4. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. van Kessel M, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528:555

    Article  PubMed  PubMed Central  Google Scholar 

  6. Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–183

    Article  CAS  Google Scholar 

  7. Francis CA, Santoro A, Oakley BB, Beman JM, Roberts KJ (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. He SL, Niu QG, Ma HY, Zhang YL, Li YY (2015) The treatment performance and the bacteria preservation of anammox: a review. Water Air Soil Pollut 226:16

    Article  Google Scholar 

  9. Jian-Gong W, Fei X, Jemaneh Z, Bin Z, Sung-Keun R, Zhe-Xue Q (2017) An improved protocol with a highly degenerate primer targeting copper-containing membrane-bound monooxygenase genes for community analysis of methane- and ammonia-oxidizing bacteria. FEMS Microbiol Ecol 93:244

    Article  Google Scholar 

  10. Wang J, Dong H, Wang W, Gu JD (2014) Reverse-transcriptional gene expression of anammox and ammonia-oxidizing archaea and bacteria in soybean and rice paddy soils of Northeast China. Appl Microbiol Biotechnol 98:2675–2686

    Article  CAS  PubMed  Google Scholar 

  11. Zhao W, Bi X, Peng Y, Bai M (2022) Research advances of the phosphorus-accumulating organisms of Candidatus Accumulibacter, Dechloromonas and Tetrasphaera: metabolic mechanisms, applications and influencing factors. Chemosphere 307:135675

    Article  CAS  PubMed  Google Scholar 

  12. Jiang H, Wang Z, Ren S, Qiu JG, Li XY, Peng YZ (2021) Culturing sludge fermentation liquid-driven partial denitrification in two-stage Anammox process to realize advanced nitrogen removal from mature landfill leachate. J Hazard Mater 415:11

    Article  Google Scholar 

  13. Qiu SJ, Liu JJ, Zhang L, Zhang Q, Peng YZ (2021) Sludge fermentation liquid addition attained advanced nitrogen removal in low C/N ratio municipal wastewater through short-cut nitrification-denitrification and partial anammox. Front Environ Sci Eng 15:10

    Article  Google Scholar 

  14. Li JW, Peng YZ, Zhang L, Liu JJ, Wang XD, Gao RT, Pang L, Zhou YX (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 

  15. Head IM, Hiorns WD, Embley TM, Mccarthy AJ, Saunders JR (1993) The phylogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal RNA gene sequences. J Gen Microbiol 139:1147–1153

    Article  CAS  PubMed  Google Scholar 

  16. Zhao WH, Peng YZ, Wang MX, Huang Y, Li XY (2019) Nutrient removal and microbial community structure variation in the two-sludge system treating low carbon/nitrogen domestic wastewater. Biores Technol 294:9

    Article  Google Scholar 

  17. Chen S, Ling J, Blancheton JP (2006) Nitrification kinetics of biofilm as affected by water quality factors. Aquacult Eng 34:179–197

    Article  Google Scholar 

  18. Park HD, Noguera DR (2004) Evaluating the effect of dissolved oxygen on ammonia-oxidizing bacterial communities in activated sludge. Water Res 38:3275–3286

    Article  CAS  PubMed  Google Scholar 

  19. Woese CR, Weisburg WG, Hahn CM, Paster BJ, Zablen LB, Lewis BJ, Macke TJ, Ludwig W, Stackebrandt E (1985) The phylogeny of purple bacteria: the gamma subdivision. Syst Appl Microbiol. https://doi.org/10.1016/S0723-2020(85)80007-2

    Article  PubMed  Google Scholar 

  20. Ye RW, Thomas SM (2001) Microbial nitrogen cycles: physiology, genomics and applications. Curr Opin Microbiol 4:307–312

    Article  CAS  PubMed  Google Scholar 

  21. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  PubMed  Google Scholar 

  22. Gao JF, Luo X, Wu GX, Li T, Peng YZ (2014) Abundance and diversity based on amoA genes of ammonia-oxidizing archaea and bacteria in ten wastewater treatment systems. Appl Microbiol Biotechnol 98:3339–3354

