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Research progress and prospects of complete ammonia oxidizing bacteria in wastewater treatment

Research progress and prospects of complete ammonia oxidizing bacteria in wastewater treatment Front. Environ. Sci. Eng. 2022, 16(9): 123 https://doi.org/10.1007/s11783-022-1555-2 REVIEW ARTICLE Research progress and prospects of complete ammonia oxidizing bacteria in wastewater treatment 1 2 3 1 Shaoping Luo , Yi Peng , Ying Liu , Yongzhen Peng (✉) 1 National Engineering Laboratory for Advanced Municipal Wastewater Treatment and Reuse Technology, Engineering Research Center of Beijing, Beijing University of Technology, Beijing 100124, China 2 Xinkai Water Environmental Investment Co. Ltd., Beijing 101101, China 3 Zhongshan Public Utilities Water Co. Ltd., Zhongshan 528400, China HIGH LIGHTS GRAPHIC A BSTRA CT � Comammox bacteria have unique physiological characteristics. � Comammox bacteria are widely distributed in natural and artificial systems. � Comammox bacteria have the potential to reduce N O emissions. � Coupling comammox bacteria with DEAMOX can be promoted in wastewater treatment. � Comammox bacteria have significant potential for enhancing total nitrogen removal. ABSTRA CT Complete ammonia oxidizing bacteria, or comammox bacteria (CAOB), can oxidize ammonium to nitrate on its own. Its discovery revolutionized our understanding of biological nitrification, and its distribution in both natural and artificial systems has enabled a reevaluation of the relative contribution of microorganisms to the nitrogen cycle. Its wide distribution, adaptation to oligotrophic medium, and AR TICL E IN F O diverse metabolic pathways, means extensive research on CAOB and its application in water treatment can be promoted. Furthermore, the energy-saving characteristics of high oxygen affinity and low Article history: sludge production may also become frontier directions for wastewater treatment. This paper provides Received 22 September 2021 an overview of the discovery and environmental distribution of CAOB, as well as the physiological characteristics of the microorganisms, such as nutrient medium, environmental factors, enzymes, and Revised 14 December 2021 metabolism, focusing on future research and the application of CAOB in wastewater treatment. Further Accepted 27 December 2021 research should be carried out on the physiological characteristics of CAOB, to analyze its ecological Available online 18 February 2022 niche and impact factors, and explore its application potential in wastewater treatment nitrogen cycle improvement. Keywords: Complete ammonia oxidizing (comammox) bacteria Nitrogen cycle © The Author(s) 2022. This article is published with open access at link.springer.com and journal.hep. Physiological characteristics com.cn Wastewater treatment Kuypers et al., 2018). The first step is ammonia oxidation 1 Introduction + – (NH -N ! NO -N, Eq. 1), mediated by ammonia 4 2 oxidizing microorganisms (AOM), including ammonia As a key process in the natural nitrogen cycle, nitrification oxidizing bacteria (AOB) and ammonia oxidizing archaea is a microbial process by which ammonium (NH -N) is – – (AOA), which use ammonia monooxygenase (AMO) and sequentially oxidized to nitrite (NO -N) and nitrate (NO 2 3 hydroxylamine dehydrogenase (HAO) to oxidize ammonia -N) by two separate organisms (Winogradsky, 1890; to nitrite (Arp et al., 2002; Könneke et al., 2005). The – – second step is nitrite oxidation (NO -N ! NO -N, 2 3 ✉ Corresponding author Eq. 2), catalyzed by nitrite oxidizing bacteria (NOB), E-mail: pyz@bjut.edu.cn which uses nitrite oxidoreductase (NXR) to oxidize nitrite to nitrate (Teske et al., 1994). However, in 2015, the Special Issue—Visions 2 Front. Environ. Sci. Eng. 2022, 16(9): 123 discovery of complete ammonia oxidizing bacteria, which plants reaching up to 100% (Zhou et al., 2021). How to can oxidize ammonium directly to nitrate in a single utilize the physiological characteristics of comammox organism (Fig. 1), challenged our understanding of the bacteria in aquatic ecosystems is of great significance. The conventional two-step nitrification process (Daims et al., integration of comammox bacteria into existing waste- 2015; Van Kessel et al., 2015). Furthermore, comammox water treatment processes has important research prospects bacteria have been detected in various environments, such and application potential for improving the effectiveness as wastewater treatment facilities, drinking water systems, and stability of domestic wastewater treatment, reducing natural wetlands, lake sediments, and soil (Wang et al., sewage treatment costs, and decreasing greenhouse gas emissions. 2017; Annavajhala et al., 2018; Xia et al., 2018). Their wide distribution has attracted great interest in their ecological role compared with other nitrifiers. 2 Discovery of comammox bacteria Costa et al. (2006) speculated that, from a thermodynamic perspective, there was a microorganism that can comple- + – tely oxidize ammonium to nitrate (NH -N ! NO -N, 4 3 Eq. 3). This single microorganism, which can complete nitrification, is named complete ammonia oxidizing bacteria (CAOB). In 2015, two laboratories in the Nether- lands and Austria found strains in the genus Nitrospira that can independently complete the entire nitrification process, confirming the existence of comammox bacteria (Daims et al., 2015; Van Kessel et al., 2015). þ – þ NH þ 1:5O ↕ ↓NO þ H O þ 2H 4 2 2 2 ðΔG ¼ –274:7KJ=molÞ (1) – – NO þ 0:5O ↕ ↓NO ðΔG ¼ –74:1KJ=molÞ (2) 2 2 3 þ – þ NH þ 2O ↕ ↓NO þ H O þ 2H 4 2 3 2 Fig. 1 Differences between traditional microbial nitrification and comammox bacteria nitrification. ðΔG ¼ –348:9KJ=molÞ (3) After comammox bacteria were discovered, compar- isons of comammox bacteria with the amoA gene in the 2.1 Candidatus Nitrospira inopinata NCBI database identified a large number of highly similar sequences, in both natural (forests, plains, wetlands, etc.) Daims et al. (2015) collected biofilm from the wall of a hot water pipe of a 1200 m deep oil exploration well in North and artificial systems (drinking water plants, sewage Caucasus, Russia, and enriched it in an ammonium- treatment plants, paddy fields, etc.) (Erwin et al., 2005; containing inorganic medium at a constant temperature Knief et al., 2006; Jia et al., 2007; Vigliotta et al., 2007; of 46 °C. The enriched culture could oxidize NH -N to Steenbergh et al., 2010; Daims et al., 2015; Van Kessel NO -N. By detecting the specific rRNA targeting probe of et al., 2015). Later research confirmed this, and found nitrifying bacteria, fluorescent in situ hybridization (FISH) significant differences in abundance between habits (Xia confirmed that the enriched culture only contained et al., 2018). The distribution difference of clades A and B Nitrospira, and the rest were Betaproteobacterium without had a certain relationship with the difference of the ammonia oxidation ability. A polymerase chain reaction encoded genome (Palomo et al., 2018; Koch et al., 2019). (PCR) did not detect any known amoA genes or 16S rRNA Comammox bacteria have recently been identified in genes of AOA and AOB. Metagenomic sequencing found water treatment systems, but their contribution to biologi- cal nitrogen removal remains unclear (Daims et al., 2015; that the relative abundance of Nitrospira in the enriched Van Kessel et al., 2015; Pjevac et al., 2017; Wang et al., culture was 68%–80%. Further enrichment revealed that + – 2017; Zhao et al., 2019). They significantly contribute to Nitrospira could oxidize NH -N to NO -N. Therefore, it 4 3 nitrification in water treatment systems (Pinto et al., 2015; was considered to be a microbial strain with complete Xia et al., 2018), with the abundance ratio of comammox ammonia oxidation ability and was named Candidatus bacteria to total amoA genes in some wastewater treatment Nitrospira inopinata (Ca. N. inopinata). In 2017, Kits et al. Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 3 (2017) obtained the pure culture strain of Ca. N. inopinata (2015) found that the amoA gene in Ca. N. nitrosa and Ca. by enrichment culture, which was also the first pure culture N. nitrificans is different from that of typical ammonia strain of comammox bacteria. oxidizing bacteria, and belongs to two different branches phylogenetic, but is highly similar to pmoA of the methane 2.2 Candidatus Nitrospira nitrosa and Candidatus monooxygenase of Crenohrix polyspora. Therefore, it is Nitrospira nitrificans inferred that the amoA gene of some comammox bacteria in the previous study may be incorrectly classified as Also in 2015, van Kessel et al. (2015) sampled the methane monooxygenase and could be ignored (Daims anaerobic compartment of a trickling filter connected to a et al., 2015; Van Kessel et al., 2015). The discovery of comammox bacteria revolutionized recirculation aquaculture system. Under low dissolved our understanding of the nitrification process, and the oxygen (DO£3.1 μmol/L O ) and oligotrophic conditions, relative contribution of microorganisms to the nitrogen the genus Brocadia of anammox bacteria (AnAOB) and two different Nitrospira genus were enriched by culturing cycle should be reassessed. for 12 months. A high abundance of Nitrospira was rarely seen under low DO conditions. Both NOB species carried the genes (amo and hao) for ammonia oxidation as well as 3 Physiological characteristics of the nxr gene necessary for nitrite oxidation; therefore, comammox bacteria these two strains were confirmed to have the metabolic + – potential to oxidize NH -N to NO -N, and are named 3.1 Nutrient matrix 4 3 Candidatus Nitrospira nitrosa (Ca.N.nitrosa)and Candidatus Nitrospira nitrificans (Ca. N. nitrificans), Comammox bacteria have advantages over traditional respectively. The phylogeny of 16S rRNA genes indicates nitrifying bacteria in oligotrophic substrates, such as low that they belong to lineage II of the genus Nitrospira. ammonia nitrogen and low DO (Kits et al., 2017). In addition to the reported AOA of marine N. maritimus 2.3 Candidatus Nitrospira kreftii SCM1, the ammonia half-saturation constant of AOA and AOB is much higher than that of purified and cultured Ca. N. inopinata, but the affinity of comammox bacteria to Sakoula et al. (2021) used a continuous membrane nitrite is much lower than that of traditional NOB (Kits bioreactor with an effective volume of 5 L containing et al., 2017). Zhao et al. (2021) used urea and nitrite to Ca. N. nitrosa and Ca. N. nitrificans (van Kessel et al., enrich and cultivate comammox bacteria for 390 days to 2015), operated at room temperature and under suitable increase the ratio of amoA gene, indicating that comam- conditions (e.g., pH = 7.5, DO = 50% oxygen saturation) mox bacteria have diverse metabolic potential. for 39 months. They obtained a novel comammox bacteria species, Candidatus Nitrospira kreftti (Ca. N. kreftti), which displayed clear differences in terms of ammonia and 3.2 Environmental factors nitrite oxidation kinetics. For example, Ca. N. kreftti has a higher nitrite affinity. Furthermore, partial inhibition of Environmental conditions, such as DO, pH, and tempera- ammonia oxidation at ammonium concentrations as low as ture have a significant impact on the growth and activity of 25 µM was observed in the bioreactor, indicating that comammox bacteria (Kits et al.,2017; Palomo et al., 2018; differences in ammonium