Overlooked nitrogen-cycling microorganisms in biological wastewater treatment

Highlights

• AOA and comammox bacteria can be more abundant and active than AOB/NOB at WWTPs.

• Coupled DNRA/anammox and NO_x-DAMO/anammox/comammox processes are demonstrated.

• Substrate level, SRT and stressors determine the niches of overlooked microbes.

• Applications of overlooked microbes in enhancing nitrogen removal are promising.

Abstract

Nitrogen-cycling microorganisms play key roles at the intersection of microbiology and wastewater engineering. In addition to the well-studied ammonia oxidizing bacteria, nitrite oxidizing bacteria, heterotrophic denitrifiers, and anammox bacteria, there are some other N-cycling microorganisms that are less abundant but functionally important in wastewater nitrogen removal. These microbes include, but not limited to ammonia oxidizing archaea (AOA), complete ammonia oxidation (comammox) bacteria, dissimilatory nitrate reduction to ammonia (DNRA) bacteria, and nitrate/nitrite-dependent anaerobic methane oxidizing (NO_x-DAMO) microorganisms. In the past decade, the development of high-throughput molecular technologies has enabled the detection, quantification, and characterization of these minor populations. The aim of this review is therefore to synthesize the current knowledge on the distribution, ecological niche, and kinetic properties of these “overlooked” N-cycling microbes at wastewater treatment plants. Their potential applications in novel wastewater nitrogen removal processes are also discussed. A comprehensive understanding of these overlooked N-cycling microbes from microbiology, ecology, and engineering perspectives will facilitate the design and operation of more efficient and sustainable biological nitrogen removal processes.

Graphical abstract

Keywords

Ammonia oxidizing archaea (AOA) / Complete ammonia oxidizing (comammox) bacteria / Dissimilatory nitrate reduction to ammonium (DNRA) bacteria / Nitrate/nitrite-dependent anaerobic methane oxidizing (NO_x-DAMO) microorganisms / Engineering application

References

[1] Akunna J C, Bizeau C, Moletta R (1993). Nitrate and nitrite reductions with anaerobic sludge using various carbon sources: Glucose, glycerol, acetic acid, lactic acid and methanol. Water Research, 27(8): 1303–1312

[2] Ali M, Oshiki M, Awata T, Isobe K, Kimura Z, Yoshikawa H, Hira D, Kindaichi T, Satoh H, Fujii T, Okabe S (2015). Physiological characterization of anaerobic ammonium oxidizing bacterium ‘Candidatus Jettenia caeni’. Environmental Microbiology, 17(6): 2172–2189

[3] Annavajhala M K, Kapoor V, Santo-Domingo J, Chandran K (2018). Comammox functionality identified in diverse engineered biological wastewater treatment systems. Environmental Science & Technology Letters, 5(2): 110–116

[4] Arshad A, Speth D R, De Graaf R M, Op Den Camp H J M, Jetten M S M, Welte C U (2015). A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by methanoperedens-like archaea. Frontiers in Microbiology, 6: 1423

[5] Bartelme R P, Mclellan S L, Newton R J (2017). Freshwater recirculating aquaculture system operations drive biofilter bacterial community shifts around a stable nitrifying consortium of ammonia-oxidizing archaea and comammox Nitrospira. Frontiers in Microbiology, 8: 101

[6] Beeckman F, Motte H, Beeckman T (2018). Nitrification in agricultural soils: impact, actors and mitigation. Current Opinion in Biotechnology, 50: 166–173

[7] Blackburne R, Vadivelu V M, Yuan Z, Keller J (2007). Kinetic characterisation of an enriched Nitrospira culture with comparison to Nitrobacter. Water Research, 41(14): 3033–3042

[8] Camejo P Y, Santo Domingo J, Mcmahon K D, Noguera D R (2017). Genome-enabled insights into the ecophysiology of the comammox bacterium “Candidatus Nitrospira nitrosa”. mSystems, 2(5): e00059-17