    Article  CAS  PubMed  Google Scholar 

  23. Yasuda T, Waki M, Kuroda K, Hanajima D, Fukumoto Y, Yamagishi T, Suwa Y, Suzuki K (2013) Responses of community structure of amoA-encoding archaea and ammonia-oxidizing bacteria in ammonia biofilter with rockwool mixtures to the gradual increases in ammonium and nitrate. J Appl Microbiol 114:746–761

    Article  CAS  PubMed  Google Scholar 

  24. Sims A, Gajaraj S, Hu ZQ (2012) Seasonal population changes of ammonia-oxidizing organisms and their relationship to water quality in a constructed wetland. Ecol Eng 40:100–107

    Article  Google Scholar 

  25. Zhang T, Wang B, Li XY, Zhang Q, Wu L, He Y, Peng YZ (2018) Achieving partial nitrification in a continuous post- denitrification reactor treating low C/N sewage. Chem Eng J 335:330–337

    Article  CAS  Google Scholar 

  26. Zhang M, Yang Q, Zhang JH, Wang C, Wang SY, Peng YZ (2016) Enhancement of denitrifying phosphorus removal and microbial community of long-term operation in an anaerobic anoxic oxic-biological contact oxidation system. J Biosci Bioeng 122:456–466

    Article  CAS  PubMed  Google Scholar 

  27. Zhao W, Bai M (2022) Upgrading integrated fixed-biofilm activated sludge (IFAS) system into separated two-sludge denitrifying phosphorus removal system: nutrient removal and microbial structure. Chemosphere 307:135918

    Article  CAS  PubMed  Google Scholar 

  28. Zhao WH, Wang MX, Li JW, Huang Y, Li BK, Pan C, Li XY, Peng YZ (2018) Optimization of denitrifying phosphorus removal in a pre-denitrification anaerobic/anoxic/post-aeration plus nitrification sequence batch reactor (pre-A(2)NSBR) system: Nitrate recycling, carbon/nitrogen ratio and carbon source type. Front Environ Sci Eng 12:10

    Article  Google Scholar 

  29. Gatti MN, Gimenez JB, Carretero L, Ruano MV, Borras L, Serralta J, Seco A (2015) Enrichment of AOB and NOB population by applying a BABE reactor in an activated sludge pilot plant. Water Environ Res 87:369–377

    Article  CAS  PubMed  Google Scholar 

  30. Zhang Y, Wang J, Peng S, Zhao D, Miao L (2022) Autotrophic biological nitrogen removal in a bacterial-algal symbiosis system: formation of integrated algae/partial-nitrification/anammox biofilm and metagenomic analysis. Chem Eng J 439:135689

    Article  CAS  Google Scholar 

  31. Hans-Peter K, Andreas PR (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37:1–9

    Article  Google Scholar 

  32. 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

    CAS  PubMed  Google Scholar 

  33. Le LT, Lee S, Bui XT, Jahng D (2020) Suppression of nitrite-oxidizing bacteria under the combined conditions of high free ammonia and low dissolved oxygen concentrations for mainstream partial nitritation. Environ Technol Innov 20:12

    Article  Google Scholar 

  34. Abeling U, Seyfried CF (1992) Anaerobic-aerobic treatment of high-strength ammonium wastewater—nitrogen removal via nitrite. Water Sci Technol 26:1007–1015

    Article  CAS  Google Scholar 

  35. Fitzgerald CM, Comejo P, Oshlag JZ, Noguera DR (2015) Ammonia-oxidizing microbial communities in reactors with efficient nitrification at low-dissolved oxygen. Water Res 70:38–51

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  37. Tokutomi T (2004) Operation of a nitrite-type airlift reactor at low DO concentration. Water Sci Technol 49:81

    Article  CAS  PubMed  Google Scholar 

  38. Groeneweg J, Sellner B, Tappe W (1994) Ammonia oxidation in nitrosomonas at NH 3 concentrations near km: effects of pH and temperature. Water Res 28:2561–2566

    Article  Google Scholar 

  39. Laanbroek HJ, Bodelier P, Gerards S (1994) Oxygen consumption kinetics of Nitrosomonas europaea and Nitrobacter hamburgensis grown in mixed continuous cultures at different oxygen concentrations. Arch Microbiol 161:156–162