tolerance could potentially be a Roots et al., 2019; Takahashi et al., 2020; Sun et al., 2020). niche-determining factor for different comammox Nitros- The microbial oxidase of comammox bacteria is similar to pira. cytochrome bd-type terminal oxidase, which is generally expressed under extremely low DO concentrations and has 2.4 Summary a higher affinity for DO (Borisov et al., 2011). There are currently no reports on the half-saturation constant of All identified comammox are Nitrospira bacteria, belong- oxygen, but comammox bacteria are more competitive ing to lineage II of the Nitrospira genus, and are under low DO conditions. With increasing DO, AOA and phylogenetically divided into two branches according to AOB activities gradually increase, but comammox bacteria the amoA gene: clade A and clade B. These two clades lose their competitiveness (Palomo et al., 2018; Roots et al., 2019). Sun et al. (2020) found that when the pH was have significant differences in substrate operation and between 6.74 and 8.65, the abundance of comammox metabolism, energy transfer, and environmental adapt- bacteria in coastal wetlands was positively correlated with ability (Palomo et al., 2018). In comammox bacteria pH. In addition, comammox bacteria can show nitrifying enrichment cultures, genome analysis has identified the activity at pH 3–4, indicating that comammox bacteria may amoA gene, encoding AMO; hao encoding HAO; and nxr be able to adapt to low pH (Takahashi et al., 2020). Shi encoding NXR, which can independently perform the et al. found that the abundance of comammox bacteria was complete nitrification process (Daims et al., 2015; Van relatively high in samples collected from wetland ecosys- Kessel et al., 2015; Sakoula et al., 2021). Van Kessel et al. 4 Front. Environ. Sci. Eng. 2022, 16(9): 123 tems. Based on the changes in comammox bacteria species sequester carbon through the reduced tricarboxylic acid diversity in summer and winter, they speculated that (rTCA) cycle. The rTCA cycle is usually the mechanism of temperature may be a key factor affecting the structure of CO fixation by anaerobic or aerobic microorganisms comammox bacteria (Shi et al., 2020). Zhou et al. (2021) (Lücker et al., 2010); compared with the Calvin cycle tested the abundance, activity, and metabolic character- corresponding to AOB, the fixed unit CO of the rTCA istics of nitrifying bacteria in drinking water and waste- cycle consumes less adenosine triphosphate (ATP) and water treatment plants with seasonal changes and found requires less oxygen (Lawson and Lücker, 2018). that the network complex of comammox microorganisms Theoretically, the comammox bacteria oxidation unit in sewage treatment plants was highest in December. NH -N has a shorter metabolic pathway and a higher However, a study by Kits et al. (2017) found that the growth yield than AOB, so it is easier to obtain a optimal growth of Ca. N. inopinata occurred at 37 °C, and competitive advantage under low DO conditions (Costa the optimal enrichment culture temperature was 46 °C. et al., 2006). This indicates that different comammox bacteria can adapt to growth environments of different temperatures. 3.4 Natural habitat distribution 3.3 Enzymes and metabolism Similar to AOA, comammox bacteria have a high affinity + + for NH -N and are suitable for growth under low NH -N 4 4 The comammox bacteria metabolism pathway is complex conditions. There are numerous natural systems suitable and can adapt to different nutrient substrates (Daims et al., for the growth of comammox bacteria. Table 1 shows 2015; Van Kessel et al., 2015; Shen et al., 2016; Kits et al., partial statistics of the distribution of comammox bacteria 2017; Han et al., 2019; Liu et al., 2020a; Wang et al., 2021; in natural ecosystems. Zhao et al., 2021). Liu et al. (2020a) found that comammox Comammox bacteria are widely distributed in nature, bacteria contribute 34%–87% of nitrification in a typical and the distribution further confirms that comammox oligotrophic environment with high pH and low tempera- bacteria like to grow under conditions of low DO and ture along the Yangtze River. Kits et al. (2017) enriched NH -N. AOA was first discovered in the marine environ- and cultivated comammox bacteria under higher tempera- ment. However, although the physiological characteristics ture conditions, demonstrating that comammox micro- of comammox bacteria are similar to those of AOA, Liu organisms can adapt to varying and more extreme et al. (2020b) detected a high abundance of comammox environments. Metagenomic analysis shows that the bacteria in extremely saline sediments, showing that discovered comammox bacteria can use urea as a nitrogen comammox bacteria can adapt to high-salinity environ- source for energy metabolism and biosynthesis (Daims ments, and a distinct differentiation of comammox et al., 2015; Van Kessel et al., 2015; Zhao et al., 2021). Nitrospira groups driven by salinity has been identified Studies have found that comammox bacteria can use (Sun et al. 2021). However, so far, comammox bacteria hydrogen sulfide, sulfide, and fermentation products for have not been found in the ocean (Daims et al., 2015; metabolism (Kits et al., 2017), while trace organic Kuypers, 2017; Xu et al. 2020), indicating that salinity is a pollutants in the environment can be removed through key factor. Whether there are comammox bacteria in metabolism (Han et al., 2019). Some comammox may also marine habitats is an important research direction. have the potential to oxidize formic acid and hydrogen At present, data on the nitrification kinetics of (Palomo et al., 2018), and a variety of antibiotics have been comammox bacteria are derived from pure cultured Ca. N. used to effectively and selectively enrich different strains inopinata. (Kits et al., 2017). Therefore, there are some of comammox bacteria (Wang et al., 2021). In addition, limitations for studying the nitrification kinetics of comammox bacteria have a gene encoding alkaline comammox. With the widespread discovery of comammox phosphatase, which can make it more advantageous bacteria and the versatility of metabolism, research on the under insufficient phosphorus conditions (Shen et al., physiological characteristics of comammox bacteria will 2016). further understanding of the niche characteristics of Comammox bacteria have a complete genome of key comammox bacteria in the biosphere and its relative functional enzymes in the oxidation process of NH -N to contribution to the nitrogen cycle. NO -N, and can complete the whole process of traditional two-step nitrification metabolism itself. The comammox bacteria genome encodes the nitrite reductase gene (nir) 4 Application in wastewater treatment but lacks the nitric oxide reductase gene (nor). In theory, it 4.1 Distribution in water systems produces NO but not N O during biological reactions (Kits et al., 2019). Palomo et al. (2018) found that there In conventional artificial system studies, only the nitrifica- was no pathway related to NO metabolism in the known tion activity of AOM and NOB is evaluated, and the comammox bacteria genome, and the NO reduction presence of comammox bacteria is rarely considered. NOB reaction may not be possible. Comammox bacteria Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 5 Table 1 Comammox bacteria partial distribution in natural ecosystems Growth environment Country Strains Research method Key finding Reference a) Atmospheric fine China N. inopinata PCR The abundance of comammox bacteria in Gao et al., 2016 particles Clone sequencing the atmosphere is less than AOA and greater than AOB. Forest soil, lake Austria; / Metagenome A PCR primer set was developed Pjevac et al., 2017 sediments, freshwater Netherlands specifically for the subunit amoA gene organisms, etc. encoding the unique amoA of comammox bacteria. Forest soil China / qPCR The abundance of comammox bacteria is Hu and He, 2017 very high. When the pH is 4.0–9.0, the abundance exceeds AOB and NOB. Sediments from the China N. inopinata Metagenome; The presence of comammox bacteria was Yu et al., 2018 Yangtze River Estuary N. nitrosa Macrotranscriptome; detected, and a primer set for clade A was N. nitrificans qPCR designed to quantitatively detect the amoA gene of comammox bacteria. Riparian soil China N. nitrosa qPCR; The microbial abundance of comammox Wang et al, 2019 N. nitrificans Correlation analysis in the riparian soil was 10 copies/g, and the abundance of comammox and Nitrospira was significantly correlated under certain conditions. Note: a) qPCR: quantitative polymerase chain reaction. of the Nitrospira genus was mistakenly thought to exist that comammox bacteria may play an important role in widely in artificial systems. Metagenomic detection and wastewater treatment. Sato et al. (2021) used a segmented analysis show that some of these have a full set of reactor to first ammonify organic nitrogen, and then nitrate characteristic genes for ammonia oxidation, indicating into nitrate as a hydroponic fertilizer for plant growth. that they may be comammox bacteria (Pinto et al., 2015). Through 16S rRNA gene sequencing and shotgun Table 2 shows partial statistics on the distribution of metagenomic analysis, the dominant microorganism in comammox bacteria in artificial systems. the nitrification process was confirmed as comammox Comammox bacteria are widely distributed in natural bacteria, and qPCR analysis showed that the expression of and artificial systems (Fig. 2). However, previous calcula- comammox-type AMO was more than 500 times higher tions on the contribution of ammonia oxidizing micro- than that of traditional AMO. Heise et al. (2021) found that organisms in the nitrogen cycle ignored the role of comammox bacteria participated in the removal of NH -N comammox bacteria. Theoretically, the AOM/NOB value at low steady-state NH -N concentrations in an aquaponic in the traditional nitrification process should be between system, indicating that comammox plays an important role two and three (Winkler et al., 2012), but studies have found in this system. that the abundance of Nitrospira in the same habitat Research on the growth mechanisms and physiological exceeds AOM (Zeng et al., 2015), which cannot be characteristics of comammox bacteria can improve the explained by traditional nitrification theories. It has now treatment of urban domestic wastewater. Fig. 3 shows a been demonstrated that some Nitrospira may be comam- common microbial denitrification process in wastewater mox bacteria (Pinto et al., 2015; Tatari et al., 2017). The plants. For urban wastewater partial nitrification-denitrifi- discovery of comammox will cause a reevaluation of the cation (PN/D) and partial nitrification-anaerobic ammonia relative contribution of nitrification in the nitrogen cycle, oxidation (PN/A) denitrification systems, the growth and and the structure of the flora. enrichment of comammox bacteria are one of the important reasons for the destruction of these systems (Wang et al., 4.2 Potential application in wastewater treatment 2020). Controlling the growth of comammox bacteria is an important factor in realizing PN/D or PN/A of urban Wang et al. (2018) found that, among eight wastewater domestic wastewater. Purified and cultured comammox treatment plant samples investigated, activity abundance of bacteria have a low affinity for nitrite (Kits et al., 2017; Xia amoA of the comammox