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The nitrite oxidizing bacterial genus Ca. Nitrotoga was only recently discovered to be widespread in freshwater systems; however, limited information is currently available on the environmental factors and seasonal effects that influence its distribution in lakes. In a one-year study in a dimictic lake, based on monthly sampling along a vertical profile, the droplet digital PCR quantification of Ca. Nitrotoga showed a strong spatio-temporal patchiness. A correlation ana-lysis with environmental parameters revealed that the abundance of Ca. Nitrotoga correlated with dissolved oxygen and ammonium, suggesting that the upper hypolimnion of the lake is the preferred habitat.

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With the increasing complexity of influent composition in wastewater treatment plants, the potential stimulating effects of refractory organic matter in wastewater on growth characteristics and genera conversion of nitrifying bacteria (ammonium-oxidizing bacteria [AOB] and nitrite-oxidizing bacteria [NOB]) need to be further investigated. In this study, domestic wastewater was co-treated with landfill leachate in the lab-scale reactor, and the competition and co-existence of NOB genera Nitrotoga and Nitrospira were observed. The results demonstrated that the addition of landfill leachate could induce the growth of Nitrotoga, whereas Nitrotoga populations remain less competitive in domestic wastewater operation. In addition, the refractory organic matter in the landfill leachate also would have a potential stimulating effect on the maximum specific growth rate of AOB genus Nitrosomonas (µmax, aob). The µmax, aob of Nitrosomonas in the control group was estimated to be 0.49 d-1 by fitting the ASM model, and the µmax, aob reached 0.66-0.71 d-1 after injection of refractory organic matter in the landfill leachate, while the maximum specific growth rate of NOB (µmax, nob) was always in the range of 1.05-1.13 d-1. These findings have positive significance for the understanding of potential stimulation on nitrification processes and the stable operation of innovative wastewater treatment process.

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Landfill leachate, due to its recalcitrant nature and toxicity, poses a serious environmental threat, which requires the implementation of effective treatment processes. In this work, a full-scale treatment system consisting of two Sequencing Batch Reactors (SBRs) was used for the processing of landfill leachate of intermediate to mature age (BOD/COD ratio of 0.16). Biosystem operation resulted in BOD5, COD and TKN removal efficiencies of 81%, 39% and 76%, respectively, whereas the low residual NO3--N concentration in the effluent (4.01 ± 0.10 mg/L) was indicative of the efficient denitrification process. Assessment of hydrolytic potential of activated sludge revealed high endocellular and extracellular lipase activities, which reached values up to 206 and 141 U/g protein respectively, possibly as the consequence of plastics degradation during maturation process. Implementation of Illumina sequencing indicated the predominance of Alphaproteobacteria, accompanied by members of Bacteroidetes, Betaproteobacteria and Chloroflexi. Paracoccus was the predominant genus identified, followed by representatives of the genera Bellilinea, Flavobacterium, Thauera and Truepera. Nitrosomonas was the major ammonia-oxidizing bacterium (AOB), while nitrite oxidation was mainly achieved by the uncultured nitrite-oxidizing bacterium (NOB) Candidatus Nitrotoga.

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Due to the key role of nitrite in novel nitrogen removal systems, nitrite oxidizing bacteria (NOB) have been receiving increasing attention. In this study, the coexistence and interactions of nitrifying bacteria were explored at decreasing solids retention times (SRTs). Four 5-week washout experiments were carried out in laboratory-scale (V = 10 L) sequencing batch reactors (SBRs) with mixed liquor from two full-scale activated sludge systems (continuous flow vs SBR). During the experiments, the SRT was gradually reduced from the initial value of 4.0 d to approximately 1.0 d. The reactors were operated under limited dissolved oxygen conditions (set point of 0.6 mg O2/L) and two process temperatures: 12 °C (winter) and 20 °C (summer). At both temperatures, the progressive SRT reduction was inefficient for the out-selection of both canonical NOB and comammox Nitrospira. However, the dominant NOB switched from Nitrospira to Ca. Nitrotoga, whereas the dominant AOB was always Nitrosomonas. The results of this study are important for optimizing NOB suppression strategies in the novel N removal processes, which are based on nitrite accumulation.