    Article  CAS  Google Scholar 

  40. 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 

  41. Khin T, Annachhatre AP (2004) Novel microbial nitrogen removal processes. Biotechnol Adv 22:519–532

    Article  CAS  PubMed  Google Scholar 

  42. Lopez-Palau S, Sancho I, Pinto A, Dosta J, Mata-Alvarez J (2013) Influence of temperature on the partial nitritation of reject water in a Granular Sequencing Batch Reactor. Environ Technol 34:2625–2632

    Article  CAS  PubMed  Google Scholar 

  43. Yoo H, Ahn KH, Lee HJ, Lee KH, Kwak YJ, Song KG (1999) Nitrogen removal from synthetic wastewater by simultaneous nitrification and denitrification (SND) via nitrite in an intermittently-aerated reactor. Water Res 33:145–154

    Article  CAS  Google Scholar 

  44. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W (2004) Environmental Genome Shotgun Sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  45. Hallam S, Mincer T, Schleper C, Preston C, Roberts K, Richardson P, Delong E (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine crenarchaeota. PLoS Biol 4:520–536

    Article  CAS  Google Scholar 

  46. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  CAS  PubMed  Google Scholar 

  47. Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660

    Article  PubMed  Google Scholar 

  48. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 105:2134–2139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. French E, Kozlowski JA, Mukherjee M, Bullerjahn G, Bollmann A (2012) Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl Environ Microbiol 78:5773–5780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079

    Article  CAS  PubMed  Google Scholar 

  52. Bai YH, Sun QH, Wen DH, Tang XY (2012) Abundance of ammonia-oxidizing bacteria and archaea in industrial and domestic wastewater treatment systems. FEMS Microbiol Ecol 80:323–330

    Article  CAS  PubMed  Google Scholar 

  53. Wells GF, Park HD, Yeung CH, Eggleston B, Francis CA, Criddle CS (2009) Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ Microbiol 11:2310–2328

    Article  CAS  PubMed  Google Scholar 

  54. Park HD, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Zhang T, Jin T, Yan Q, Shao M, Wells G, Criddle C, Fang HHP (2009) Occurrence of ammonia-oxidizing Archaea in activated sludges of a laboratory scale reactor and two wastewater treatment plants. J Appl Microbiol 107:970–977

    Article  CAS  PubMed  Google Scholar 

  56. Herrmann M, Saunders AM, Schramm A (2009) Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl Environ Microbiol 75:3127–3136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976-U234

    Article  CAS  PubMed  Google Scholar 

  58. Hugoni M, Etien S, Bourges A, Lepere C, Domaizon I, Mallet C, Bronner G, Debroas D, Mary I (2013) Dynamics of ammonia-oxidizing Archaea and Bacteria in contrasted freshwater ecosystems. Res Microbiol 164:360–370

    Article  CAS  PubMed  Google Scholar 

  59. Lu L, Jia ZJ (2013) Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environ Microbiol 15:1795–1809

    Article  CAS  PubMed  Google Scholar 

  60. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

    Article  CAS  PubMed  Google Scholar 

  61. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510

    Article  CAS  PubMed  Google Scholar 

  62. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797

    Article  CAS  PubMed  Google Scholar 

  63. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    Article  CAS  PubMed  Google Scholar 

  64. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174

    Article  CAS  PubMed  Google Scholar 

  65. Zhang CL, Ye Q, Huang ZY, Li WJ, Chen JQ, Song ZQ, Zhao WD, Bagwell C, Inskeep WP, Ross C, Gao L, Wiegel J, Romanek CS, Shock EL, Hedlund BP (2008) Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl Environ Microbiol 74:6417–6426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Xia WW, Zhang CX, Zeng XW, Feng YZ, Weng JH, Lin XG, Zhu JG, Xiong ZQ, Xu J, Cai ZC, Jia ZJ (2011) Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5:1226–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Costa E, Pérez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219

    Article  CAS  PubMed  Google Scholar 

  68. Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel M, Daebeler A, Steinberger M, Jetten MSM, Lucker S, Wagner M, Daims H (2017) AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox nitrospira in the environment. Front Microbiol 8:11

    Article  Google Scholar 

  69. Palomo A, Pedersen AG, Fowler SJ, Dechesne A, Sicheritz-Ponten T, Smets BF (2018) Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J 12:1779–1793

    Article  PubMed  PubMed Central  Google Scholar 

  70. Xia F, Wang JG, Zhu T, Zou B, Rhee SK, Quan ZX (2018) Ubiquity and diversity of complete ammonia oxidizers (Comammox). Appl Environ Microbiol 84:14