bacteria in six samples was et al., 2018). Meanwhile, comammox bacteria and significantly higher than or comparable to that of AOB, anammox bacteria can form copolymers under hypoxic even reaching 24 times more in some wastewater plants. conditions (Van Kessel et al., 2015; Gottshall et al., 2021; The abundance of comammox bacteria to total amoA genes Shao and Wu, 2021). In theory, the nitrite oxidation in drinking water plants and AAO wastewater treatment activity of comammox bacteria can be inhibited by plants is up to 46%–100% (Zhou et al., 2021), indicating controlling conditions to achieve stable PN/A. In the PN/ 6 Front. Environ. Sci. Eng. 2022, 16(9): 123 Table 2 Comammox bacteria partial distribution in artificial systems Growth environment Country Species Research method Key finding Reference Wastewater treatment China N. inopinata Metagenome; Comammox bacteria abundance accounts Chao et al., 2016 plants (WWTPs) 16S rRNA for£0.1%. It is speculated that the contribution of comammox bacteria nitrification is small in the sewage treatment process. Drinking water Singapore; N. inopinata Metagenome Comammox bacteria are widely distributed in Wang et al., 2017 systems China; N. nitrosa drinking water systems and coexist with traditional United States N. nitrificans AOM. The nitrification of drinking water systems may be mainly completed by comammox bacteria. WWTPs United States N. nitrosa Metagenome To achieve enrichment of Ca. N. nitrosa, it has a Kits et al., 2017 higher affinity for urea. WWTPs United States N. inopinata Metagenome; A primer set and qPCR targeting clade A were Camejo et al., United Kingdom N. nitrosa qPCR designed; comammox bacteria prefer long sludge age 2017 N. nitrificans and attached growth, and the increase in abundance in the same habitat has no correlation with the decrease in AOB and NOB abundance. Urban lake China / 16S rRNA Comammox bacteria are widely distributed in Xu et al., 2020 urban lakes, eutrophication may inhibit its growth. Acidic soils Japan / 16S rRNA When the pH is 3–4, nitrification activity of Takahashi et al., comammox bacteria is still detected. 2020 A continuous Netherlands N. Kreftii FISH; They obtained a novel comammox bacteria species, Sakoula et al., membrane Metagenome; Ca. N. kreftti. Moreover, they think differences in 2021 bioreactor ammonium tolerance could potentially be a niche-determining factor for different comammox Nitrospira. Lab-scale PN/A SBR China / 16S rRNA The amoA gene of comammox bacteria in the Shao and Wu, Reactor qPCR PN/A system that has been running stably for more 2021 than 1,000 days accounted for 89.27.9%, achieving synergistic denitrification under hypoxic conditions. Aquaponic system Germany / 16S rRNA Comammox bacteria are found in the high- Heise et al., 2021 efficiency aquaponic symbiosis system, which participate in the removal of NH -N at low steady-state NH -N concentrations. A process, NH -N and DO continuously decrease as Compared with PN/A, the DEAMOX process has many particles or biofilms develop, which may lead to the advantages, such as a more stable accumulation of NO -N, enrichment of comammox bacteria (Wang et al., 2020), no complicated control, and theoretical 100% deep competing with AOB and reducing the total nitrogen denitrification. In this process, comammox bacteria are removal rate, instead of the traditional NOB proliferation used to couple partial denitrification-anaerobic ammonia effect. oxidation to develop a new type of denitrification process. In some wastewater treatment plants, comammox Hypoxic nitrification reduces aeration energy consump- bacteria account for a relatively high proportion of tion, and anoxic partial denitrification-anaerobic ammonia activated sludge (Zhou et al., 2021). An important research oxidation saves carbon sources (Fig. 4). The process is direction in wastewater treatment is how to use the stable and easy to control, with a low sludge output and a physiological characteristics of comammox bacteria to reduction in greenhouse gas emissions, and may be more further reduce sewage treatment costs and improve suitable for saving energy, reducing consumption, and treatment effects. Using comammox bacteria to treat low deep denitrification (Xu et al., 2021). NH -N municipal sewage under low DO conditions can Traditional biological denitrification is usually achieved reduce the aeration; therefore, the energy consumption. through nitrification and denitrification, producing N Oin The generation of sludge can also be reduced, as well as the the process. N O is an important greenhouse gas. cost of post-sludge treatment and disposal. With the recent Comammox bacteria have no N O biosynthesis pathway; research and development of partial denitrification (NO - therefore, using comammox bacteria as the main reaction N ! NO -N) and the anaerobic ammonia oxidation microorganism in the nitrification process may greatly coupling process (DEAMOX), simultaneous treatment of reduce N O emissions. Comammox bacteria can oxidize – + NO -N and NH -N in the same reactor has been realized. low ammonia nitrogen to nitrate nitrogen under low DO 3 4 Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 7 Fig. 2 Ternary plot of the proportions of comammox, AOB, and AOA in 111 metagenomic data sets of different environmental samples from the NCBI SRA database (Xia et al. 2018). Fig. 3 Common microbial denitrification processes in wastewater treatment plants. (DNRA: dissimilatory nitrate reduction to ammonium). conditions. Low DO meets the reaction conditions of treatment. All comammox that have been discovered are simultaneous denitrification (Holman and Wareham, Nitrospira bacteria, belonging to lineage II of the 2005). Simultaneous nitrification and denitrification can Nitrospira genus. The affinity of comammox bacteria to reduce internal circulation and aeration energy consump- ammonium is higher and is also slower growing than tion and save space, while the nitrification process, conventional AOB/NOB, so better adapted to oligotrophic avoiding the accumulation of nitrite, can be used to treat conditions. Furthermore, comammox bacteria have a micro-polluted drinking water, improve treatment effi- complex pathway and can live in many adverse environ- ciency, and avoid the potential risk of nitrite production. ments, as demonstrated by their wide distribution in natural and artificial systems. Coupling with DEAMOX or enriching in oligotrophic conditions can promote total 5 Conclusions and outlook nitrogen removal, thereby reducing both costs and N O emissions. This review summarizes the discovery, physiological The discovery of comammox bacteria has important characteristics, and ecological distribution of comammox significance and research value for calculating and bacteria, and proposes potential applications in wastewater evaluating the relative contribution of nitrification in the 8 Front. Environ. Sci. Eng. 2022, 16(9): 123 Fig. 4 Application of comammox bacteria in wastewater treatment. (DB: denitrifying bacteria). microbial nitrogen cycle. To detect the presence and be developed (e.g., AOB/AOA/NOB/comammox bac- abundance of comammox bacteria using the amoA gene of teria), and the accuracy and sensitivity of specific primers comammox bacteria, a variety of specific primers have need to be further improved; 2) In wastewater treatment been developed to identify and quantify comammox plants, the quantity of comammox bacteria as a proportion bacteria of different branches and species levels. However, of nitrifying bacteria varies, and the relative contribution is the accuracy and sensitivity of these need to be further not clear; evaluation and calculation of this should be improved. strengthened in the future; 3) Comammox bacteria are used Comammox bacteria are of great significance in both to couple DEAMOX to develop a new nitrogen removal natural and artificial systems, but the niche differences and process, the potential of comammox bacteria in more influencing factors between them and AOB, AOA, NOB, sustainable nitrogen removal techniques could be assessed and other microorganisms remain unclear, and may be a from the point of view of engineering applications. research hotspot for microbial applications in the future. At Acknowledgements This research project was financially supported by the present, our understanding of comammox bacteria is Foundation for Innovation Research Groups of the National Natural Science limited, and the in situ activity of comammox bacteria Foundation of China (No. 62021003); Biological Wastewater Treatment and cannot be fully evaluated. There is an urgent need to Process Control Technology, Beijing International Science and technology develop isolation and purification methods to study the Cooperation Base; and the Founding projects of Beijing Municipal physiological characteristics of microorganisms at the Commission of Education. single-cell level, and to explore the coupling mechanism Open Access This article is licensed under a Creative Commons between comammox bacteria and traditional nitrification Attribution 4.0 International License, which permits use, sharing, adaptation, and denitrification. For the treatment of micro-polluted distribution and reproduction in any medium or format, as long as you give water sources, it is necessary to further explore the appropriate credit to the original author(s) and the source, provide a link to the enrichment and operating conditions of comammox 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 bacteria. In wastewater treatment, the use of comammox Commons licence, unless indicated otherwise in a credit line to the material. bacteria can reduce aeration energy consumption, green- If material is not included in the article’s Creative Commons licence and your house gas N O emissions, and sludge production, while intended use is not permitted by statutory regulation or exceeds the permitted improving deep denitrification efficiency. It has a broad use, you will need to obtain permission directly from the copyright holder. To application potential and may become a new biological view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. denitrification process in the future. The following areas should be given priority in future studies on comammox bacteria: 1) Efficient and accurate References methods that can identify the contribution of diverse microorganisms from similar functional microbes should Annavajhala M K, Kapoor V, Santo-Domingo J, Chandran K (2018). Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 9 Comammox functionality identified in diverse engineered biological Kits K D, Sedlacek C J, Lebedeva E V, Han P, Bulaev A, Pjevac P, wastewater treatment systems. Environmental Science & Technology Daebeler A, Romano S, Albertsen M, Stein L Y, Daims H, Wagner M Letters, 5(2): 110–116 (2017). Kinetic analysis of a complete nitrifier reveals an oligotrophic Arp D J, Sayavedra-Soto L A, Hommes N G (2002). Molecular biology lifestyle. Nature, 549(7671): 269–272 and biochemistry of ammonia oxidation by Nitrosomonas europaea. Knief C, Kolb S, Bodelier P L E, Lipski A, Dunfield P F (2006). The Archives of Microbiology, 178(4): 250–255 active methanotrophic community in hydromorphic soils changes in Borisov V B, Gennis R B, Hemp J, Verkhovsky M I (2011). The response to changing methane concentration. Environmental Micro- cytochrome bd respiratory oxygen reductases. Biochimica et biology, 8(2): 321–333 Biophysica Acta (BBA) - Bioenergetics, 1807(11): 1398–1413 Koch H, van Kessel M A H J, Lücker S (2019). Complete nitrification: Camejo P Y, Santo Domingo J, McMahon K D, Noguera D R (2017). insights into the ecophysiology of comammox Nitrospira. Applied Genome-enabled insights into the ecophysiology of the comammox Microbiology and Biotechnology, 103(1): 177–189 bacterium “Candidatus Nitrospira nitrosa”. mSystems, 2(5): Könneke M, Bernhard A E, de la Torre J R, Walker C B, Waterbury J B, e00059–e17 Stahl D A (2005). Isolation of an autotrophic ammonia-oxidizing Chao Y Q, Mao Y P, Yu K, Zhang T (2016). Novel nitrifiers and marine archaeon. Nature, 437(7058): 543–546 comammox in a full-scale hybrid biofilm and activated sludge reactor Kuypers M M M (2017). Microbiology: A fight for scraps of ammonia. revealed by metagenomic approach. Applied Microbiology and Nature, 549(7671): 162–163 Biotechnology, 100(18): 8225–8237 Kuypers M M M, Marchant H K, Kartal B (2018). The microbial Costa E, Pérez J, Kreft J U (2006). Why is metabolic labour divided in nitrogen-cycling network. Nature Reviews. Microbiology, 16(5): nitrification? Trends in Microbiology, 14(5): 213–219 263–276 Daims H, Lebedeva E V, Pjevac P, Han P, Herbold C, Albertsen M, Lawson C E, Lücker S (2018). Complete ammonia oxidation: An Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard R H, important control on nitrification in engineered ecosystems? Current von Bergen M, Rattei T, Bendinger B, Nielsen P H, Wagner M Opinion in Biotechnology, 50: 158–165 (2015). Complete nitrification by Nitrospira bacteria. Nature, 528 Liu S, Wang H, Chen L, Wang J, Zheng M, Liu S, Chen Q, Ni J (2020a). (7583): 504–509 Comammox Nitrospira within the Yangtze River continuum: Erwin D P, Erickson I K, Delwiche M E, Colwell F S, Strap J L, community, biogeography, and ecological drivers. The ISME Crawford R L (2005). Diversity of oxygenase genes from methane- Journal, 14(10): 2488–2504 and ammonia-oxidizing bacteria in the Eastern Snake River Plain Liu Z, Zhang C, Wei Q, Zhang S, Quan Z, Li M (2020b). Temperature aquifer. Applied and Environmental Microbiology, 71(4): 2016–2025 and salinity drive comammox community composition in mangrove Gao J F, Fan X Y, Pan K L, Li H Y, Sun L X (2016). Diversity, ecosystems across southeastern China. The Science of the total abundance and activity of ammonia-oxidizing microorganisms in fine environment, 742: 140456 particulate matter. Scientific Reports, 6(1): 38785 Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei Gottshall E Y, Bryson S J, Cogert K I, Landreau M, Sedlacek C J, Stahl T, Damsté J S, Spieck E, Le Paslier D, Daims H (2010). A Nitrospira D A, Daims H, Winkler M (2021). Sustained nitrogen loss in a metagenome illuminates the physiology and evolution of globally symbiotic association of comammox Nitrospira and anammox important nitrite-oxidizing bacteria. Proceedings of the National bacteria. Water Research, 202(1): 117426 Academy of Sciences of the United States of America, 107(30): Han P, Yu Y, Zhou L, Tian Z, Li Z, Hou L, Liu M, Wu Q, Wagner M, 13479–13484 Men Y (2019). Specific micropollutant biotransformation pattern by Palomo A, Pedersen A G, Fowler S J, Dechesne A, Sicheritz-Pontén T, the comammox bacterium Nitrospira inopinata. Environmental Smets B F (2018). Comparative genomics sheds light on niche Science & Technology, 53(15): 8695–8705 differentiation and the evolutionary history of comammox Nitros- Heise J, Müller H, Probst A J, Meckenstock R U (2021). Ammonium pira. The ISME Journal, 12(7): 1779–1793 removal in aquaponics indicates participation of comammox Pinto A J, Marcus D N, Ijaz U Z, Bautista-de Lose Santos Q M, Dick G J, Nitrospira. Current Microbiology, 78(3): 894–903 Raskin L (2015). Metagenomic evidence for the presence of Holman J B, Wareham D G (2005). COD, ammonia and dissolved comammox Nitrospira-like bacteria in a drinking water system. oxygen time profiles in the simultaneous nitrification/denitrification MSphere, 1(1): e00054–e15 process. Biochemical Engineering Journal, 22(2): 125–133 Pjevac P, Schauberger C, Poghosyan L, Herbold C W, van Kessel M A Hu H W, He J Z (2017). Comammox–A newly discovered nitrification H J, Daebeler A, Steinberger M, Jetten M S M, Lücker S, Wagner M, process in the terrestrial nitrogen cycle. Journal of Soils and Daims H (2017). AmoA-targeted polymerase chain reaction primers 17(12): 2709–2717 Sediments, for the specific detection and quantification of comammox Nitrospira Jia Z J, Kikuchi H, Watanabe T, Asakawa S, Kimura M (2007). in the environment. Frontiers in Microbiology, 8: 1508 Molecular identification of methane oxidizing bacteria in a Japanese Roots P, Wang Y, Rosenthal A F, Griffin J S, Sabba F, Petrovich M, rice field soil. Biology and Fertility of Soils, 44(1): 121–130 Yang F, Kozak J A, Zhang H, Wells G F (2019). Comammox Kits K D, Jung M Y, Vierheilig J, Pjevac P, Sedlacek C J, Liu S, Herbold Nitrospira are the dominant ammonia oxidizers in a mainstream low C, Stein L Y, Richter A, Wissel H, Brüggemann N, Wagner M, dissolved oxygen nitrification reactor. Water Research, 157: 396–405 Daims H (2019). Low yield and abiotic origin of N O formed by the 2 Sakoula D, Koch H, Frank J, Jetten M S M, van Kessel M A H J, Lücker complete nitrifier Nitrospira inopinata. Nature Communications, 10 S (2021). Enrichment and physiological characterization of a novel (1): 1836 comammox Nitrospira indicates ammonium inhibition of complete 10 Front. Environ. Sci. Eng. 2022, 16(9): 123 nitrification. The ISME journal, 15(4): 1010–1024 Wang S Y, Pi Y L, Jiang Y Y, Pan H W, Wang X X, Wang X M, Zhou Z Sato Y, Tanaka E, Hori T, Futamata H, Murofushi K, Takagi H, Akachi M, Zhu G B (2019). Nitrate reduction in the reed rhizosphere of a T, Miwa T, Inaba T, Aoyagi T, Habe H (2021). Efficient conversion riparian zone: From functional genes to activity and contribution. of organic nitrogenous wastewater to nitrate solution driven by Environmental Research, 180(6): 108867 comammox Nitrospira. Water Research, 197: 117088 Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017). Shao Y H, Wu J H (2021). comammox Nitrospira species dominate in an Comammox in drinking water systems. Water Research, 116: 332– efficient partial nitrification-anammox bioreactor for treating ammo- nium at low loadings. Environmental Science & Technology, 55(3): Wang Y L, Zhao R X, Liu L, Li B, Zhang T (2021). Selective enrichment 2087–2098 of comammox from activated sludge using antibiotics. Water Shen Y C, Hu Y N, Shaw G C (2016). Expressions of alkaline Research, 197: 117087 phosphatase genes during phosphate starvation are under positive Wang Z, Zhang L, Zhang F Z, Jiang H, Ren S, Wang W, Peng Y Z influences of multiple cell wall hydrolase genes in Bacillus subtilis. (2020). Nitrite accumulation in comammox-dominated nitrification- The Journal of General and Applied Microbiology, 62(2): 106–109 reactors: Effects of DO concentration and hydro- denitrification Shi Y, Jiang Y Y, Wang S Y, Wang X M, Zhu G B (2020). xylamine addition. Journal of Hazardous Materials, 384: 121375 Biogeographic distribution of comammox bacteria in diverse Winkler M K, Bassin J P, Kleerebezem R, Sorokin D Y, van Loosdrecht terrestrial habitats. Science of the Total Environment, 717: 137257 M C (2012). Unravelling the reasons for disproportion in the ratio of Steenbergh A K, Meima M M, Kamst M, Bodelier P L E (2010). AOB and NOB in aerobic granular sludge. Applied Microbiology Biphasic kinetics of a methanotrophic community is a combination of and Biotechnology, 94(6): 1657–1666 growth and increased activity per cell. FEMS Microbiology Ecology, Winogradsky S (1890). The morphology of the contributions of 71(1): 12–22 nitrification system. Archives of Biological Sciences, 4: 257–275 Sun D Y, Tang X F, Zhao M Y, Zhang Z X, Hou L J, Liu M, Wang B Z, Xia F, Wang J G, Zhu T, Zou B, Rhee S K, Quan Z X (2018). Ubiquity Klümper U, Han P (2020). Distribution and diversity of comammox and diversity of complete ammonia oxidizers (comammox). Applied Nitrospira in coastal wetlands of China. Frontiers in Microbiology, and Environmental Microbiology, 84(24): e01390–e18 11: 589268 Xu S Y, Wu X L, Lu H J (2021). Overlooked nitrogen-cycling Sun D Y, Zhao M Y, Tang X F, Liu M, Hou L J, Zhao Q, Li J, Gu J D, microorganisms in biological wastewater treatment. Frontiers of Han P (2021). Niche adaptation strategies of different clades of Environmental Science & Engineering, 15(6): 133 comammox Nitrospira in the Yangtze Estuary. International Xu Y F, Lu J, Wang Y C, Liu G L, Wan X Q, Hua Y M, Zhu D W, Zhao J Biodeterioration & Biodegradation, 164: 105286 W (2020). Diversity and abundance of comammox bacteria in the Takahashi Y, Fujitani H, Hirono Y, Tago K, Wang Y, Hayatsu M, sediments of an urban lake. Journal of Applied Microbiology, 128(6): Tsuneda S (2020). Enrichment of comammox and nitrite-oxidizing 1647–1657 Nitrospira from acidic soils. Frontiers in Microbiology, 11: 1737 Yu C, Hou L, Zheng Y, Liu M, Yin G, Gao J, Liu C, Chang Y, Han P Tatari K, Musovic S, Gülay A, Dechesne A, Albrechtsen H, Smets B F (2018). Evidence for complete nitrification in enrichment culture of (2017). Density and distribution of nitrifying guilds in rapid sand tidal sediments and diversity analysis of clade a comammox filters for drinking water production: Dominance of Nitrospira spp. Nitrospira in natural environments. Applied Microbiology and Water Research, 127: 239–248 Biotechnology, 102(21): 9363–9377 Teske A, Alm E, Regan J M, Toze S, Rittmann B E, Stahl D A (1994). Zeng W, Zhang L M, Wang A Q, Zhang J, Peng Y Z, Duan J L (2015). Evolutionary relationships among ammonia- and nitrite-oxidizing Community structures and population dynamics of nitrifying bacteria bacteria. Journal of Bacteriology, 176(21): 6623–6630 in activated sludges of wastewater treatment plants. China Environ- Van Kessel M A H J, Speth D R, Albertsen M, Nielsen P H, Op den mental Science, 35(11): 3257–3265 (in Chinese) Camp H J M, Kartal B, Jetten M S M, Lücker S (2015). Complete Zhao Y X, Hu J J, Yang W L, Wang J Q, Jia Z J, Zheng P, Hu B L (2021). nitrification by a single microorganism. Nature, 528(7583): 555–559 The long-term effects of using nitrite and urea on the enrichment of Vigliotta G, Nutricati E, Carata E, Tredici S M, De Stefano M, Pontieri P, comammox bacteria. Science of the Total Environment, 755(Pt 2): Massardo D R, Prati M V, De Bellis L, Alifano P (2007). Clonothrix fusca Roze 1896, a filamentous, sheathed, methanotrophic γ- Zhao Z, Huang G, He S, Zhou N, Wang M, Dang C, Wang J, Zheng M proteobacterium. Applied and Environmental Microbiology, 73 (2019). Abundance and community composition of comammox (11): 3556–3565 bacteria in different ecosystems by a universal primer set. Science of Wang M Y, Huang G H, Zhao Z R, Dang C Y, Liu W, Zheng M S the Total Environment , 691: 146–155 (2018). Newly designed primer pair revealed dominant and diverse Zhou X, Li B, Wei J, Ye Y, Xu J, Chen L, Lu C (2021). Temperature comammox amoA gene in full-scale wastewater treatment plants. influenced the comammox community composition in drinking water Bioresource Technology, 270: 580–587 and wastewater treatment plants. Microbial Ecology, 82(4): 870–884 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers of Environmental Science & Engineering Springer Journals

Research progress and prospects of complete ammonia oxidizing bacteria in wastewater treatment