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[This corrects the article DOI: 10.3389/fmicb.2021.709371.].

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Mainstream nitrogen removal by partial nitritation/anammox (PN/A) can realize energy and cost savings for sewage treatment. Selective suppression of nitrite oxidizing bacteria (NOB) remains a key bottleneck for PN/A implementation. A rotating biological contactor was studied with an overhead cover and controlled air/N2 inflow to regulate oxygen availability at 20 °C. Biofilm exposure to dissolved oxygen concentrations < 0.51 ± 0.04 mg O2 L-1 when submerged in the water and < 1.41 ± 0.31 mg O2 L-1 when emerged in the headspace (estimated), resulted in complete and long-term NOB suppression with a low relative nitrate production ratio of 10 ± 4%. Additionally, weekly biofilm stressor treatments with free ammonia (FA) (29 ± 1 mg NH3-N L-1 for 3 h) could improve the NOB suppression while free nitrous acid treatments had insufficient effect. This study demonstrated the potential of managing NOB suppression in biofilm-based systems by oxygen control and recurrent FA exposure, opening opportunities for resource efficient nitrogen removal.

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Nitrogen cycling microbes, including nitrite-oxidizing bacteria (NOB), perform critical ecosystem functions that help mitigate anthropogenic stresses and maintain ecosystem health. Activity of these beneficial nitrogen cycling microbes is dictated in part by the microorganisms' response to physicochemical conditions, such as temperature, pH, and nutrient availability. NOB from the newly described Candidatus Nitrotoga genus have been detected in a wide range of habitats across the globe, yet only a few organisms within the genus have been physiologically characterized. For freshwater systems where NOB are critical for supporting aquatic life, Ca. Nitrotoga have been previously detected but little is known about the physiological potential of these organisms or their response to changing environmental conditions. Here, we determined functional response to environmental change for a representative freshwater species of Ca. Nitrotoga (Ca. Nitrotoga sp. CP45, enriched from a Colorado river). The physiological findings demonstrated that CP45 maintained nitrite oxidation at pH levels of 5-8, at temperatures from 4 to 28°C, and when incubated in the dark. Light exposure and elevated temperature (30°C) completely halted nitrite oxidation. Ca. Nitrotoga sp. CP45 maintained nitrite oxidation upon exposure to four different antibiotics, and potential rates of nitrite oxidation by river sediment communities were also resilient to antibiotic stress. We explored the Ca. Nitrotoga sp. CP45 genome to make predictions about adaptations to enable survival under specific conditions. Overall, these results contribute to our understanding of the versatility of a representative freshwater Ca. Nitrotoga sp. Identifying the specific environmental conditions that maximize NOB metabolic rates may ultimately direct future management decisions aimed at restoring impacted systems.

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Many biotechnological applications deal with nitrification, one of the main steps of the global nitrogen cycle. The biological oxidation of ammonia to nitrite and further to nitrate is critical to avoid environmental damage and its functioning has to be retained even under adverse conditions. Bacteria performing the second reaction, oxidation of nitrite to nitrate, are fastidious microorganisms that are highly sensitive against disturbances. One important finding with relevance for nitrogen removal systems was the discovery of the mainly cold-adapted Cand. Nitrotoga, whose activity seems to be essential for the recovery of nitrite oxidation in wastewater treatment plants at low temperatures, e.g., during cold seasons. Several new strains of this genus have been recently described and ecophysiologically characterized including genome analyses. With increasing diversity, also mesophilic Cand. Nitrotoga representatives have been detected in activated sludge. This review summarizes the natural distribution and driving forces defining niche separation in artificial nitrification systems. Further critical aspects for the competition with Nitrospira and Nitrobacter are discussed. Knowledge about the physiological capacities and limits of Cand. Nitrotoga can help to define physico-chemical parameters for example in reactor systems that need to be run at low temperatures. KEY POINTS: • Characterization of the psychrotolerant nitrite oxidizer Cand. Nitrotoga • Comparison of the physiological features of Cand. Nitrotoga with those of other NOB • Identification of beneficial environmental/operational parameters for proliferation.