    Article  Google Scholar 

  71. Roots P, Wang YB, Rosenthal AF, Griffin JS, Sabba F, Petrovich M, Yang FH, Kozak JA, Zhang H, Wells GF (2019) Comammox Nitrospira are the dominant ammonia oxidizers in a mainstream low dissolved oxygen nitrification reactor. Water Res 157:396–405

    Article  CAS  PubMed  Google Scholar 

  72. Spasov E, Tsuji JM, Hug LA, Doxey AC, Sauder LA, Parker WJ, Neufeld JD (2020) High functional diversity among Nitrospira populations that dominate rotating biological contactor microbial communities in a municipal wastewater treatment plant. ISME J 14:1857–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Wang MY, Huang GH, Zhao ZR, Dang CY, Liu W, Zheng MS (2018) Newly designed primer pair revealed dominant and diverse comammox amoA gene in full-scale wastewater treatment plants. Biores Technol 270:580–587

    Article  CAS  Google Scholar 

  74. Cotto I, Dai ZH, Huo LX, Anderson CL, Vilardi KJ, Ijaz U, Khunjar W, Wilson C, De Clippeleir H, Gilmore K, Bailey E, Pinto AJ (2020) Long solids retention times and attached growth phase favor prevalence of comammox bacteria in nitrogen removal systems. Water Res 169:15

    Article  Google Scholar 

  75. Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549:269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Fowler SJ, Palomo A, Dechesne A, Mines PD, Smets BF (2018) Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environ Microbiol 20:1002–1015

    Article  CAS  PubMed  Google Scholar 

  77. Camejo PY, Santo Domingo J, Mcmahon KD, Noguera DR, Summers ZM (2017) Genome-Enabled Insights into the Ecophysiology of the Comammox Bacterium “Candidatus Nitrospira nitrosa.” mSystems 2:e00059-00017

    Article  Google Scholar 

  78. Broda E (1977) Two kinds of lithotrophs missing in nature. Ztschrift Fur Allgemne Mikrobiologie 17:491–493

    Article  CAS  Google Scholar 

  79. Jetten M, Wagner M, Fuerst J, Loosdrecht MV, Strous M (2001) Microbiology and application of the anaerobic ammonium oxidation ('anammox’) process. Curr Opin Biotechnol 12:283–288

    Article  CAS  PubMed  Google Scholar 

  80. Karlsson R, Karlsson A, Backman O, Johansson BR, Hulth S (2009) Identification of key proteins involved in the anammox reaction. FEMS Microbiol Lett 297:87–94

    Article  CAS  PubMed  Google Scholar 

  81. 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 440:790–794

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  83. Jia FX, Peng YZ, Li JW, Li XY, Yao H (2021) Metagenomic prediction analysis of microbial aggregation in anammox-dominated community. Water Environ Res 93:2549–2558

    Article  CAS  PubMed  Google Scholar 

  84. 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 

  85. Wu GX, Zhang TQ, Gu MQ, Chen Z, Yin QD (2020) Review of characteristics of anammox bacteria and strategies for anammox start-up for sustainable wastewater resource management. Water Sci Technol 82:1742–1757

    Article  CAS  PubMed  Google Scholar 

  86. Wang SY, Peng YZ, Ma B, Wang SY, Zhu GB (2015) Anaerobic ammonium oxidation in traditional municipal wastewater treatment plants with low-strength ammonium loading: Widespread but overlooked. Water Res 84:66–75

    Article  CAS  PubMed  Google Scholar 

  87. 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. Biores Technol 271:150–158

    Article  CAS  Google Scholar 

  88. Dapena-Mora A, Fernández I, Campos JL, Mosquera-Corral A, Méndez R, Jetten M (2007) Evaluation of activity and inhibition effects on Anammox process by batch tests based on the nitrogen gas production. Enzyme Microb Technol 40:859–865

    Article  CAS  Google Scholar 

  89. Huang DQ, Fu JJ, Li ZY, Fan NS, Jin RC (2022) Inhibition of wastewater pollutants on the anammox process: a review. Sci Total Environ 803:12