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Front. Environ. Sci. Eng. 2022, 16(9): 123 https://doi.org/10.1007/s11783-022-1555-2 REVIEW ARTICLE Research progress and prospects of complete ammonia oxidizing bacteria in wastewater treatment 1 2 3 1 Shaoping Luo , Yi Peng , Ying Liu , Yongzhen Peng (✉) 1 National Engineering Laboratory for Advanced Municipal Wastewater Treatment and Reuse Technology, Engineering Research Center of Beijing, Beijing University of Technology, Beijing 100124, China 2 Xinkai Water Environmental Investment Co. Ltd., Beijing 101101, China 3 Zhongshan Public Utilities Water Co. Ltd., Zhongshan 528400, China HIGH LIGHTS GRAPHIC A BSTRA CT � Comammox bacteria have unique physiological characteristics. � Comammox bacteria are widely distributed in natural and artificial systems. � Comammox bacteria have the potential to reduce N O emissions. � Coupling comammox bacteria with DEAMOX can be promoted in wastewater treatment. � Comammox bacteria have significant potential for enhancing total nitrogen removal. ABSTRA CT Complete ammonia oxidizing bacteria, or comammox bacteria (CAOB), can oxidize ammonium to nitrate on its own. Its discovery revolutionized our understanding of biological nitrification, and its distribution in both natural and artificial systems has enabled a reevaluation of the relative contribution of microorganisms to the nitrogen cycle. Its wide distribution, adaptation to oligotrophic medium, and AR TICL E IN F O diverse metabolic pathways, means extensive research on CAOB and its application in water treatment can be promoted. Furthermore, the energy-saving characteristics of high oxygen affinity and low Article history: sludge production may also become frontier directions for wastewater treatment. This paper provides Received 22 September 2021 an overview of the discovery and environmental distribution of CAOB, as well as the physiological characteristics of the microorganisms, such as nutrient medium, environmental factors, enzymes, and Revised 14 December 2021 metabolism, focusing on future research and the application of CAOB in wastewater treatment. Further Accepted 27 December 2021 research should be carried out on the physiological characteristics of CAOB, to analyze its ecological Available online 18 February 2022 niche and impact factors, and explore its application potential in wastewater treatment nitrogen cycle improvement. Keywords: Complete ammonia oxidizing (comammox) bacteria Nitrogen cycle © The Author(s) 2022. This article is published with open access at link.springer.com and journal.hep. Physiological characteristics com.cn Wastewater treatment Kuypers et al., 2018). The first step is ammonia oxidation 1 Introduction + – (NH -N ! NO -N, Eq. 1), mediated by ammonia 4 2 oxidizing microorganisms (AOM), including ammonia As a key process in the natural nitrogen cycle, nitrification oxidizing bacteria (AOB) and ammonia oxidizing archaea is a microbial process by which ammonium (NH -N) is – – (AOA), which use ammonia monooxygenase (AMO) and sequentially oxidized to nitrite (NO -N) and nitrate (NO 2 3 hydroxylamine dehydrogenase (HAO) to oxidize ammonia -N) by two separate organisms (Winogradsky, 1890; to nitrite (Arp et al., 2002; Könneke et al., 2005). The – – second step is nitrite oxidation (NO -N ! NO -N, 2 3 ✉ Corresponding author Eq. 2), catalyzed by nitrite oxidizing bacteria (NOB), E-mail: pyz@bjut.edu.cn which uses nitrite oxidoreductase (NXR) to oxidize nitrite to nitrate (Teske et al., 1994). However, in 2015, the Special Issue—Visions 2 Front. Environ. Sci. Eng. 2022, 16(9): 123 discovery of complete ammonia oxidizing bacteria, which plants reaching up to 100% (Zhou et al., 2021). How to can oxidize ammonium directly to nitrate in a single utilize the physiological characteristics of comammox organism (Fig. 1), challenged our understanding of the bacteria in aquatic ecosystems is of great significance. The conventional two-step nitrification process (Daims et al., integration of comammox bacteria into existing waste- 2015; Van Kessel et al., 2015). Furthermore, comammox water treatment processes has important research prospects bacteria have been detected in various environments, such and application potential for improving the effectiveness as wastewater treatment facilities, drinking water systems, and stability of domestic wastewater treatment, reducing natural wetlands, lake sediments, and soil (Wang et al., sewage treatment costs, and decreasing greenhouse gas emissions. 2017; Annavajhala et al., 2018; Xia et al., 2018). Their wide distribution has attracted great interest in their ecological role compared with other nitrifiers. 2 Discovery of comammox bacteria Costa et al. (2006) speculated that, from a thermodynamic perspective, there was a microorganism that can comple- + – tely oxidize ammonium to nitrate (NH -N ! NO -N, 4 3 Eq. 3). This single microorganism, which can complete nitrification, is named complete ammonia oxidizing bacteria (CAOB). In 2015, two laboratories in the Nether- lands and Austria found strains in the genus Nitrospira that can independently complete the entire nitrification process, confirming the existence of comammox bacteria (Daims et al., 2015; Van Kessel et al., 2015). þ – þ NH þ 1:5O ↕ ↓NO þ H O þ 2H 4 2 2 2 ðΔG ¼ –274:7KJ=molÞ (1) – – NO þ 0:5O ↕ ↓NO ðΔG ¼ –74:1KJ=molÞ (2) 2 2 3 þ – þ NH þ 2O ↕ ↓NO þ H O þ 2H 4 2 3 2 Fig. 1 Differences between traditional microbial nitrification and comammox bacteria nitrification. ðΔG ¼ –348:9KJ=molÞ (3) After comammox bacteria were discovered, compar- isons of comammox bacteria with the amoA gene in the 2.1 Candidatus Nitrospira inopinata NCBI database identified a large number of highly similar sequences, in both natural (forests, plains, wetlands, etc.) Daims et al. (2015) collected biofilm from the wall of a hot water pipe of a 1200 m deep oil exploration well in North and artificial systems (drinking water plants, sewage Caucasus, Russia, and enriched it in an ammonium- treatment plants, paddy fields, etc.) (Erwin et al., 2005; containing inorganic medium at a constant temperature Knief et al., 2006; Jia et al., 2007; Vigliotta et al., 2007; of 46 °C. The enriched culture could oxidize NH -N to Steenbergh et al., 2010; Daims et al., 2015; Van Kessel NO -N. By detecting the specific rRNA targeting probe of et al., 2015). Later research confirmed this, and found nitrifying bacteria, fluorescent in situ hybridization (FISH) significant differences in abundance between habits (Xia confirmed that the enriched culture only contained et al., 2018). The distribution difference of clades A and B Nitrospira, and the rest were Betaproteobacterium without had a certain relationship with the difference of the ammonia oxidation ability. A polymerase chain reaction encoded genome (Palomo et al., 2018; Koch et al., 2019). (PCR) did not detect any known amoA genes or 16S rRNA Comammox bacteria have recently been identified in genes of AOA and AOB. Metagenomic sequencing found water treatment systems, but their contribution to biologi- cal nitrogen removal remains unclear (Daims et al., 2015; that the relative abundance of Nitrospira in the enriched Van Kessel et al., 2015; Pjevac et al., 2017; Wang et al., culture was 68%–80%. Further enrichment revealed that + – 2017; Zhao et al., 2019). They significantly contribute to Nitrospira could oxidize NH -N to NO -N. Therefore, it 4 3 nitrification in water treatment systems (Pinto et al., 2015; was considered to be a microbial strain with complete Xia et al., 2018), with the abundance ratio of comammox ammonia oxidation ability and was named Candidatus bacteria to total amoA genes in some wastewater treatment Nitrospira inopinata (Ca. N. inopinata). In 2017, Kits et al. Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 3 (2017) obtained the pure culture strain of Ca. N. inopinata (2015) found that the amoA gene in Ca. N. nitrosa and Ca. by enrichment culture, which was also the first pure culture N. nitrificans is different from that of typical ammonia strain of comammox bacteria. oxidizing bacteria, and belongs to two different branches phylogenetic, but is highly similar to pmoA of the methane 2.2 Candidatus Nitrospira nitrosa and Candidatus monooxygenase of Crenohrix polyspora. Therefore, it is Nitrospira nitrificans inferred that the amoA gene of some comammox bacteria in the previous study may be incorrectly classified as Also in 2015, van Kessel et al. (2015) sampled the methane monooxygenase and could be ignored (Daims anaerobic compartment of a trickling filter connected to a et al., 2015; Van Kessel et al., 2015). The discovery of comammox bacteria revolutionized recirculation aquaculture system. Under low dissolved our understanding of the nitrification process, and the oxygen (DO£3.1 μmol/L O ) and oligotrophic conditions, relative contribution of microorganisms to the nitrogen the genus Brocadia of anammox bacteria (AnAOB) and two different Nitrospira genus were enriched by culturing cycle should be reassessed. for 12 months. A high abundance of Nitrospira was rarely seen under low DO conditions. Both NOB species carried the genes (amo and hao) for ammonia oxidation as well as 3 Physiological characteristics of the nxr gene necessary for nitrite oxidation; therefore, comammox bacteria these two strains were confirmed to have the metabolic + – potential to oxidize NH -N to NO -N, and are named 3.1 Nutrient matrix 4 3 Candidatus Nitrospira nitrosa (Ca.N.nitrosa)and Candidatus Nitrospira nitrificans (Ca. N. nitrificans), Comammox bacteria have advantages over traditional respectively. The phylogeny of 16S rRNA genes indicates nitrifying bacteria in oligotrophic substrates, such as low that they belong to lineage II of the genus Nitrospira. ammonia nitrogen and low DO (Kits et al., 2017). In addition to the reported AOA of marine N. maritimus 2.3 Candidatus Nitrospira kreftii SCM1, the ammonia half-saturation constant of AOA and AOB is much higher than that of purified and cultured Ca. N. inopinata, but the affinity of comammox bacteria to Sakoula et al. (2021) used a continuous membrane nitrite is much lower than that of traditional NOB (Kits bioreactor with an effective volume of 5 L containing et al., 2017). Zhao et al. (2021) used urea and nitrite to Ca. N. nitrosa and Ca. N. nitrificans (van Kessel et al., enrich and cultivate comammox bacteria for 390 days to 2015), operated at room temperature and under suitable increase the ratio of amoA gene, indicating that comam- conditions (e.g., pH = 7.5, DO = 50% oxygen saturation) mox bacteria have diverse metabolic potential. for 39 months. They obtained a novel comammox bacteria species, Candidatus Nitrospira kreftti (Ca. N. kreftti), which displayed clear differences in terms of ammonia and 3.2 Environmental factors nitrite oxidation kinetics. For example, Ca. N. kreftti has a higher nitrite affinity. Furthermore, partial inhibition of Environmental conditions, such as DO, pH, and tempera- ammonia oxidation at ammonium concentrations as low as ture have a significant impact on the growth and activity of 25 µM was observed in the bioreactor, indicating that comammox bacteria (Kits et al.,2017; Palomo et al., 2018; differences in ammonium tolerance could potentially be a Roots et al., 2019; Takahashi et al., 2020; Sun et al., 2020). niche-determining factor for different comammox