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Numerous wastewater treatment processes are designed by engineers to achieve specific treatment goals. However, the impact of these different process designs on bacterial community composition is poorly understood. In this study, 24 different municipal wastewater treatment facilities (37 bioreactors) with various system designs were analyzed by sequencing of PCR-amplified 16S rRNA gene fragments. Although a core microbiome was observed in all of the bioreactors, the overall microbial community composition (analysis of molecular variance; P = 0.001) as well as that of a specific population of Nitrosomonas spp. (P = 0.04) was significantly different between A/O (anaerobic/aerobic) systems and conventional activated sludge (CAS) systems. Community α-diversity (number of observed operational taxonomic units [OTUs] and Shannon diversity index) was also significantly higher in A/O systems than in CAS systems (Wilcoxon; P < 2 × 10-16). In addition, wastewater bioreactors with short mean cell residence time (<2 days) had very low community α-diversity and fewer nitrifying bacteria compared to those of other system designs. Nitrospira spp. (0.71%) and Nitrotoga spp. (0.41%) were the most prominent nitrite-oxidizing bacteria (NOB); because these two genera were rarely prominent at the same time, these populations appeared to be functionally redundant. Weak evidence (AOB:NOB « 2; substantial quantities of Nitrospira sublineage II) was also obtained suggesting that complete ammonia oxidation by a single organism was occurring in system designs known to impose stringent nutrient limitation. This research demonstrates that design decisions made by wastewater treatment engineers significantly affect the microbiome of wastewater treatment bioreactors. IMPORTANCE Municipal wastewater treatment facilities rely on the application of numerous "activated sludge" process designs to achieve site-specific treatment goals. A plethora of microbiome studies on municipal wastewater treatment bioreactors have been performed previously; however, the role of process design on the municipal wastewater treatment microbiome is poorly understood. In fact, wastewater treatment engineers have attempted to control the microbiome of wastewater bioreactors for decades without sufficient empirical evidence to support their design paradigms. Our research demonstrates that engineering decisions with respect to system design have a significant impact on the microbiome of wastewater treatment bioreactors.

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This study aimed to understand the effect of different dissolved oxygen (DO) concentrations on the abundance and performance of nitrifying bacteria in full-scale wastewater treatment bioreactors, particularly during the winter when nitrifying bacterial activity is often negligible. Biomass samples were collected from three parallel full-scale bioreactors with low DO concentrations (<1.3 mg/ L) and from two full-scale bioreactors with higher DO concentrations (~4.0 and ~2.3 mg/ L). The relative abundance of nitrifying bacteria was determined by sequencing of PCR-amplified 16S rRNA gene fragments. In the three bioreactors with low DO concentrations, effluent ammonia concentrations sharply increased with a decline in temperature below approximately 17 °C, while the bioreactors with high DO concentrations showed stable nitrification regardless of temperature. Even with the decline in nitrification during the winter in the three low DO bioreactors, the relative abundance of ammonia oxidizing bacteria (mostly Nitrosomonas spp.) was curiously maintained. The relative abundance of nitrite oxidizing bacteria was similarly maintained, although there were substantial seasonal fluctuations in the relative abundance values of Nitrospira spp. versus Nitrotoga spp. This research suggests that nitrification activity can be controlled during the winter via DO to produce better effluent quality with high DO concentrations or to reduce aeration costs with a concomitant decline in nitrification activity.

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Nitrifying biofilms developed in brackish water are reported to be more robust to salinity changes than freshwater biofilms. This makes them a promising strategy for water treatment systems with variable salinity, such as recirculating aquaculture systems for Atlantic salmon. However, little is known about the time required for nitrification start-up in brackish water or the microbial community dynamics. To investigate the development of nitrifying biofilms at intermediate salinity, we compared the startup of moving bed biofilm reactors with virgin carriers in brackish- (12‰ salinity) and freshwater. After 60 days, the brackish water biofilm had half the nitrification capacity of the freshwater biofilm, with a less diverse microbial community, lower proportion of nitrifiers, and a significantly different nitrifying community composition. Nitrosomonas and Nitrosospira-like bacteria were the main ammonia oxidizers in the brackish water biofilms, whereas Nitrosomonas was dominant in freshwater biofilms. Nitrotoga was the dominant nitrite oxidizer in both treatments. Despite the lower nitrification capacity in the brackish water treatment, the low ammonia and nitrite concentration with rapidly increasing nitrate concentration indicated that complete nitrification was established in both reactors within 60 days. The results suggest that biofilms develop nitrification in brackish water in comparable time as in freshwater, and brackish start-up can be a strategy for bioreactors with varying salinity.