    Article  Google Scholar 

  90. Jin RC, Xing BS, Yu JJ, Qin TY, Chen SX (2013) The importance of the substrate ratio in the operation of the Anammox process in upflow biofilter. Ecol Eng 53:130–137

    Article  Google Scholar 

  91. Strous MM, Kuenen J, Jetten M (1999) Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol 65:3248–3250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Awata T, Goto Y, Kindaichi T, Ozaki N, Ohashi A (2015) Nitrogen removal using an anammox membrane bioreactor at low temperature. Water Sci Technol 72:2148–2153

    Article  CAS  PubMed  Google Scholar 

  93. Lin XM, Wang YY, Ma X, Yan Y, Wu M, Bond PL, Guo JH (2018) Evidence of differential adaptation to decreased temperature by anammox bacteria. Environ Microbiol 20:3514–3528

    Article  CAS  PubMed  Google Scholar 

  94. Dosta J, Fernandez I, 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 154:688–693

    Article  CAS  PubMed  Google Scholar 

  95. Fu LL, Chen YY, Li SQ, He H, Mi TZ, Zhen Y, Yu ZG (2019) Shifts in the anammox bacterial community structure and abundance in sediments from the Changjiang Estuary and its adjacent area. Syst Appl Microbiol 42:383–396

    Article  CAS  PubMed  Google Scholar 

  96. Strous M, Gerven EV, Kuenen JG, Jetten M (1997) Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (anammox) sludge. Appl Environ Microbiol. https://doi.org/10.1128/aem.63.6.2446-2448.1997

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  98. Miao L, Yang GQ, Tao T, Peng YZ (2019) Recent advances in nitrogen removal from landfill leachate using biological treatments—a review. J Environ Manag 235:178–185

    Article  CAS  Google Scholar 

  99. Zhang L, Jiang L, Zhang JT, Li JL, Peng YZ (2022) Enhancing nitrogen removal through directly integrating anammox into mainstream wastewater treatment: advantageous, issues and future study. Biores Technol 362:7

    Article  Google Scholar 

  100. Wang Q, He J (2022) Partnering of anammox and denitrifying bacteria benefits anammox’s recovery from starvation and complete nitrogen removal. Sci Total Environ 815:152696

    Article  CAS  PubMed  Google Scholar 

  101. Feng Y, Luo SP, Zhang YX, Wang SY, Peng YZ (2022) Enhanced nutrient removal from mainstream sewage via denitrifying dephosphatation, endogenous denitrification and anammox in a novel continuous flow process. Biores Technol 351:9

    Article  Google Scholar 

  102. Song T, Zhang X, Li J, Wu X, Feng H, Dong W (2021) A review of research progress of heterotrophic nitrification and aerobic denitrification microorganisms (HNADMs). Sci Total Environ 801:149319

    Article  CAS  PubMed  Google Scholar 

  103. Zhao Y, Li J, Liu Q, Qi Z, Li X, Zhang Q, Sui J, Wang C, Peng Y (2023) Fast start-up and stable operation of mainstream anammox without inoculation in an A2/O process treating low COD/N real municipal wastewater. Water Res 231:119598

    Article  CAS  PubMed  Google Scholar 

  104. Henze M, Loosdrecht M, Ekama GA, Brdjanovic D (2008) Wastewater treatment development. Modern Chem Ind 29:66–69

    Google Scholar 

  105. He QL, Song Q, Zhang SL, Zhang W, Wang HY (2018) Simultaneous nitrification, denitrification and phosphorus removal in an aerobic granular sequencing batch reactor with mixed carbon sources: reactor performance, extracellular polymeric substances and microbial successions. Chem Eng J 331:841–849

    Article  CAS  Google Scholar 

  106. Zhao WH, Zhang Y, Lv PM, Wang MX, Peng YZ, Li BK (2016) Advanced nitrogen and phosphorus removal in the pre-denitrification anaerobic/anoxic/aerobic nitrification sequence batch reactor (pre-A(2)NSBR) treating low carbon/nitrogen (C/N) wastewater. Chem Eng J 302:296–304

    Article  CAS  Google Scholar 

  107. Xu ZS, Dai XH, Chai XL (2018) Effect of different carbon sources on denitrification performance, microbial community structure and denitrification genes. Sci Total Environ 634:195–204

