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 (NOx-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.
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References
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
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
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
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
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
Beeckman F, Motte H, Beeckman T (2018). Nitrification in agricultural soils: impact, actors and mitigation. Current Opinion in Biotechnology, 50: 166–173
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
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
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
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
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
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
Hatzenpichler R (2012). Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Applied and Environmental Microbiology, 78(21): 7501–7510
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
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
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
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
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
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
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
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
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
Jiang Q Q, Bakken L R (1999). Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiology Ecology, 30(2): 171–186
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
Kartal B, Kuenen J G, Van Loosdrecht M C M (2010). Sewage treatment with anammox. Science, 328(5979): 702–703
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
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
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
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
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
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
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
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
Lawson C E, Lücker S (2018). Complete ammonia oxidation: an important control on nitrification in engineered ecosystems? Current Opinion in Biotechnology, 50: 158–165
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
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
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
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
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
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
Lu H, Chandran K, Stensel D (2014). Microbial ecology of denitrification in biological wastewatertreatment. Water Research, 64: 237–254
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
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
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
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
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
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
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
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
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
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
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
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 fullscale glycerol-fed nitritation-denitritation separate centrate treatment process. Water Research, 111: 265–273
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
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
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
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
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
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
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: https://doi.org/10.1038/s41396-020-00827-4
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
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
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
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
Simon J (2002). Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiology Reviews, 26(3): 285–309
Soliman M, Eldyasti A (2018). Ammonia-Oxidizing Bacteria (AOB): opportunities and applications: A review. Reviews in Environmental Science and Biotechnology, 17(2): 285–321
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
Stahl D A, De La Torre J R (2012). Physiology and diversity of ammonia-oxidizing archaea. Annual Review of Microbiology, 66(1): 83–101
Stein L Y, Klotz M G (2016). The nitrogen cycle. Current Biology, 26 (3): R94–R98
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Wiesmann U (1994). Biological nitrogen removal from wastewater. In: Wiesmann U, ed. Biotechnics/Wastewater. Berlin, Heidelberg: Springer, 113–154
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
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
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
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
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
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
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
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
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
Zhang L, Okabe S (2020). Ecological niche differentiation among anammox bacteria. Water Research, 171: 115468
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).
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Highlights
• AOA and comammox bacteria can be more abundant and active than AOB/NOB at WWTPs.
• Coupled DNRA/anammox and NOx-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.
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Xu, S., Wu, X. & Lu, H. Overlooked nitrogen-cycling microorganisms in biological wastewater treatment. Front. Environ. Sci. Eng. 15, 133 (2021). https://doi.org/10.1007/s11783-021-1426-2
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DOI: https://doi.org/10.1007/s11783-021-1426-2