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Sludge treatment using free ammonia (FA) is an innovative approach that was recently reported effective achieving stable mainstream nitrogen removal via the nitrite pathway. This study aims to investigate the adaptation of nitrifying community and the response of nitrification performance to high-level of FA exposure under real wastewater conditions. Two parallel lab-scale sequencing batch reactors were operated and fed with real municipal wastewater, with one receiving sludge treatment by FA and another as a control. While the FA approach rapidly achieved partial nitrification with a nitrite accumulation ratio (NAR) of approximately 60%, the partial nitrification eventually failed due to nitrite-oxidizing bacteria (NOB) adaptation to FA inactivation. NOB activity in the inoculum was suppressed by 82% after exposure to FA at ~220 mg NH3-N/L. However, towards the end of the experiments, significantly higher NOB activities were observed after exposure to the same level of FA. Distinct behaviours of NOB observed in batch tests during the study supported the reactor operational data and strongly suggested the adaptation of NOB under the FA stress. Furthermore, microbial community analysis revealed the underlying mechanism of the observed adaptation: the dominant NOB changed from Nitrospira to Candidatus Nitrotoga. It is for the first time shown that Ca. Nitrotoga are highly resistant to FA inhibition and inactivation in comparison to Nitrospira and Nitrobacter. In addition, while the Nitrosomonas genus was always the dominant ammonia-oxidizing bacteria (AOB) throughout the study, different shift in a species level was observed.

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Nitrification is an essential process for N removal in activated sludge to avoid toxicity of ammonium and nitrite. Besides Nitrospira, "Candidatus Nitrotoga" has been identified as a key nitrite-oxidizing bacterium (NOB) performing the second step of nitrification, nitrite oxidation to nitrate, in wastewater treatment plants (WWTPs). However, the driving forces for the dominance of Nitrotoga in certain plants have often remained unclear and could not be explained solely by temperature effects. In this study, we characterized the physiology of the ammonium-dependent Nitrotoga sp. BS with regard to temperature and pH variations and evaluated its competitiveness against Nitrospira defluvii Both NOB originated from the same WWTP and shared a comparable pH optimum of 7.3. Based on these results, coculturing experiments with these NOB were performed in batch reactors operated at either 17°C or 22°C to compare their abundances under optimal (pH 7.4) or suboptimal (pH 6.4) conditions using 1 mM nitrite. As revealed by quantitative PCR (qPCR), fluorescence in situ hybridization (FISH), and 16S amplicon sequencing, Nitrotoga sp. BS was clearly favored by its optimal growth parameters and dominated over Ns. defluvii at pH 7.4 and 17°C, whereas a pH of 6.4 was more selective for Ns. defluvii Our synthetic communities revealed that niche differentiation of NOB is influenced by a complex interaction of environmental parameters and has to be evaluated for single species.IMPORTANCE "Ca. Nitrotoga" is a NOB of high environmental relevance, but physiological data exist for only a few representatives. Initially, it was detected in specialized niches of low temperature and low nitrite concentrations, but later on, its ubiquitous distribution revealed its critical role for N removal in engineered systems like WWTPs. In this study, we analyzed the competition between Nitrotoga and Nitrospira in bioreactors and identified conditions where the K strategist Ns. defluvii was almost replaced by Nitrotoga sp. BS. We show that the pH value is an important factor that regulates the composition of the nitrite-oxidizing enrichment with a dominance of Nitrotoga sp. BS versus Ns. defluvii at a neutral pH of 7.4 in combination with a temperature of 17°C. The physiological diversity of novel Nitrotoga cultures improves our knowledge about niche differentiation of NOB with regard to functional nitrification under suboptimal conditions.