[9] Carlson H K, Lui L M, Price M N, Kazakov A E, Carr A V, Kuehl J V, Owens T K, Nielsen T, Arkin A P, Deutschbauer A M (2020). Selective carbon sources influence the end products of microbial nitrate respiration. ISME Journal, 14(8): 2034–2045

[10] Castro-Barros C M, Jia M, Van Loosdrecht M C M, Volcke E I P, Winkler M K H (2017). Evaluating the potential for dissimilatory nitrate reduction by anammox bacteria for municipal wastewater treatment. Bioresource Technology, 233: 363–372

[11] Chen H, Jin W, Liang Z, Abomohra A E F, Zhou X, Tu R, Han S (2017). Abundance and diversity of ammonia-oxidizing archaea in a biological aerated filter process. Annals of Microbiology, 67(6): 405–416

[12] Chen H, Wang M, Chang S (2020). Disentangling community structure of ecological system in activated sludge: core communities, functionality, and functional redundancy. Microbial Ecology, 80(2): 296–308

[13] Cotto I, Dai Z, Huo L, Anderson C L, Vilardi K J, Ijaz U, Khunjar W, Wilson C, De Clippeleir H, Gilmore K, Bailey E, Pinto A J (2020). Long solids retention times and attached growth phase favor prevalence of comammox bacteria in nitrogen removal systems. Water Research, 169: 115268

[14] Daims H, Lebedeva E V, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard R H, Von Bergen M, Rattei T, Bendinger B, Nielsen P H, Wagner M (2015). Complete nitrification by Nitrospira bacteria. Nature, 528(7583): 504–509

[15] Ettwig K F, Butler M K, Le Paslier D, Pelletier E, Mangenot S, Kuypers M M M, Schreiber F, Dutilh B E, Zedelius J, De Beer D, Gloerich J, Wessels H J C T, Van Alen T, Luesken F, Wu M L, Van De Pas-Schoonen K T, Op Den Camp H J M O, Janssen-Megens E M, Francoijs K J, Stunnenberg H, Weissenbach J, Jetten M S M, Strous M (2010). Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature, 464(7288): 543–548

[16] Fan S Q, Xie G J, Lu Y, Liu B F, Xing D F, Han H J, Yuan Z, Ren N Q (2020). Granular sludge coupling nitrate/nitrite dependent anaerobic methane oxidation with anammox: from proof-of-concept to high rate nitrogen removal. Environmental Science & Technology, 54(1): 297–305

[17] Fan X Y, Gao J F, Pan K L, Li D C, Dai H H, Li X (2019). Temporal heterogeneity and temperature response of active ammonia-oxidizing microorganisms in winter in full-scale wastewater treatment plants. Chemical Engineering Journal, 360: 1542–1552

[18] Fowler S J, Palomo A, Dechesne A, Mines P D, Smets B F (2018). Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environmental Microbiology, 20(3): 1002–1015

[19] Gao J, Duan Y, Liu Y, Zhuang X, Liu Y, Bai Z, Ma W, Zhuang G (2019). Long- and short-chain AHLs affect AOA and AOB microbial community composition and ammonia oxidation rate in activated sludge. Journal of Environmental Sciences-China, 78: 53–62

[20] Gao J, Luo X, Wu G, Li T, Peng Y (2014). Abundance and diversity based on amoA genes of ammonia-oxidizing archaea and bacteria in ten wastewater treatment systems. Applied Microbiology and Biotechnology, 98(7): 3339–3354

[21] Gottshall E Y, Bryson S J, Cogert K I, Landreau M, Sedlacek C J, Stahl D A, Daims H, Winkler M (2020). Sustained nitrogen loss in a symbiotic association of comammox Nitrospira and anammox bacteria. bioRxiv.