Nitros- The microbial oxidase of comammox bacteria is similar to pira. cytochrome bd-type terminal oxidase, which is generally expressed under extremely low DO concentrations and has 2.4 Summary a higher affinity for DO (Borisov et al., 2011). There are currently no reports on the half-saturation constant of All identified comammox are Nitrospira bacteria, belong- oxygen, but comammox bacteria are more competitive ing to lineage II of the Nitrospira genus, and are under low DO conditions. With increasing DO, AOA and phylogenetically divided into two branches according to AOB activities gradually increase, but comammox bacteria the amoA gene: clade A and clade B. These two clades lose their competitiveness (Palomo et al., 2018; Roots et al., 2019). Sun et al. (2020) found that when the pH was have significant differences in substrate operation and between 6.74 and 8.65, the abundance of comammox metabolism, energy transfer, and environmental adapt- bacteria in coastal wetlands was positively correlated with ability (Palomo et al., 2018). In comammox bacteria pH. In addition, comammox bacteria can show nitrifying enrichment cultures, genome analysis has identified the activity at pH 3–4, indicating that comammox bacteria may amoA gene, encoding AMO; hao encoding HAO; and nxr be able to adapt to low pH (Takahashi et al., 2020). Shi encoding NXR, which can independently perform the et al. found that the abundance of comammox bacteria was complete nitrification process (Daims et al., 2015; Van relatively high in samples collected from wetland ecosys- Kessel et al., 2015; Sakoula et al., 2021). Van Kessel et al. 4 Front. Environ. Sci. Eng. 2022, 16(9): 123 tems. Based on the changes in comammox bacteria species sequester carbon through the reduced tricarboxylic acid diversity in summer and winter, they speculated that (rTCA) cycle. The rTCA cycle is usually the mechanism of temperature may be a key factor affecting the structure of CO fixation by anaerobic or aerobic microorganisms comammox bacteria (Shi et al., 2020). Zhou et al. (2021) (Lücker et al., 2010); compared with the Calvin cycle tested the abundance, activity, and metabolic character- corresponding to AOB, the fixed unit CO of the rTCA istics of nitrifying bacteria in drinking water and waste- cycle consumes less adenosine triphosphate (ATP) and water treatment plants with seasonal changes and found requires less oxygen (Lawson and Lücker, 2018). that the network complex of comammox microorganisms Theoretically, the comammox bacteria oxidation unit in sewage treatment plants was highest in December. NH -N has a shorter metabolic pathway and a higher However, a study by Kits et al. (2017) found that the growth yield than AOB, so it is easier to obtain a optimal growth of Ca. N. inopinata occurred at 37 °C, and competitive advantage under low DO conditions (Costa the optimal enrichment culture temperature was 46 °C. et al., 2006). This indicates that different comammox bacteria can adapt to growth environments of different temperatures. 3.4 Natural habitat distribution 3.3 Enzymes and metabolism Similar to AOA, comammox bacteria have a high affinity + + for NH -N and are suitable for growth under low NH -N 4 4 The comammox bacteria metabolism pathway is complex conditions. There are numerous natural systems suitable and can adapt to different nutrient substrates (Daims et al., for the growth of comammox bacteria. Table 1 shows 2015; Van Kessel et al., 2015; Shen et al., 2016; Kits et al., partial statistics of the distribution of comammox bacteria 2017; Han et al., 2019; Liu et al., 2020a; Wang et al., 2021; in natural ecosystems. Zhao et al., 2021). Liu et al. (2020a) found that comammox Comammox bacteria are widely distributed in nature, bacteria contribute 34%–87% of nitrification in a typical and the distribution further confirms that comammox oligotrophic environment with high pH and low tempera- bacteria like to grow under conditions of low DO and ture along the Yangtze River. Kits et al. (2017) enriched NH -N. AOA was first discovered in the marine environ- and cultivated comammox bacteria under higher tempera- ment. However, although the physiological characteristics ture conditions, demonstrating that comammox micro- of comammox bacteria are similar to those of AOA, Liu organisms can adapt to varying and more extreme et al. (2020b) detected a high abundance of comammox environments. Metagenomic analysis shows that the bacteria in extremely saline sediments, showing that discovered comammox bacteria can use urea as a nitrogen comammox bacteria can adapt to high-salinity environ- source for energy metabolism and biosynthesis (Daims ments, and a distinct differentiation of comammox et al., 2015; Van Kessel et al., 2015; Zhao et al., 2021). Nitrospira groups driven by salinity has been identified Studies have found that comammox bacteria can use (Sun et al. 2021). However, so far, comammox bacteria hydrogen sulfide, sulfide, and fermentation products for have not been found in the ocean (Daims et al., 2015; metabolism (Kits et al., 2017), while trace organic Kuypers, 2017; Xu et al. 2020), indicating that salinity is a pollutants in the environment can be removed through key factor. Whether there are comammox bacteria in metabolism (Han et al., 2019). Some comammox may also marine habitats is an important research direction. have the potential to oxidize formic acid and hydrogen At present, data on the nitrification kinetics of (Palomo et al., 2018), and a variety of antibiotics have been comammox bacteria are derived from pure cultured Ca. N. used to effectively and selectively enrich different strains inopinata. (Kits et al., 2017). Therefore, there are some of comammox bacteria (Wang et al., 2021). In addition, limitations for studying the nitrification kinetics of comammox bacteria have a gene encoding alkaline comammox. With the widespread discovery of comammox phosphatase, which can make it more advantageous bacteria and the versatility of metabolism, research on the under insufficient phosphorus conditions (Shen et al., physiological characteristics of comammox bacteria will 2016). further understanding of the niche characteristics of Comammox bacteria have a complete genome of key comammox bacteria in the biosphere and its relative functional enzymes in the oxidation process of NH -N to contribution to the nitrogen cycle. NO -N, and can complete the whole process of traditional two-step nitrification metabolism itself. The comammox bacteria genome encodes the nitrite reductase gene (nir) 4 Application in wastewater treatment but lacks the nitric oxide reductase gene (nor). In theory, it 4.1 Distribution in water systems produces NO but not N O during biological reactions (Kits et al., 2019). Palomo et al. (2018) found that there In conventional artificial system studies, only the nitrifica- was no pathway related to NO metabolism in the known tion activity of AOM and NOB is evaluated, and the comammox bacteria genome, and the NO reduction presence of comammox bacteria is rarely considered. NOB reaction may not be possible. Comammox bacteria Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 5 Table 1 Comammox bacteria partial distribution in natural ecosystems Growth environment Country Strains Research method Key finding Reference a) Atmospheric fine China N. inopinata PCR The abundance of comammox bacteria in Gao et al., 2016 particles Clone sequencing the atmosphere is less than AOA and greater than AOB. Forest soil, lake Austria; / Metagenome A PCR primer set was developed Pjevac et al., 2017 sediments, freshwater Netherlands specifically for the subunit amoA gene organisms, etc. encoding the unique amoA of comammox bacteria. Forest soil China / qPCR The abundance of comammox bacteria is Hu and He, 2017 very high. When the pH is 4.0–9.0, the abundance exceeds AOB and NOB. Sediments from the China N. inopinata Metagenome; The presence of comammox bacteria was Yu et al., 2018 Yangtze River Estuary N. nitrosa Macrotranscriptome; detected, and a primer set for clade A was N. nitrificans qPCR designed to quantitatively detect the amoA gene of comammox bacteria. Riparian soil China N. nitrosa qPCR; The microbial abundance of comammox Wang et al, 2019 N. nitrificans Correlation analysis in the riparian soil was 10 copies/g, and the abundance of comammox and Nitrospira was significantly correlated under certain conditions. Note: a) qPCR: quantitative polymerase chain reaction. of the Nitrospira genus was mistakenly thought to exist that comammox bacteria may play an important role in widely in artificial systems. Metagenomic detection and wastewater treatment. Sato et al. (2021) used a segmented analysis show that some of these have a full set of reactor to first ammonify organic nitrogen, and then nitrate characteristic genes for ammonia oxidation, indicating into nitrate as a hydroponic fertilizer for plant growth. that they may be comammox bacteria (Pinto et al., 2015). Through 16S rRNA gene sequencing and shotgun Table 2 shows partial statistics on the distribution of metagenomic analysis, the dominant microorganism in comammox bacteria in artificial systems. the nitrification process was confirmed as comammox Comammox bacteria are widely distributed in natural bacteria, and qPCR analysis showed that the expression of and artificial systems (Fig. 2). However, previous calcula- comammox-type AMO was more than 500 times higher tions on the contribution of ammonia oxidizing micro- than that of traditional AMO. Heise et al. (2021) found that organisms in the nitrogen cycle ignored the role of comammox bacteria participated in the removal of NH -N comammox bacteria. Theoretically, the AOM/NOB value at low steady-state NH -N concentrations in an aquaponic in the traditional nitrification process should be between system, indicating that comammox plays an important role two and three (Winkler et al., 2012), but studies have found in this system. that the abundance of Nitrospira in the same habitat Research on the growth mechanisms and physiological exceeds AOM (Zeng et al., 2015), which cannot be characteristics of comammox bacteria can improve the explained by traditional nitrification theories. It has now treatment of urban domestic wastewater. Fig. 3 shows a been demonstrated that some Nitrospira may be comam- common microbial denitrification process in wastewater mox bacteria (Pinto et al., 2015; Tatari et al., 2017). The plants. For urban wastewater partial nitrification-denitrifi- discovery of comammox will cause a reevaluation of the cation (PN/D) and partial nitrification-anaerobic ammonia relative contribution of nitrification in the nitrogen cycle, oxidation (PN/A) denitrification systems, the growth and and the structure of the flora. enrichment of comammox bacteria are one of the important reasons for the destruction of these systems (Wang et al., 4.2 Potential application in wastewater treatment 2020). Controlling the growth of comammox bacteria is an important factor in realizing PN/D or PN/A of urban Wang et al. (2018) found that, among eight wastewater domestic wastewater. Purified and cultured comammox treatment plant samples investigated, activity abundance of bacteria have a low affinity for nitrite (Kits et al., 2017; Xia amoA of the comammox bacteria in six samples was et al., 2018). Meanwhile, comammox bacteria and significantly higher than or comparable to that of AOB, anammox bacteria