Transformation of Bisphenol A and Alkylphenols by Ammonia

Mar 21, 2012 - ABSTRACT: Transformation of bisphenol A (BPA) by ammonia-oxidizing bacteria (AOB) Nitrosomonas europaea. ATCC 19718 was ...
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Transformation of Bisphenol A and Alkylphenols by AmmoniaOxidizing Bacteria through Nitration Qian Sun,† Yan Li,† Pei-Hsin Chou,‡ Po-Yi Peng,‡ and Chang-Ping Yu*,† †

Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China ‡ Department of Environmental Engineering, National Cheng Kung University, Tainan 70101, Taiwan S Supporting Information *

ABSTRACT: Transformation of bisphenol A (BPA) by ammonia-oxidizing bacteria (AOB) Nitrosomonas europaea ATCC 19718 was investigated. On the basis of the ultraperformance liquid chromatography (UPLC) coupled to quadrupole time-of-flight mass spectrometry (Q-TOF MS) and nuclear magnetic resonance analysis, we found N. europaea could transform BPA into nitro- and dinitro-BPA, suggesting that abiotic nitration between the biogenic nitrite and BPA played a major role in the transformation of BPA in the batch AOB system. Nitrite concentrations, temperature, and pH values were the major factors to influence the reaction rate. Furthermore, the yeast estrogenic screening assay showed that the formed nitro- and dinitro-BPA had much less estrogenic activity as compared with its parent compound BPA. Similar reactions of abiotic nitration were considered for 4-nnonylphenol (nNP) and 4-n-octylphenol (nOP) since nitronNP and nitro-nOP were detected by UPLC-Q-TOF MS. In addition, results from the local wastewater treatment plant (WWTP) showed the occurrence of nitro-BPA and dinitro-BPA during the biological treatment process and in the effluent, indicating that nitration of BPA is also a pathway for removal of BPA. Results of this study provided implication that AOB in the WWTPs might contribute to removal of selected endocrine-disrupting compounds (EDCs) through abiotic nitritation.

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INTRODUCTION The presence of endocrine-disrupting compounds (EDCs) in the aquatic environment has raised a great concern due to its correlation to high incidence of adverse effects on the sexual and reproductive systems in wildlife and fish.1 Three widely detected phenolic EDCs, bisphenol A (BPA), 4-n-nonylphenol (nNP), and 4-n-octylphenol (nOP), were chosen to investigate in this study. BPA is a monomer and found in epoxy resins commonly used in can lining and hard polycarbonate plastic, such as baby bottles, water bottles, and food containers. Besides, it is widely used in a number of products such as adhesives, building materials, and powder paints. Alkylphenols, including nNP and nOP, are degradation products of alkylphenol ethoxylates, which are widely used as surfactants and detergents in domestic and industrial products. Both BPA and alkylphenols are known to act like hormones to interfere with the endocrine systems of animals and humans.2,3 The effluents discharged from wastewater treatment plants (WWTPs) are a primary source for EDCs to enter the aquatic environment.4,5 The ranges of reported influent concentration were from 699 to 1416 ng/L for BPA, 43 to 101 ng/L for nNP, and 38 to 159 ng/L for nOP, while effluent concentrations were © 2012 American Chemical Society

from 56 to 138 ng/L for BPA, 15 to 58 ng/L for nNP, and 10 to 95 ng/L for nOP.6 The WWTPs could remove BPA effectively with more than 90% reduction, while they removed less than 40% alkylphenols.6 Most of their removal occurred during the biological treatment process. BPA-, NP- and OP-degrading bacteria have been reported to exist in the WWTPs. Strains MV1 and Pseudomonas paucimobilis FJ-4, which can use BPA as a sole source of carbon and energy, were isolated from activated sludge of a plastics manufacturing facility7 and an epoxy resin manufacturing plant,8 respectively. NP- and OP-degrading bacteria from activated sludge have also been reported, including Sphingobium xenophagum Bayram,9 Sphingomonas cloacae S-3T,10 and Sphingomonas sp. PWE1.11 Oxidation of ammonia is the first step in nitrification processes during biological wastewater treatment. This reaction is carried out by ammonia-oxidizing bacteria (AOB), a group of Received: Revised: Accepted: Published: 4442