[22] Graf J S, Mayr M J, Marchant H K, Tienken D, Hach P F, Brand A, Schubert C J, Kuypers M M M, Milucka J (2018). Bloom of a denitrifying methanotroph, ‘Candidatus Methylomirabilis limnetica’, in a deep stratified lake. Environmental Microbiology, 20(7): 2598–2614

[23] Guerrero-Cruz S, Stultiens K, Van Kessel M a H J, Versantvoort W, Jetten M S M, Op den Camp H J M, Kartal B (2019). Key physiology of a nitrite-dependent methane-oxidizing enrichment culture. Applied and Environmental Microbiology, 85(8): e00124-19

[24] Gwak J H, Jung M Y, Hong H, Kim J G, Quan Z X, Reinfelder J R, Spasov E, Neufeld J D, Wagner M, Rhee S K (2020). Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants. ISME Journal, 14(2): 335–346

[25] Han P, Yu Y, Zhou L J, Tian Z, Li Z, Hou L, Liu M, Wu Q, Wagner M, Men Y (2019). Specific micropollutant biotransformation pattern by the comammox bacterium Nitrospira inopinata. Environment Science & Technology, 53(15): 8695–8705

[26] Haroon M F,Hu S H, Shi Y, Imelfort M, Keller J,Hugenholtz P,Yuan Z G, Tyson G W ( 2013). Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature, 500(7464): 567

[27] Hatzenpichler R (2012). Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Applied and Environmental Microbiology, 78(21): 7501–7510

[28] He Z, Cai C, Geng S, Lou L, Xu X, Zheng P, Hu B (2013). Modelling a nitrite-dependent anaerobic methane oxidation process: parameters identification and model evaluation. Bioresource Technology, 147: 315–320

[29] He Z, Cai C, Wang J, Xu X, Zheng P, Jetten M S M, Hu B (2016). A novel denitrifying methanotroph of the NC10 phylum and its microcolony. Scientific Reports, 6(1): 32241

[30] He Z, Geng S, Pan Y, Cai C, Wang J, Wang L, Liu S, Zheng P, Xu X, Hu B (2015a). Improvement of the trace metal composition of medium for nitrite-dependent anaerobic methane oxidation bacteria: Iron (II) and copper (II) make a difference. Water Research, 85: 235–243

[31] He Z, Geng S, Shen L, Lou L, Zheng P, Xu X, Hu B (2015b). The short- and long-term effects of environmental conditions on anaerobic methane oxidation coupled to nitrite reduction. Water Research, 68: 554–562

[32] Holman J B, Wareham D G (2005). COD, ammonia and dissolved oxygen time profiles in the simultaneous nitrification/denitrification process. Biochemical Engineering Journal, 22(2): 125–133

[33] Holmes D E, Dang Y, Smith J A (2019). Chapter Four- Nitrogen cycling during wastewater treatment. In: Gadd G M, Sariaslani S, ed. Advances in Applied Microbiology. Salt Lake City: Academic Press, 106: 113–192

[34] Hu B, He Z, Geng S, Cai C, Lou L, Zheng P, Xu X (2014). Cultivation of nitrite-dependent anaerobic methane-oxidizing bacteria: impact of reactor configuration. Applied Microbiology and Biotechnology, 98(18): 7983–7991

[35] Hu Z, Ma R (2016). Distribution and characteristic of nitrite-dependent anaerobic methane oxidation bacteria by comparative analysis of wastewater treatment plants and agriculture fields in northern China. PeerJ, 4: e2766

[36] Insel G (2007). Effects of design and aeration control parameters on Simultaneous nitrification and denitrification (SNdN) performance for activated sludge process. Environmental Engineering Science, 24(5): 675–686

[37] Jiang Q Q, Bakken L R (1999). Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiology Ecology, 30(2): 171–186

[38] Kampman C, Temmink H, Hendrickx T L G, Zeeman G, Buisman C J N (2014). Enrichment of denitrifying methanotrophic bacteria from municipal wastewater sludge in a membrane bioreactor at 20°C. Journal of Hazardous Materials, 274: 428–435

[39] Kartal B, Kuenen J G, Van Loosdrecht M C M (2010). Sewage treatment with anammox. Science, 328(5979): 702–703

[40] Keren R, Lawrence J E, Zhuang W, Jenkins D, Banfield J F, Alvarez-Cohen L, Zhou L, Yu K (2020). Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance. Microbiome, 8(1): 7

[41] Kim H, Park D, Yoon S (2017). pH control enables simultaneous enhancement of nitrogen retention and N₂O reduction in Shewanella loihica Strain PV-4. Frontiers in Microbiology, 8: 1820