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K. Kitzinger et al. (mBio 9:e01186-18, 2018, https://doi.org/10.1128/mBio.01186-18) report the first isolation of a novel nitrite-oxidizing bacterium, "Candidatus Nitrotoga," and provide the first detailed information on the physiology, phylogeny, and characterization of the nitrite-oxidizing system of this genus. The isolate was derived from a wastewater treatment system and exhibits adaptation and tolerance to relatively high levels of nitrite. The origin of its nitrite oxidoreductase is distinct from other known nitrite oxidoreductase (NXR) systems, having arisen either in this organism or by horizontal gene transfer. In contrast to many earlier-characterized nitrite oxidizers, it displays substantial metabolic plasticity in its mode of energetic metabolism with capabilities to use both hydrogen and sulfite as electron donors.

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Nitrification is a key process of the biogeochemical nitrogen cycle and of biological wastewater treatment. The second step, nitrite oxidation to nitrate, is catalyzed by phylogenetically diverse, chemolithoautotrophic nitrite-oxidizing bacteria (NOB). Uncultured NOB from the genus "Candidatus Nitrotoga" are widespread in natural and engineered ecosystems. Knowledge about their biology is sparse, because no genomic information and no pure "Ca Nitrotoga" culture was available. Here we obtained the first "Ca Nitrotoga" isolate from activated sludge. This organism, "Candidatus Nitrotoga fabula," prefers higher temperatures (>20°C; optimum, 24 to 28°C) than previous "Ca Nitrotoga" enrichments, which were described as cold-adapted NOB. "Ca Nitrotoga fabula" also showed an unusually high tolerance to nitrite (activity at 30 mM NO2-) and nitrate (up to 25 mM NO3-). Nitrite oxidation followed Michaelis-Menten kinetics, with an apparent Km (Km(app)) of ~89 µM nitrite and a Vmax of ~28 µmol of nitrite per mg of protein per h. Key metabolic pathways of "Ca Nitrotoga fabula" were reconstructed from the closed genome. "Ca Nitrotoga fabula" possesses a new type of periplasmic nitrite oxidoreductase belonging to a lineage of mostly uncharacterized proteins. This novel enzyme indicates (i) separate evolution of nitrite oxidation in "Ca Nitrotoga" and other NOB, (ii) the possible existence of phylogenetically diverse, unrecognized NOB, and (iii) together with new metagenomic data, the potential existence of nitrite-oxidizing archaea. For carbon fixation, "Ca Nitrotoga fabula" uses the Calvin-Benson-Bassham cycle. It also carries genes encoding complete pathways for hydrogen and sulfite oxidation, suggesting that alternative energy metabolisms enable "Ca Nitrotoga fabula" to survive nitrite depletion and colonize new niches.IMPORTANCE Nitrite-oxidizing bacteria (NOB) are major players in the biogeochemical nitrogen cycle and critical for wastewater treatment. However, most NOB remain uncultured, and their biology is poorly understood. Here, we obtained the first isolate from the environmentally widespread NOB genus "Candidatus Nitrotoga" and performed a detailed physiological and genomic characterization of this organism ("Candidatus Nitrotoga fabula"). Differences between key phenotypic properties of "Ca Nitrotoga fabula" and those of previously enriched "Ca Nitrotoga" members reveal an unexpectedly broad range of physiological adaptations in this genus. Moreover, genes encoding components of energy metabolisms outside nitrification suggest that "Ca Nitrotoga" are ecologically more flexible than previously anticipated. The identification of a novel nitrite-oxidizing enzyme in "Ca Nitrotoga fabula" expands our picture of the evolutionary history of nitrification and might lead to discoveries of novel nitrite oxidizers. Altogether, this study provides urgently needed insights into the biology of understudied but environmentally and biotechnologically important microorganisms.

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Three types of nitrifying granules were grown on media simulating anaerobic digestion dewatering reject water and compared for their potential to increase nitrification capacity when added to mainstream flocculent activated sludge treatment. An advantage of nitrification bioaugmentation with sidestream granules instead of flocculent biomass is that the granules can be selectively maintained at longer retention times than flocs and thus provide higher nitrification capacity from bioaugmentation. The three granule types and feeding conditions were: nitrifying granules with aerobic feeding, nitrifying-denitrifying granules with anoxic feeding, and nitrifying-denitrifying/phosphate-accumulating (NDN-PAO) granules with anaerobic feeding. NDN-PAO granular sludge showed the highest potential for nitrification bioaugmentation due to its better treatment performance, granule physical characteristics, and much greater production of granular mass and nitrification capacity. Dechloromonas-associated organisms were dominant in these granules; Candidatus Accumulibacter-related organisms were also present. Nitrosomonas was the dominant ammonia-oxidizing bacteria, while Candidatus Nitrotoga was an abundant nitrite-oxidizer in all granule types.