December March 14, March 21, March 21,

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experiments. Chemostat culture was mixed by aeration and stirring (at 150 rpm). Samples were taken periodically up to 4 weeks. Abiotic Reaction of BPA, nNP, and nOP with Nitrite. Abiotic batch tests were carried out in Milli-Q water containing 10 mM phosphate buffer with a total volume of 250 mL. pH ranged from 6.0 to 8.0, and the NO2− was spiked using sodium nitrite to a final concentration of 250 mg N/L. BPA, nNP, and nOP had an initial concentration of 1 mg/L. Assays were maintained at 30 °C in the dark on a shaker (150 rpm). Samples for BPA, nNP, and nOP were taken periodically up to 120 h and prepared as described above. All abiotic assays were conducted in duplicate. Yeast Estrogenic Screening (YES) Assay. Solutions with a high concentration of nitro-BPA and dinitro-BPA were synthesized for analyzing estrogenicity. The nitration step was conducted by treating 25 mg/L BPA with excessive NaNO2 (6250 mg N/L) in phosphate buffer at pH 6.0. After 48 h synthesis, dinitro-BPA chemicals were purified by liquid−liquid extraction using diethyl ether. Similar synthesis of nitro-nNP or nitro-nOP was achieved by treating 2.5 mg/L nNP or nOP with excessive NaNO2 (625 mg N/L) in phosphate buffer at pH 6.0. The identity and purity were confirmed by ultraperformance liquid chromatography (UPLC) coupled to quadrupole timeof-flight mass spectrometry (Q-TOF MS). The estrogenicity of nitrated metabolites was determined by YES assays as described in the Supporting Information. OD620 and OD540 were measured in order to calculate the corrected value shown in the following equation: Corrected Value = OD540 (Sample) − [ OD620 (Sample) − OD620 (DMSO)].23 Wastewater Samples Collection and Preparation. Wastewater samples were collected in August and September 2011 from a local domestic WWTP in Xiamen, China. This secondary WWTP is equipped with an Orbal oxidation ditch process and a UV disinfection process before final effluent. Four liter amber glass bottles were used to collect wastewater samples from different stages of the WWTP treatment process, including influent, beginning of oxidation ditch, end of oxidation ditch, and final effluent. Water samples were acidified to pH 2 with sulfuric acid and filtered immediately after sampling. A 300 mL amount of sample was spiked with BPAd16. Samples were concentrated using solid-phase extraction (SPE) as described in detail in the Supporting Information. The eluents from SPE were evaporated to dryness by a gentle nitrogen stream. Residues were dissolved in 0.5 mL of methanol and filtered through a 0.22 μm membrane, and 10 μL was injected into the high-performance liquid chromatography-triple-quadrupole mass spectrometry (HPLC-QqQ MS) system for determination. Analytical Methods. In the batch and continuous flow studies, for quantitative analysis, BPA, nNP, and nOP and their nitrated forms were detected with an Agilent 1200 series HPLC with an UV detector (Agilent Technologies, Germany). Separation was achieved by an Agilent C18 column (Zorbax Eclipse XDB-C18, 4.6 × 150 mm, 5 μm) with mobile phases of water and methanol at a flow rate of 1.0 mL/min. For qualitative analysis, BPA, nNP, and nOP and their nitrated forms were identified by a Waters UPLC (Waters, USA) and a Q-TOF MS (Bruker, Germany). A Waters C18 column (Acquity UPLC BEH C18, 2.1 × 100 mm, 1.7 μm) was used with a flow rate of 0.2 mL/min. MS/MS was operated in electrospray ionization (ESI) negative mode, with a capillary voltage of 2.5 kV and collision energy of 10 eV.