[42] Kits K D, Jung M Y, Vierheilig J, Pjevac P, Sedlacek C J, Liu S, Herbold C, Stein L Y, Richter A, Wissel H, Brüggemann N, Wagner M, Daims H (2019). Low yield and abiotic origin of N₂O formed by the complete nitrifier Nitrospira inopinata. Nature Communications, 10(1): 1836

[43] Kits K D, Sedlacek C J, Lebedeva E V, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein L Y, Daims H, Wagner M (2017). Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature, 549(7671): 269–272

[44] Koch H, Van Kessel M a H J, Lücker S (2019). Complete nitrification: insights into the ecophysiology of comammox Nitrospira. Applied Microbiology and Biotechnology, 103(1): 177–189

[45] Könneke M, Bernhard A E, De La Torre J R, Walker C B, Waterbury J B, Stahl D A (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437(7058): 543–546

[46] Kraft B, Tegetmeyer H E, Sharma R, Klotz M G, Ferdelman T G, Hettich R L, Geelhoed J S, Strous M (2014). The environmental controls that govern the end product of bacterial nitrate respiration. Science, 345(6197): 676–679

[47] Laanbroek H J, Bodelier P L E, Gerards S (1994). Oxygen consumption kinetics of Nitrosomonas europaea and Nitrobacter hamburgensis grown in mixed continuous cultures at different oxygen concentrations. Archives of Microbiology, 161(2): 156–162

[48] Lawson C E, Lücker S (2018). Complete ammonia oxidation: an important control on nitrification in engineered ecosystems? Current Opinion in Biotechnology, 50: 158–165

[49] Lawson C E, Wu S, Bhattacharjee A S, Hamilton J J, Mcmahon K D, Goel R, Noguera D R (2017). Metabolic network analysis reveals microbial community interactions in anammox granules. Nature Communications, 8(1): 15416

[50] Li M, Du C, Liu J, Quan X, Lan M, Li B (2018). Mathematical modeling on the nitrogen removal inside the membrane-aerated biofilm dominated by ammonia-oxidizing archaea (AOA): Effects of temperature, aeration pressure and COD/N ratio. Chemical Engineering Journal, 338: 680–687

[51] Li Z, Peng Y, Gao H (2020). Enhanced long-term advanced denitrogenation from nitrate wastewater by anammox consortia: Dissimilatory nitrate reduction to ammonium (DNRA) coupling with anammox in an upflow biofilter reactor equipped with EDTA-2Na/Fe(II) ratio and pH control. Bioresource Technology, 305: 123083

[52] Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polprasert C (2011). Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresource Technology, 102(4): 3694–3701

[53] Lin Z, Huang W, Zhou J, He X, Wang J, Wang X, Zhou J (2020). The variation on nitrogen removal mechanisms and the succession of ammonia oxidizing archaea and ammonia oxidizing bacteria with temperature in biofilm reactors treating saline wastewater. Bioresource Technology, 314: 123760

[54] Liu Y, Ngo H H, Guo W, Peng L, Pan Y, Guo J, Chen X, Ni B J (2016). Autotrophic nitrogen removal in membrane-aerated biofilms: Archaeal ammonia oxidation versus bacterial ammonia oxidation. Chemical Engineering Journal, 302: 535–544

[55] Lu H, Chandran K, Stensel D (2014). Microbial ecology of denitrification in biological wastewater treatment. Water Research, 64: 237–254

[56] Lu P, Liu T, Ni B J, Guo J, Yuan Z, Hu S (2019). Growth kinetics of ‘Candidatus Methanoperedens nitroreducens’ enriched in a laboratory reactor. Science of the Total Environment, 659: 442–450

[57] Luesken F A, Wu M L, Op Den Camp H J M, Keltjens J T, Stunnenberg H, Francoijs K J, Strous M, Jetten M S M (2012). Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environmental Microbiology, 14(4): 1024–1034

[58] Luesken F A, Zhu B, Van Alen T A, Butler M K, Diaz M R, Song B, Op Den Camp H J M, Jetten M S M, Ettwig K F (2011). pmoA primers for detection of anaerobic methanotrophs. Applied and Environmental Microbiology, 77(11): 3877–3880