can form copolymers under hypoxic even reaching 24 times more in some wastewater plants. conditions (Van Kessel et al., 2015; Gottshall et al., 2021; The abundance of comammox bacteria to total amoA genes Shao and Wu, 2021). In theory, the nitrite oxidation in drinking water plants and AAO wastewater treatment activity of comammox bacteria can be inhibited by plants is up to 46%–100% (Zhou et al., 2021), indicating controlling conditions to achieve stable PN/A. In the PN/ 6 Front. Environ. Sci. Eng. 2022, 16(9): 123 Table 2 Comammox bacteria partial distribution in artificial systems Growth environment Country Species Research method Key finding Reference Wastewater treatment China N. inopinata Metagenome; Comammox bacteria abundance accounts Chao et al., 2016 plants (WWTPs) 16S rRNA for£0.1%. It is speculated that the contribution of comammox bacteria nitrification is small in the sewage treatment process. Drinking water Singapore; N. inopinata Metagenome Comammox bacteria are widely distributed in Wang et al., 2017 systems China; N. nitrosa drinking water systems and coexist with traditional United States N. nitrificans AOM. The nitrification of drinking water systems may be mainly completed by comammox bacteria. WWTPs United States N. nitrosa Metagenome To achieve enrichment of Ca. N. nitrosa, it has a Kits et al., 2017 higher affinity for urea. WWTPs United States N. inopinata Metagenome; A primer set and qPCR targeting clade A were Camejo et al., United Kingdom N. nitrosa qPCR designed; comammox bacteria prefer long sludge age 2017 N. nitrificans and attached growth, and the increase in abundance in the same habitat has no correlation with the decrease in AOB and NOB abundance. Urban lake China / 16S rRNA Comammox bacteria are widely distributed in Xu et al., 2020 urban lakes, eutrophication may inhibit its growth. Acidic soils Japan / 16S rRNA When the pH is 3–4, nitrification activity of Takahashi et al., comammox bacteria is still detected. 2020 A continuous Netherlands N. Kreftii FISH; They obtained a novel comammox bacteria species, Sakoula et al., membrane Metagenome; Ca. N. kreftti. Moreover, they think differences in 2021 bioreactor ammonium tolerance could potentially be a niche-determining factor for different comammox Nitrospira. Lab-scale PN/A SBR China / 16S rRNA The amoA gene of comammox bacteria in the Shao and Wu, Reactor qPCR PN/A system that has been running stably for more 2021 than 1,000 days accounted for 89.27.9%, achieving synergistic denitrification under hypoxic conditions. Aquaponic system Germany / 16S rRNA Comammox bacteria are found in the high- Heise et al., 2021 efficiency aquaponic symbiosis system, which participate in the removal of NH -N at low steady-state NH -N concentrations. A process, NH -N and DO continuously decrease as Compared with PN/A, the DEAMOX process has many particles or biofilms develop, which may lead to the advantages, such as a more stable accumulation of NO -N, enrichment of comammox bacteria (Wang et al., 2020), no complicated control, and theoretical 100% deep competing with AOB and reducing the total nitrogen denitrification. In this process, comammox bacteria are removal rate, instead of the traditional NOB proliferation used to couple partial denitrification-anaerobic ammonia effect. oxidation to develop a new type of denitrification process. In some wastewater treatment plants, comammox Hypoxic nitrification reduces aeration energy consump- bacteria account for a relatively high proportion of tion, and anoxic partial denitrification-anaerobic ammonia activated sludge (Zhou et al., 2021). An important research oxidation saves carbon sources (Fig. 4). The process is direction in wastewater treatment is how to use the stable and easy to control, with a low sludge output and a physiological characteristics of comammox bacteria to reduction in greenhouse gas emissions, and may be more further reduce sewage treatment costs and improve suitable for saving energy, reducing consumption, and treatment effects. Using comammox bacteria to treat low deep denitrification (Xu et al., 2021). NH -N municipal sewage under low DO conditions can Traditional biological denitrification is usually achieved reduce the aeration; therefore, the energy consumption. through nitrification and denitrification, producing N Oin The generation of sludge can also be reduced, as well as the the process. N O is an important greenhouse gas. cost of post-sludge treatment and disposal. With the recent Comammox bacteria have no N O biosynthesis pathway; research and development of partial denitrification (NO - therefore, using comammox bacteria as the main reaction N ! NO -N) and the anaerobic ammonia oxidation microorganism in the nitrification process may greatly coupling process (DEAMOX), simultaneous treatment of reduce N O emissions. Comammox bacteria can oxidize – + NO -N and NH -N in the same reactor has been realized. low ammonia nitrogen to nitrate nitrogen under low DO 3 4 Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 7 Fig. 2 Ternary plot of the proportions of comammox, AOB, and AOA in 111 metagenomic data sets of different environmental samples from the NCBI SRA database (Xia et al. 2018). Fig. 3 Common microbial denitrification processes in wastewater treatment plants. (DNRA: dissimilatory nitrate reduction to ammonium). conditions. Low DO meets the reaction conditions of treatment. All comammox that have been discovered are simultaneous denitrification (Holman and Wareham, Nitrospira bacteria, belonging to lineage II of the 2005). Simultaneous nitrification and denitrification can Nitrospira genus. The affinity of comammox bacteria to reduce internal circulation and aeration energy consump- ammonium is higher and is also slower growing than tion and save space, while the nitrification process, conventional AOB/NOB, so better adapted to oligotrophic avoiding the accumulation of nitrite, can be used to treat conditions. Furthermore, comammox bacteria have a micro-polluted drinking water, improve treatment effi- complex pathway and can live in many adverse environ- ciency, and avoid the potential risk of nitrite production. ments, as demonstrated by their wide distribution in natural and artificial systems. Coupling with DEAMOX or enriching in oligotrophic conditions can promote total 5 Conclusions and outlook nitrogen removal, thereby reducing both costs and N O emissions. This review summarizes the discovery, physiological The discovery of comammox bacteria has important characteristics, and ecological distribution of comammox significance and research value for calculating and bacteria, and proposes potential applications in wastewater evaluating the relative contribution of nitrification in the 8 Front. Environ. Sci. Eng. 2022, 16(9): 123 Fig. 4 Application of comammox bacteria in wastewater treatment. (DB: denitrifying bacteria). microbial nitrogen cycle. To detect the presence and be developed (e.g., AOB/AOA/NOB/comammox bac- abundance of comammox bacteria using the amoA gene of teria), and the accuracy and sensitivity of specific primers comammox bacteria, a variety of specific primers have need to be further improved; 2) In wastewater treatment been developed to identify and quantify comammox plants, the quantity of comammox bacteria as a proportion bacteria of different branches and species levels. However, of nitrifying bacteria varies, and the relative contribution is the accuracy and sensitivity of these need to be further not clear; evaluation and calculation of this should be improved. strengthened in the future; 3) Comammox bacteria are used Comammox bacteria are of great significance in both to couple DEAMOX to develop a new nitrogen removal natural and artificial systems, but the niche differences and process, the potential of comammox bacteria in more influencing factors between them and AOB, AOA, NOB, sustainable nitrogen removal techniques could be assessed and other microorganisms remain unclear, and may be a from the point of view of engineering applications. research hotspot for microbial applications in the future. At Acknowledgements This research project was financially supported by the present, our understanding of comammox bacteria is Foundation for Innovation Research Groups of the National Natural Science limited, and the in situ activity of comammox bacteria Foundation of China (No. 62021003); Biological Wastewater Treatment and cannot be fully evaluated. There is an urgent need to Process Control Technology, Beijing International Science and technology develop isolation and purification methods to study the Cooperation Base; and the Founding projects of Beijing Municipal physiological characteristics of microorganisms at the Commission of Education. single-cell level, and to explore the coupling mechanism Open Access This article is licensed under a Creative Commons between comammox bacteria and traditional nitrification Attribution 4.0 International License, which permits use, sharing, adaptation, and denitrification. For the treatment of micro-polluted distribution and reproduction in any medium or format, as long as you give water sources, it is necessary to further explore the appropriate credit to the original author(s) and the source, provide a link to the enrichment and operating conditions of comammox 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 bacteria. In wastewater treatment, the use of comammox Commons licence, unless indicated otherwise in a credit line to the material. bacteria can reduce aeration energy consumption, green- If material is not included in the article’s Creative Commons licence and your house gas N O emissions, and sludge production, while intended use is not permitted by statutory regulation or exceeds the permitted improving deep denitrification efficiency. It has a broad use, you will need to obtain permission directly from the copyright holder. To application potential and may become a new biological view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. denitrification process in the future. The following areas should be given priority in future studies on comammox bacteria: 1) Efficient and accurate References methods that can identify the contribution of diverse microorganisms from similar functional microbes should Annavajhala M K, Kapoor V, Santo-Domingo J, Chandran K (2018). Shaoping Luo et al. Complete ammonia oxidizing bacteria in wastewater treatment 9 Comammox functionality identified in diverse engineered biological Kits K D, Sedlacek C J, Lebedeva E V, Han P, Bulaev A, Pjevac P, wastewater treatment systems. Environmental Science & Technology Daebeler A, Romano S, Albertsen M, Stein L Y, Daims H, Wagner M Letters, 5(2): 110–116 (2017). Kinetic analysis of a complete nitrifier reveals an oligotrophic Arp D J, Sayavedra-Soto L A, Hommes N G (2002). Molecular biology lifestyle. Nature, 549(7671): 269–272 and biochemistry of ammonia oxidation by Nitrosomonas europaea. Knief C, Kolb S, Bodelier P L E, Lipski A, Dunfield P F (2006). The Archives of Microbiology, 178(4): 250–255 active methanotrophic community in hydromorphic soils changes in Borisov V B, Gennis R B, Hemp J, Verkhovsky M I (2011). The response to changing methane concentration. Environmental Micro- cytochrome bd respiratory oxygen reductases. Biochimica et biology, 8(2): 321–333 Biophysica Acta (BBA) - Bioenergetics, 1807(11): 1398–1413 Koch H, van Kessel M A H