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Inactivation and adaptation of ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB) to free nitrous acid (FNA) was investigated. Batch test results showed that AOB and NOB were inactivated when treated with FNA. After an 85-day operating period, AOB in a continuous pre-denitrification reactor did not adapt to the FNA that was applied to treat some of the return activated sludge. In contrast, NOB did adapt to FNA. NOB activity in the seed sludge was only 11% of the original activity after FNA batch treatment, at 0.75mg HNO2-N/L. NOB activity in the pre-denitrification reactor was not affected after being exposed to this FNA level. Nitrosomonas was the dominant AOB before and after long-term FNA treatment. However, dominant NOB changed from Nitrospira to Candidatus Nitrotoga, a novel NOB genus, after long-term FNA treatment. This adaptation of NOB to FNA may be due to the shift in NOB population makeup.

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In the race to achieve a sustainable urban wastewater treatment plant, not only the energy requirements have to be considered but also the environmental impact of the facility. Thus, nitrous oxide (N2O) emissions are a key-factor to pay attention to, since they can dominate the total greenhouse gases emissions from biological wastewater treatment. In this study, N2O production factors were calculated during the operation of a granular sludge airlift reactor performing partial nitritation treating a low-strength synthetic influent, and furthermore, the effect of temperature on N2O production was assessed. Average gas emission relative to conversion of ammonium was 1.5 ± 0.3% and 3.7 ± 0.5% while the effluent contained 0.5 ± 0.1% and 0.7 ± 0.1% (% N-oxidized) at 10 and 20 °C, respectively. Hence, temperature increase resulted in higher N2O production. The reasons why high temperature favoured N2O production remained unclear, but different theoretical hypotheses were suggested.

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Nitrite-oxidizing bacteria (NOB) are responsible for the second step of nitrification in natural and engineered ecosystems. The recently discovered genus Nitrotoga belongs to the Betaproteobacteria and potentially has high environmental importance. Although environmental clones affiliated with Nitrotoga are widely distributed, the limited number of cultivated Nitrotoga spp. results in a poor understanding of their ecophysiological features. In this study, we successfully enriched the nonmarine cold-adapted Nitrotoga sp. strain AM1 from coastal sand in an eelgrass zone and investigated its physiological characteristics. Multistep-enrichment approaches led to an increase in the abundance of AM1 to approximately 80% of the total bacterial population. AM1 was the only detectable NOB in the bacterial community. The 16S rRNA gene sequence of AM1 was 99.6% identical to that of "Candidatus Nitrotoga arctica," which was enriched from permafrost-affected soil. The highest nitrogen oxidation rate of AM1 was observed at 16°C. The half-saturation constant (Km ) and the generation time were determined to be 25 µM NO2- and 54 h, respectively. The nitrite oxidation rate of AM1 was stimulated at concentrations of <30 mM NH4Cl but completely inhibited at 50 mM NH4Cl. AM1 can grow well under specific environmental conditions, such as low temperature and in the presence of a relatively high concentration of free ammonia. These results help improve our comprehension of the functional importance of NitrotogaIMPORTANCE Nitrite-oxidizing bacteria (NOB) are key players in the second step of nitrification, which is an important process of the nitrogen cycle. Recent studies have suggested that the organisms of the novel NOB genus Nitrotoga were widely distributed and played a functional role in natural and engineered ecosystems. However, only a few Nitrotoga enrichments have been obtained, and little is known about their ecology and physiology. In this study, we successfully enriched a Nitrotoga sp. from sand in a shallow coastal marine ecosystem and undertook a physiological characterization. The laboratory experiments showed that the Nitrotoga enrichment culture could adapt not only to low temperature but also to relatively high concentrations of free ammonia. The determination of as-yet-unknown unique characteristics of Nitrotoga contributes to the improvement of our insights into the microbiology of nitrification.

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