[59] Ma R, Hu Z, Zhang J, Ma H, Jiang L, Ru D (2017). Reduction of greenhouse gases emissions during anoxic wastewater treatment by strengthening nitrite-dependent anaerobic methane oxidation process. Bioresource Technology, 235: 211–218

[60] Martens-Habbena W, Berube P M, Urakawa H, De La Torre J R, Stahl D A (2009). Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature, 461(7266): 976–979

[61] Meng H, Zhang X, Zhou Z, Luo L, Lan W, Lin J G, Li X Y, Gu J D (2021). Simultaneous occurrence and analysis of both anammox and n-damo bacteria in five full-scale wastewater treatment plants. International Biodeterioration & Biodegradation, 156: 105112

[62] Nowka B, Daims H, Spieck E (2015). Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Applied and Environmental Microbiology, 81(2): 745–753

[63] Palomo A, Pedersen A G, Fowler S J, Dechesne A, Sicheritz-Ponten T, Smets B F (2018). Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME Journal, 12(7): 1779–1793

[64] Pan K L, Gao J F, Fan X Y, Li D C, Dai H H (2018). The more important role of archaea than bacteria in nitrification of wastewater treatment plants in cold season despite their numerical relationships. Water Research, 145: 552–561

[65] Pan Y, Ni B J, Liu Y, Guo J (2016). Modeling of the interaction among aerobic ammonium-oxidizing archaea/bacteria and anaerobic ammonium-oxidizing bacteria. Chemical Engineering Science, 150: 35–40

[66] Pandey C B, Kumar U, Kaviraj M, Minick K J, Mishra A K, Singh J S (2020). DNRA: A short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems. Science of the Total Environment, 738: 139710

[67] Park H, Brotto A C, Van Loosdrecht M C M, Chandran K (2017). Discovery and metagenomic analysis of an anammox bacterial enrichment related to “Candidatus Brocadia caroliniensis” in a full-scale glycerol-fed nitritation-denitritation separate centrate treatment process. Water Research, 111: 265–273

[68] Park H D, Wells G F, Bae H, Criddle C S, Francis C A (2006). Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Applied and Environmental Microbiology, 72(8): 5643–5647

[69] Pjevac P, Schauberger C, Poghosyan L, Herbold C W, Van Kessel M A, Daebeler A, Steinberger M, Jetten M S, Lücker S, Wagner M, Daims H (2017). AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Frontiers in Microbiology, 8: 1508

[70] Prosser J I, Hink L, Gubry Rangin C, Nicol G W (2020). Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies. Global Change Biology, 26(1): 103–118

[71] Qin W, Amin S A, Martens-Habbena W, Walker C B, Urakawa H, Devol A H, Ingalls A E, Moffett J W, Armbrust E V, Stahl D A (2014). Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proceedings of the National Academy of Sciences of the United States of America, 111(34): 12504–12509

[72] Ren Y, Huu Hao N, Guo W, Wang D, Peng L, Ni B J, Wei W, Liu Y (2020). New perspectives on microbial communities and biological nitrogen removal processes in wastewater treatment systems. Bioresource Technology, 297: 122491

[73] Roots P, Wang Y, Rosenthal A F, Griffin J S, Sabba F, Petrovich M, Yang F, Kozak J A, Zhang H, Wells G F (2019). Comammox Nitrospira are the dominant ammonia oxidizers in a mainstream low dissolved oxygen nitrification reactor. Water Research, 157: 396–405

[74] Sakoula D, Koch H, Frank J, Jetten M S M, Van Kessel M a H J, Lücker S (2020). Enrichment and physiological characterization of a novel comammox Nitrospira indicates ammonium inhibition of complete nitrification. The ISME Journal, doi: 10.1038/s41396-020-00827-4

[75] Sauder L A, Albertsen M, Engel K, Schwarz J,Nielsen P H, Wagner M, Neufeld J D (2017). Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME Journal, 11(5): 1142–1157