    Article  CAS  PubMed  Google Scholar 

  108. Seifi M, Fazaelipoor MH (2012) Modeling simultaneous nitrification and denitrification (SND) in a fluidized bed biofilm reactor. Appl Math Model 36:5603–5613

    Article  Google Scholar 

  109. Zhao WH, Huang Y, Wang MX, Pan C, Li XY, Peng YZ, Li BK (2018) Post-endogenous denitrification and phosphorus removal in an alternating anaerobic/oxic/anoxic (AOA) system treating low carbon/nitrogen (C/N) domestic wastewater (vol 339, pg 450, 2018). Chem Eng J 394:1

    Google Scholar 

  110. Layer M, Villodres MG, Hernandez A, Reynaert E, Morgenroth E, Derlon N (2020) Limited simultaneous nitrification-denitrification (SND) in aerobic granular sludge systems treating municipal wastewater: mechanisms and practical implications. Water Res X 7:13

    Article  Google Scholar 

  111. Liu T, Li Q, Wu N, Quan X (2022) Enhancing the formation of simultaneous nitrification and denitrification (SND) biofilm and nitrogen removal performance using two-units IFFAS process filled with surface-modified carriers. Biochem Eng J 179:10

    Article  Google Scholar 

  112. Zhao W, Bai M (2022) Advanced nutrient removal and functional microorganism enrichment in AOA system reinforced by side-stream sludge fermentation. J Environ Chem Eng 10:108487

    Article  CAS  Google Scholar 

  113. 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 

  114. Ge SJ, Wang SY, Yang X, Qiu S, Li BK, Peng YZ (2015) Detection of nitrifiers and evaluation of partial nitrification for wastewater treatment: a review. Chemosphere 140:85–98

    Article  CAS  PubMed  Google Scholar 

  115. Peng YZ, Guo JH, Horn H, Yang X, Wang SY (2012) Achieving nitrite accumulation in a continuous system treating low-strength domestic wastewater: switchover from batch start-up to continuous operation with process control. Appl Microbiol Biotechnol 94:517–526

    Article  CAS  PubMed  Google Scholar 

  116. Xiao J, Tang JH (2014) Nitrogen removal with nitrification and denitrification via nitrite. Adv Mater Res 908:175–178

    Article  CAS  Google Scholar 

  117. Miao YY, Zhang L, Yu DS, Zhang JH, Zhang WK, Ma GC, Zhao XC, Peng YZ (2022) Application of intermittent aeration in nitrogen removal process: development, advantages and mechanisms. Chem Eng J 430:11

    Article  Google Scholar 

  118. Gabarro J, Ganigue R, Gich F, Ruscalleda M, Balaguer MD, Colprim J (2012) Effect of temperature on AOB activity of a partial nitritation SBR treating landfill leachate with extremely high nitrogen concentration. Biores Technol 126:283–289

    Article  CAS  Google Scholar 

  119. Wang QL, Ye L, Jiang GM, Hu SH, Yuan ZG (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 

  120. Bin Ma, Shanyun W, Shenbin C, Yuanyuan M, Fangxu J (2016) Biological nitrogen removal from sewage via anammox: recent advances. Biores Technol 200:981–990

    Article  Google Scholar 

  121. Terada A, Zhou S, Hosomi M (2011) Presence and detection of anaerobic ammonium-oxidizing (anammox) bacteria and appraisal of anammox process for high-strength nitrogenous wastewater treatment: a review. Clean Technol Environ Policy 13:759–781

    Article  CAS  Google Scholar 

  122. Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303

    Article  CAS  PubMed  Google Scholar 

  123. Li J, Du Q, Peng H, Zhang Y, Liu T (2020) Optimization of biochemical oxygen demand to total nitrogen ratio for treating landfill leachate in a single-stage partial nitrification-denitrification system. J Clean Prod 266:121809

    Article  CAS  Google Scholar 

  124. van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, van Loosdrecht MCM (2010) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam (vol 41, pg 18, 2007). Water Res 44:1025–1025

    Article  Google Scholar 

  125. Miao YY, Zhang L, Li BK, Zhang Q, Wang SM, Peng YZ (2017) Enhancing ammonium oxidizing bacteria activity was key to single-stage partial nitrification-anammox system treating low-strength sewage under intermittent aeration condition. Biores Technol 231:36–44

