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Front. Environ. Sci. Eng.    2021, Vol. 15 Issue (6) : 133    https://doi.org/10.1007/s11783-021-1426-2
REVIEW ARTICLE
Overlooked nitrogen-cycling microorganisms in biological wastewater treatment
Shaoyi Xu, Xiaolong Wu, Huijie Lu()
Key Laboratory of Environment Remediation and Ecological Health (Ministry of Education), College of Environmental Resource Sciences, Zhejiang University, Hangzhou 310058, China
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Abstract

• 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.

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.
Keywords Ammonia oxidizing archaea (AOA)      Complete ammonia oxidizing (comammox) bacteria      Dissimilatory nitrate reduction to ammonium (DNRA) bacteria      Nitrate/nitrite-dependent anaerobic methane oxidizing (NOx-DAMO) microorganisms      Engineering application     
Corresponding Author(s): Huijie Lu   
Issue Date: 26 March 2021
 Cite this article:   
Shaoyi Xu,Xiaolong Wu,Huijie Lu. Overlooked nitrogen-cycling microorganisms in biological wastewater treatment[J]. Front. Environ. Sci. Eng., 2021, 15(6): 133.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-021-1426-2
https://academic.hep.com.cn/fese/EN/Y2021/V15/I6/133
Fig.1  Overlooked microorganisms in the wastewater microbial nitrogen cycle.
Microbes Reaction equation Key characteristics Representative species at WWTPs Reference
AOA NH4+ + 1.5O2 = NO2− + H2O+ 2H+
(DG°′ = - 274.7 kJ/mol)		 Aerobic, Thaumarchaeota Nitrosopumilus maritimus
Candidatus Nitrosocosmicus exaquare
Candidatus Nitrosotenuis cloacae		 Martens-Habbena et al., 2009
Comammox bacteria NH4+ + 2O2 = NO3− + H2O+ 2H+
(DG°′ = - 348.9 kJ/mol)		 Aerobic, Nitrospira lineage II
Mixotrophic (e.g., formate, urea)		 Nitrospira inopinata
Canditatus Nitrospira nitrosa/ nitrificans/ kreftii		 Daims et al., 2015; Van Kessel et al., 2015
DNRA bacteria C6H12O6 + 3 NO3− + 6H+
= 6 CO2 + 3NH4+ + H2O
(DG°′ = - 623 kJ/mol NO3−-N)		 Respiratory/Fermentative
Electron donors: organics, H2, HS−
Enzymes: Nar/Nir, or Nap/Nrf		 Wolinella succinogenes
Serratia marcescens
Salmonella typhimurium
Escherichia coli		 Tiedje, 1988; Holmes et al., 2019; Pandey et al., 2020
N-DAMO archaea 4NO3− + CH4 = 4NO2− + CO2 + 2H2O
(DG°′ = - 503 kJ/mol CH4)		 Reverse methanogenesis, ANME-2D lineage
Enzymes: NarGH, MCR		 Candidatus Methanoperedens nitroreducens Haroon et al., 2013
n-DAMO bacteria 8NO2− + 3CH4 + 8H+ = 4N2 + 3CO2 +
10H2O
(DG°′ = - 928 kJ/mol CH4)		 Inter-aerobic pathway, NC10 phylum
Enzymes: NirSJFD/GH/L, pMMO		 Candidatus Methylomirabilis oxyfera/sinica/
limnetica/ lanthanidiphila		 Ettwig et al., 2010; He et al., 2016; Graf et al., 2018
Tab.1  Basic characteristics of the four overlooked nitrogen-cycling microorganisms
Microbes Electron donor/acceptor Half saturation
constant of
electron donors Km,d (µmol/L)		 Half saturation
constant of
electron acceptors Km,a (µmol/L)		 Maximum specific growth rate µmax (/h) Cell yield
(mg Protein /mol
NH3 or NO2−)		 Reference
Ammonia oxidizers NH4+-N/O2 (bacteria) 1.9–200 6.9–17.4 0.007–0.088 250 Laanbroek et al., 1994; Jiang and Bakken, 1999; Lawson and Lücker, 2018
NH4+-N/O2 (archaea) 0.003–4.4 2.01–10.38 0.010–0.050 298.4–304.3 Martens-Habbena et al., 2009; Qin et al., 2014; Kits et al., 2017; Lawson and Lücker, 2018
Nitrite oxidizers NO2−-N/O2
(Nitrobacter)		 49–1380 5.31–165.63 0.0115–0.125 83–108 Laanbroek et al., 1994; Blackburne et al., 2007; Nowka et al., 2015; Lawson and Lücker, 2018
NO2−-N/O2
(Nitrospira)		 9–27 2.19–5.94 0.027–0.083 120–213
Comammox bacteria NH4+-N/O2 0.049, 0.040 NA 0.0061 394.7 Kits et al., 2017; Sakoula et al., 2020
NO2−-N/O2 449.2, 12.5 NA NA NA
DNRA bacteria Organic/ (NO3−, NO2−) NA NA 0.11–0.5 NA Simon, 2002
Inorganics/(NO3−, NO2−) NA NA 0.091 NA
N-DAMO archaea
n-DAMO bacteria		 CH4/NO3− 500 150±28.6 NA 73–85*
CH4/NO2− 2.6–5.9, 91.8±5 4.28–7 0.0015–0.0583 NA He et al., 2013; Winkler et al., 2015; Guerrero-Cruz et al., 2019; Lu et al., 2019
Anammox bacteria NH4+-N/ NO2−-N 2.54–673.90 0.22–361.35 0.0022–0.014 30–70# Ali et al., 2015; Zhang and Okabe, 2020
Tab.2  Kinetic parameters of the conventional and overlooked nitrogen-cycling microorganisms
Fig.2  Abundances of AOA, comammox bacteria, DNRA bacteria and NOx-DAMO microorganisms in wastewater treatment. Data are collected from published results, representing samples from municipal WWTPs, industrial WWTPs, recirculating aquaculture systems, and drinking water treatment systems.
Fig.3  Potential applications of AOA (a), comammox bacteria (b), DNRA bacteria (c) and NOx-DAMO microorganisms (d) in novel wastewater nitrogen removal processes.
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