J, Lücker S (2019). Complete nitrification: Camejo P Y, Santo Domingo J, McMahon K D, Noguera D R (2017). insights into the ecophysiology of comammox Nitrospira. Applied Genome-enabled insights into the ecophysiology of the comammox Microbiology and Biotechnology, 103(1): 177–189 bacterium “Candidatus Nitrospira nitrosa”. mSystems, 2(5): Könneke M, Bernhard A E, de la Torre J R, Walker C B, Waterbury J B, e00059–e17 Stahl D A (2005). Isolation of an autotrophic ammonia-oxidizing Chao Y Q, Mao Y P, Yu K, Zhang T (2016). Novel nitrifiers and marine archaeon. Nature, 437(7058): 543–546 comammox in a full-scale hybrid biofilm and activated sludge reactor Kuypers M M M (2017). Microbiology: A fight for scraps of ammonia. revealed by metagenomic approach. Applied Microbiology and Nature, 549(7671): 162–163 Biotechnology, 100(18): 8225–8237 Kuypers M M M, Marchant H K, Kartal B (2018). The microbial Costa E, Pérez J, Kreft J U (2006). Why is metabolic labour divided in nitrogen-cycling network. Nature Reviews. Microbiology, 16(5): nitrification? Trends in Microbiology, 14(5): 213–219 263–276 Daims H, Lebedeva E V, Pjevac P, Han P, Herbold C, Albertsen M, Lawson C E, Lücker S (2018). Complete ammonia oxidation: An Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard R H, important control on nitrification in engineered ecosystems? Current von Bergen M, Rattei T, Bendinger B, Nielsen P H, Wagner M Opinion in Biotechnology, 50: 158–165 (2015). Complete nitrification by Nitrospira bacteria. Nature, 528 Liu S, Wang H, Chen L, Wang J, Zheng M, Liu S, Chen Q, Ni J (2020a). (7583): 504–509 Comammox Nitrospira within the Yangtze River continuum: Erwin D P, Erickson I K, Delwiche M E, Colwell F S, Strap J L, community, biogeography, and ecological drivers. The ISME Crawford R L (2005). Diversity of oxygenase genes from methane- Journal, 14(10): 2488–2504 and ammonia-oxidizing bacteria in the Eastern Snake River Plain Liu Z, Zhang C, Wei Q, Zhang S, Quan Z, Li M (2020b). Temperature aquifer. Applied and Environmental Microbiology, 71(4): 2016–2025 and salinity drive comammox community composition in mangrove Gao J F, Fan X Y, Pan K L, Li H Y, Sun L X (2016). Diversity, ecosystems across southeastern China. The Science of the total abundance and activity of ammonia-oxidizing microorganisms in fine environment, 742: 140456 particulate matter. Scientific Reports, 6(1): 38785 Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei Gottshall E Y, Bryson S J, Cogert K I, Landreau M, Sedlacek C J, Stahl T, Damsté J S, Spieck E, Le Paslier D, Daims H (2010). A Nitrospira D A, Daims H, Winkler M (2021). Sustained nitrogen loss in a metagenome illuminates the physiology and evolution of globally symbiotic association of comammox Nitrospira and anammox important nitrite-oxidizing bacteria. Proceedings of the National bacteria. Water Research, 202(1): 117426 Academy of Sciences of the United States of America, 107(30): Han P, Yu Y, Zhou L, Tian Z, Li Z, Hou L, Liu M, Wu Q, Wagner M, 13479–13484 Men Y (2019). Specific micropollutant biotransformation pattern by Palomo A, Pedersen A G, Fowler S J, Dechesne A, Sicheritz-Pontén T, the comammox bacterium Nitrospira inopinata. Environmental Smets B F (2018). Comparative genomics sheds light on niche Science & Technology, 53(15): 8695–8705 differentiation and the evolutionary history of comammox Nitros- Heise J, Müller H, Probst A J, Meckenstock R U (2021). Ammonium pira. The ISME Journal, 12(7): 1779–1793 removal in aquaponics indicates participation of comammox Pinto A J, Marcus D N, Ijaz U Z, Bautista-de Lose Santos Q M, Dick G J, Nitrospira. Current Microbiology, 78(3): 894–903 Raskin L (2015). Metagenomic evidence for the presence of Holman J B, Wareham D G (2005). COD, ammonia and dissolved comammox Nitrospira-like bacteria in a drinking water system. oxygen time profiles in the simultaneous nitrification/denitrification MSphere, 1(1): e00054–e15 process. Biochemical Engineering Journal, 22(2): 125–133 Pjevac P, Schauberger C, Poghosyan L, Herbold C W, van Kessel M A Hu H W, He J Z (2017). Comammox–A newly discovered nitrification H J, Daebeler A, Steinberger M, Jetten M S M, Lücker S, Wagner M, process in the terrestrial nitrogen cycle. Journal of Soils and Daims H (2017). AmoA-targeted polymerase chain reaction primers 17(12): 2709–2717 Sediments, for the specific detection and quantification of comammox Nitrospira Jia Z J, Kikuchi H, Watanabe T, Asakawa S, Kimura M (2007). in the environment. Frontiers in Microbiology, 8: 1508 Molecular identification of methane oxidizing bacteria in a Japanese Roots P, Wang Y, Rosenthal A F, Griffin J S, Sabba F, Petrovich M, rice field soil. Biology and Fertility of Soils, 44(1): 121–130 Yang F, Kozak J A, Zhang H, Wells G F (2019). Comammox Kits K D, Jung M Y, Vierheilig J, Pjevac P, Sedlacek C J, Liu S, Herbold Nitrospira are the dominant ammonia oxidizers in a mainstream low C, Stein L Y, Richter A, Wissel H, Brüggemann N, Wagner M, dissolved oxygen nitrification reactor. Water Research, 157: 396–405 Daims H (2019). Low yield and abiotic origin of N O formed by the 2 Sakoula D, Koch H, Frank J, Jetten M S M, van Kessel M A H J, Lücker complete nitrifier Nitrospira inopinata. Nature Communications, 10 S (2021). Enrichment and physiological characterization of a novel (1): 1836 comammox Nitrospira indicates ammonium inhibition of complete 10 Front. Environ. Sci. Eng. 2022, 16(9): 123 nitrification. The ISME journal, 15(4): 1010–1024 Wang S Y, Pi Y L, Jiang Y Y, Pan H W, Wang X X, Wang X M, Zhou Z Sato Y, Tanaka E, Hori T, Futamata H, Murofushi K, Takagi H, Akachi M, Zhu G B (2019). Nitrate reduction in the reed rhizosphere of a T, Miwa T, Inaba T, Aoyagi T, Habe H (2021). Efficient conversion riparian zone: From functional genes to activity and contribution. of organic nitrogenous wastewater to nitrate solution driven by Environmental Research, 180(6): 108867 comammox Nitrospira. Water Research, 197: 117088 Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017). Shao Y H, Wu J H (2021). comammox Nitrospira species dominate in an Comammox in drinking water systems. Water Research, 116: 332– efficient partial nitrification-anammox bioreactor for treating ammo- nium at low loadings. Environmental Science & Technology, 55(3): Wang Y L, Zhao R X, Liu L, Li B, Zhang T (2021). Selective enrichment 2087–2098 of comammox from activated sludge using antibiotics. Water Shen Y C, Hu Y N, Shaw G C (2016). Expressions of alkaline Research, 197: 117087 phosphatase genes during phosphate starvation are under positive Wang Z, Zhang L, Zhang F Z, Jiang H, Ren S, Wang W, Peng Y Z influences of multiple cell wall hydrolase genes in Bacillus subtilis. (2020). Nitrite accumulation in comammox-dominated nitrification- The Journal of General and Applied Microbiology, 62(2): 106–109 reactors: Effects of DO concentration and hydro- denitrification Shi Y, Jiang Y Y, Wang S Y, Wang X M, Zhu G B (2020). xylamine addition. Journal of Hazardous Materials, 384: 121375 Biogeographic distribution of comammox bacteria in diverse Winkler M K, Bassin J P, Kleerebezem R, Sorokin D Y, van Loosdrecht terrestrial habitats. Science of the Total Environment, 717: 137257 M C (2012). Unravelling the reasons for disproportion in the ratio of Steenbergh A K, Meima M M, Kamst M, Bodelier P L E (2010). AOB and NOB in aerobic granular sludge. Applied Microbiology Biphasic kinetics of a methanotrophic community is a combination of and Biotechnology, 94(6): 1657–1666 growth and increased activity per cell. FEMS Microbiology Ecology, Winogradsky S (1890). The morphology of the contributions of 71(1): 12–22 nitrification system. Archives of Biological Sciences, 4: 257–275 Sun D Y, Tang X F, Zhao M Y, Zhang Z X, Hou L J, Liu M, Wang B Z, Xia F, Wang J G, Zhu T, Zou B, Rhee S K, Quan Z X (2018). Ubiquity Klümper U, Han P (2020). Distribution and diversity of comammox and diversity of complete ammonia oxidizers (comammox). Applied Nitrospira in coastal wetlands of China. Frontiers in Microbiology, and Environmental Microbiology, 84(24): e01390–e18 11: 589268 Xu S Y, Wu X L, Lu H J (2021). Overlooked nitrogen-cycling Sun D Y, Zhao M Y, Tang X F, Liu M, Hou L J, Zhao Q, Li J, Gu J D, microorganisms in biological wastewater treatment. Frontiers of Han P (2021). Niche adaptation strategies of different clades of Environmental Science & Engineering, 15(6): 133 comammox Nitrospira in the Yangtze Estuary. International Xu Y F, Lu J, Wang Y C, Liu G L, Wan X Q, Hua Y M, Zhu D W, Zhao J Biodeterioration & Biodegradation, 164: 105286 W (2020). Diversity and abundance of comammox bacteria in the Takahashi Y, Fujitani H, Hirono Y, Tago K, Wang Y, Hayatsu M, sediments of an urban lake. Journal of Applied Microbiology, 128(6): Tsuneda S (2020). Enrichment of comammox and nitrite-oxidizing 1647–1657 Nitrospira from acidic soils. Frontiers in Microbiology, 11: 1737 Yu C, Hou L, Zheng Y, Liu M, Yin G, Gao J, Liu C, Chang Y, Han P Tatari K, Musovic S, Gülay A, Dechesne A, Albrechtsen H, Smets B F (2018). Evidence for complete nitrification in enrichment culture of (2017). Density and distribution of nitrifying guilds in rapid sand tidal sediments and diversity analysis of clade a comammox filters for drinking water production: Dominance of Nitrospira spp. Nitrospira in natural environments. Applied Microbiology and Water Research, 127: 239–248 Biotechnology, 102(21): 9363–9377 Teske A, Alm E, Regan J M, Toze S, Rittmann B E, Stahl D A (1994). Zeng W, Zhang L M, Wang A Q, Zhang J, Peng Y Z, Duan J L (2015). Evolutionary relationships among ammonia- and nitrite-oxidizing Community structures and population dynamics of nitrifying bacteria bacteria. Journal of Bacteriology, 176(21): 6623–6630 in activated sludges of wastewater treatment plants. China Environ- Van Kessel M A H J, Speth D R, Albertsen M, Nielsen P H, Op den mental Science, 35(11): 3257–3265 (in Chinese) Camp H J M, Kartal B, Jetten M S M, Lücker S (2015). Complete Zhao Y X, Hu J J, Yang W L, Wang J Q, Jia Z J, Zheng P, Hu B L (2021). nitrification by a single microorganism. Nature, 528(7583): 555–559 The long-term effects of using nitrite and urea on the enrichment of Vigliotta G, Nutricati E, Carata E, Tredici S M, De Stefano M, Pontieri P, comammox bacteria. Science of the Total Environment, 755(Pt 2): Massardo D R, Prati M V, De Bellis L, Alifano P (2007). Clonothrix fusca Roze 1896, a filamentous, sheathed, methanotrophic γ- Zhao Z, Huang G, He S, Zhou N, Wang M, Dang C, Wang J, Zheng M proteobacterium. Applied and Environmental Microbiology, 73 (2019). Abundance and community composition of comammox (11): 3556–3565 bacteria in different ecosystems by a universal primer set. Science of Wang M Y, Huang G H, Zhao Z R, Dang C Y, Liu W, Zheng M S the Total Environment , 691: 146–155 (2018). Newly designed primer pair revealed dominant and diverse Zhou X, Li B, Wei J, Ye Y, Xu J, Chen L, Lu C (2021). Temperature comammox amoA gene in full-scale wastewater treatment plants. influenced the comammox community composition in drinking water Bioresource Technology, 270: 580–587 and wastewater treatment plants. Microbial Ecology, 82(4): 870–884

Journal

Frontiers of Environmental Science & Engineering – Springer Journals

Published: Sep 1, 2022

Keywords: Complete ammonia oxidizing (comammox) bacteria; Nitrogen cycle; Physiological characteristics; Wastewater treatment

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