[76] Sauder L A, Peterse F, Schouten S, Neufeld J D (2012). Low-ammonia niche of ammonia-oxidizing archaea in rotating biological contactors of a municipal wastewater treatment plant. Environmental Microbiology, 14(9): 2589–2600

[77] Schouten S, Hopmans E C, Sinninghe Damsté J S (2013). The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review. Organic Geochemistry, 54: 19–61

[78] Shi Y, Hu S, Lou J, Lu P, Keller J, Yuan Z (2013). Nitrogen removal from wastewater by coupling anammox and methane-dependent denitrification in a membrane biofilm reactor. Environmental Science & Technology, 47(20): 11577–11583

[79] Simon J (2002). Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiology Reviews, 26(3): 285–309

[80] Soliman M, Eldyasti A (2018). Ammonia-Oxidizing Bacteria (AOB): opportunities and applications: A review. Reviews in Environmental Science and Biotechnology, 17(2): 285–321

[81] Spasov E, Tsuji J M, Hug L A, Doxey A C, Sauder L A, Parker W J, Neufeld J D (2020). High functional diversity among Nitrospira populations that dominate rotating biological contactor microbial communities in a municipal wastewater treatment plant. ISME Journal, 14(7): 1857–1872

[82] Stahl D A, De La Torre J R (2012). Physiology and diversity of ammonia-oxidizing archaea. Annual Review of Microbiology, 66(1): 83–101

[83] Stein L Y, Klotz M G (2016). The nitrogen cycle. Current Biology, 26(3): R94–R98

[84] Straka L L, Meinhardt K A, Bollmann A, Stahl D A, Winkler M K H (2019). Affinity informs environmental cooperation between ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (anammox) bacteria. ISME Journal, 13(8): 1997–2004

[85] Tiedje J M (1988). Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Sehnder A J B, ed. Biology of Anaerobic Miroorganisms.New York: Wiley, 179–244

[86] Van Den Berg E M, Boleij M, Kuenen J G, Kleerebezem R, Van Loosdrecht M C M (2016). DNRA and denitrification coexist over a broad range of acetate/N-NO₃⁻ ratios, in a chemostat enrichment culture. Frontiers in Microbiology, 7: 1842–1842

[87] Van Den Berg E M, Elisário M P, Kuenen J G, Kleerebezem R, Van Loosdrecht M C M (2017). Fermentative bacteria influence the competition between denitrifiers and DNRA bacteria. Frontiers in Microbiology, 8: 1684–1684

[88] Van Kessel M a H J, Speth D R, Albertsen M, Nielsen P H, Op Den Camp H J M, Kartal B,Jetten M S M, Lücker S (2015). Complete nitrification by a single microorganism. Nature, 528(7583): 555–559

[89] Van Kessel M a H J, Stultiens K,Slegers M F W, Cruz S G, Jetten M S M, Kartal B, Op Den Camp H J M (2018). Current perspectives on the application of N-damo and anammox in wastewater treatment. Current Opinion in Biotechnology, 50: 222–227

[90] Wan Y, Huang Z, Zhou L, Li T, Liao C, Yan X, Li N, Wang X (2020). Bioelectrochemical ammoniation coupled with microbial electrolysis for nitrogen recovery from nitrate in wastewater. Environmental Science & Technology, 54(5): 3002–3011

[91] Wang J, Zhou J, Wang Y, Wen Y, He L, He Q (2020a). Efficient nitrogen removal in a modified sequencing batch biofilm reactor treating hypersaline mustard tuber wastewater: The potential multiple pathways and key microorganisms. Water Research, 177: 115734

[92] Wang M, Huang G, Zhao Z, Dang C, Liu W, Zheng M (2018). Newly designed primer pair revealed dominant and diverse comammox amoA gene in full-scale wastewater treatment plants. Bioresource Technology, 270: 580–587

[93] Wang Q, Chen Q (2016). Simultaneous denitrification and denitrifying phosphorus removal in a full-scale anoxic–oxic process without internal recycle treating low strength wastewater. Journal of Environmental Sciences-China, 39: 175–183