    Article  CAS  Google Scholar 

  126. Zhang J, Zhang Q, Li X, Miao Y, Sun Y, Zhang M, Peng Y (2017) Rapid start-up of partial nitritation and simultaneously phosphorus removal (PNSPR) granular sludge reactor treating low-strength domestic sewage. Bioresour Technol 243:660–666

    Article  CAS  PubMed  Google Scholar 

  127. Wang H, Zhang L, Dan Q, Zhang Y, Wang S, Zhang Q, Li X, Wang C, Peng Y (2023) Ultra-high nitrogen removal from real municipal wastewater using selective enhancement of glycogen accumulating organisms (GAOs) in a partial nitrification-anammox (PNA) system. Water Res 230:119594

    Article  CAS  PubMed  Google Scholar 

  128. Wett B, Podmirseg SM, Gomez-Brandon M, Hell M, Nyhuis G, Bott C, Murthy S (2015) Expanding DEMON sidestream deammonification technology towards mainstream application. Water Environ Res 87:2084–2089

    Article  CAS  PubMed  Google Scholar 

  129. Du R, Peng Y, Cao S, Wang S, Wu C (2015) Advanced nitrogen removal from wastewater by combining anammox with partial denitrification. Bioresour Technol 179:497–504

    Article  CAS  PubMed  Google Scholar 

  130. Wett B (2007) Development and implementation of a robust deammonification process. Water Sci Technol. https://doi.org/10.2166/wst.2007.611

    Article  PubMed  Google Scholar 

  131. Ma B, Qian WT, Yuan CS, Yuan ZG, Peng YZ (2017) Achieving mainstream nitrogen removal through coupling anammox with denitratation. Environ Sci Technol 51:8405–8413

    Article  CAS  PubMed  Google Scholar 

  132. Zhang XC, Miao YY, Yu DS, Qiu YL, Zhao J, Wang XX (2022) Culturing partial denitrification biofilm in side stream incubator with ordinary activated sludge as inoculum: one step closer to mainstream anammox upgrade. Biores Technol 347:126679

    Article  CAS  Google Scholar 

  133. Cao S, Wang S, Peng Y, Wu C, Du R, Gong L, Ma B (2013) Achieving partial denitrification with sludge fermentation liquid as carbon source: the effect of seeding sludge. Biores Technol 149:570–574

    Article  CAS  Google Scholar 

  134. Ma JM, Cao RR, Dang YL, Wang JL (2021) A recent progress of room-temperature airborne ozone decomposition catalysts. Chin Chem Lett 32:2985–2993

    Article  CAS  Google Scholar 

  135. Wang Q, He J (2020) Complete nitrogen removal via simultaneous nitrification and denitrification by a novel phosphate accumulating Thauera sp. strain SND5. Water Res 185:116300

    Article  CAS  PubMed  Google Scholar 

  136. Li X, Shi M, Zhang M, Li W, Xu PL, Wang YY, Yuan Y, Huang Y (2022) Progresses and challenges in sulfur autotrophic denitrification-enhanced Anammox for low carbon and efficient nitrogen removal. Crit Rev Environ Sci Technol 52:4379–4394

    Article  CAS  Google Scholar 

  137. He Z, Kan JJ, Wang YB, Huang YL, Mansfeld F, Nealson KH (2009) Electricity production coupled to ammonium in a microbial fuel cell. Environ Sci Technol 43:3391–3397

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant number: 52200063) and the Natural Science Foundation of Shandong Province, China (grant number ZR2020QE230).

Author information

Authors and Affiliations

  1. State and Local Joint Engineering Research Center of Municipal Wastewater Treatment and Resource Recycling, Qingdao University of Technology, Qingdao, 266033, People’s Republic of China

    Weihua Zhao, Xuejun Bi, Meng Bai & Yanyan Wang

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

    Weihua Zhao

  3. Qingdao University of Technology, Huangdao District, Qingdao, 266525, 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. Xuejun Bi
    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

  4. Yanyan Wang
    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 that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 150 KB)

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., Bi, X., Bai, M. et al. Research advances of ammonia oxidation microorganisms in wastewater: metabolic characteristics, microbial community, influencing factors and process applications. Bioprocess Biosyst Eng 46, 621–633 (2023). https://doi.org/10.1007/s00449-023-02866-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-023-02866-5

Keywords

Search

Navigation