[94] Wang Q, Liang J, Zhao C, Bai Y, Liu R, Liu H, Qu J (2020b). Wastewater treatment plant upgrade induces the receiving river retaining bioavailable nitrogen sources. Environmental Pollution, 263: 114478

[95] Wang S, Liu C, Wang X, Yuan D, Zhu G (2020c). Dissimilatory nitrate reduction to ammonium (DNRA) in traditional municipal wastewater treatment plants in China: Widespread but low contribution. Water Research, 179: 115877

[96] Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017). Comammox in drinking water systems. Water Research, 116: 332–341

[97] Wang Z, Zhang L, Zhang F, Jiang H, Ren S, Wang W, Peng Y (2020d). Nitrite accumulation in comammox-dominated nitrification-denitrification reactors: Effects of DO concentration and hydroxylamine addition. Journal of Hazardous Materials, 384: 121375

[98] Wiesmann U (1994). Biological nitrogen removal from wastewater. In: Wiesmann U, ed. Biotechnics/Wastewater. Berlin,Heidelberg: Springer, 113–154

[99] Winkler M K H, Ettwig K F, Vannecke T P W, Stultiens K, Bogdan A, Kartal B, Volcke E I P (2015). Modelling simultaneous anaerobic methane and ammonium removal in a granular sludge reactor. Water Research, 73: 323–331

[100] Wright C L, Schatteman A, Crombie A T, Murrell J C, Lehtovirta-Morley L E (2020). Inhibition of ammonia monooxygenase from ammonia-oxidizing archaea by linear and aromatic alkynes. Applied and Environmental Microbiology, 86(9): e02388–19

[101] Wu Y J, Whang L M, Fukushima T, Huang Y J (2020). Abundance, community structures, and nitrification inhibition on ammonia-oxidizing archaea enriched under high and low salinity. International Biodeterioration & Biodegradation, 153: 105040

[102] Xiang Y, Shao Z, Chai H, Ji F, He Q (2020). Functional microorganisms and enzymes related nitrogen cycle in the biofilm performing simultaneous nitrification and denitrification. Bioresource Technology, 314: 123697

[103] Xie G J, Liu T, Cai C, Hu S, Yuan Z (2018). Achieving high-level nitrogen removal in mainstream by coupling anammox with denitrifying anaerobic methane oxidation in a membrane biofilm reactor. Water Research, 131: 196–204

[104] Yang Y, Herbold C W, Jung M Y, Qin W, Cai M, Du H, Lin J G, Li X, Li M, Gu J D (2020). Survival strategies of ammonia-oxidizing archaea (AOA) in a full-scale WWTP treating mixed landfill leachate containing copper ions and operating at low-intensity of aeration. Water Research, 191: 116798

[105] Yin Z, Bi X, Xu C (2018). Ammonia-oxidizing archaea (AOA) play with ammonia-oxidizing bacteria (AOB) in nitrogen removal from wastewater. Archaea-an International Microbiological Journal, 2018

[106] Yin Z, Xie L, Zhou Q (2015). Effects of sulfide on the integration of denitrification with anaerobic digestion. Journal of Bioscience and Bioengineering, 120(4): 426–431

[107] Yoon S, Cruz-García C, Sanford R, Ritalahti K M, Löffler F E (2015). Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO₃-/NO₂- reduction pathways in Shewanella loihica strain PV-4. ISME Journal, 9(5): 1093–1104

[108] Zhang L, Okabe S (2020). Ecological niche differentiation among anammox bacteria. Water Research, 171: 115468

[109] Zhang Y, Tian Z, Liu M, Shi Z J, Hale L, Zhou J, Yang M (2015). High concentrations of the antibiotic spiramycin in wastewater lead to high abundance of ammonia-oxidizing archaea in nitrifying populations. Environmental Science & Technology, 49(15): 9124–9132

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 41701269), the National Key R&D Program of China (No. 2019YFC0408800), and the Fundamental Research Funds for the Central Universities (No. 2020FZZX001-06).

Open Access

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

RIGHTS & PERMISSIONS

2021 The Author(s) 2021. This article is published with open access at link.springer.com and journal.hep.com.cn