ubiquitous lithoautotrophic microorganisms capable of expressing ammonia monooxygenase (AMO) enzyme. In addition to ammonia oxidation, AMO enzymes are known to oxidize a wide range of aliphatic and aromatic hydrocarbons.12−15 Previous studies have reported that nitrifying activated sludge was capable of degrading natural and synthetic estrogens effectively.16,17 Further research using pure AOB identified the metabolites and confirmed that the abiotic nitration between the produced nitrite and estrogens and the cometabolism catalyzed by AMO were involved in the transformation of estrogens by AOB.18,19 While previous studies observed high BPA and NP degradation by nitrifying activated sludge and suggested that AOB and likely the AMO played a key role in their degradation,20,21 the metabolites were not identified to support their hypothesis. It is important to know the fate and nature of the metabolites because they may pose additional ecotoxicological effects. The aim of this study was to determine the BPA, nNP, and nOP degradation mechanism by AOB. The occurrence of the degradation byproducts in the WWTP was also examined. The results of this study could enhance our understanding of the fate of BPA and alkylphenols in wastewater treatment processes and in the environment.

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MATERIALS AND METHODS Chemicals and Reagents. BPA (99%), BPA-d16 (98%), and nOP (99%) were purchased from Sigma-Aldrich, and nNP (98%) was from Alfa Aesar. Stock solutions of BPA, nNP, and nOP were prepared in acetone with a concentration of 1000 mg/L. All other reagents used were commercial products of highest grade available. Synthesis of dinitro-BPA is described in the Supporting Information. Growth of N. europaea. N. europaea ATCC 19718 was purchased from Nite Biological Resource Center. N. europaea was grown in a defined mineral salt medium22 described in the Supporting Information. Cell concentrations were measured as optical density at 600 nm (OD600) by a UV−vis spectrophotometer. Tests of BPA Degradation by N. europaea. Experiments were conducted to examine BPA degradation by N. europaea. First, a known amount of BPA−acetone stock solution was added into empty 1 L flasks. After completely evaporating the acetone, the growth medium was added into the flasks with shaking at 150 rpm in the dark. After 2 days, BPA was completely dissolved in the growth medium in the flask. The prepared cell suspension as described previously was then added into the flasks to start experiments. Experiments were conducted with the initial OD600 around 0.025 and (NH4)2SO4 concentration of 25 mM. Autoclaved cells were used as kill control. No-BPA controls were used to assess original ammonia oxidation activities of N. europaea. Samples were filtered (0.22 μm) before nitrite analyses. Sample aliquots (4 mL) were extracted with 4 mL of diethyl ether overnight, and 2 mL of organic phase was transferred to a clean tube and evaporated to dryness. The dry solid was dissolved in 0.5 mL of methanol. Biotransformation of BPA by N. europaea in the Continuous Flow Bioreactor. The continuous flow bioreactor (chemostat volume = 1.5 L, flow rate close to 300 mL/ d) was maintained for 28 days to investigate the biotransformation of BPA by N. europaea. The culture medium, described as above, was supplemented with BPA to a final concentration of 1 mg/L. The prepared cell suspension as described previously was then added into the bioreactor to start 4443

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products of hydroxylated BPA (m/z = 244) were not detected. Samples from continuous flow study were also analyzed by UPLC-Q-TOF to investigate the transformation product of BPA. The results showed that nitro-BPA was detected in each sample from 1 to 4 weeks, ditro-BPA was only detected in the second-week sample, and no other byproduct was detected (data not shown). These results suggested that BPA degradation in the batch and continuous N. europaea cultures was due to nitration of BPA with nitrite produced by oxidation of ammonia. Abiotic BPA Nitration. Furthermore, to test the hypothesis that BPA transformation was not a result of N. europaea, the 5day N. europaea culture was centrifuged (at 10 000g and 4 °C for 30 min) to remove cells and BPA was added to the cell-free medium with an initial concentration of 1 mg/L. A similar degradation trend of BPA was observed with the increase of nitro-BPA and dinitro-BPA. In addition, abiotic nitration assays were conducted with 1 mg/L of BPA and 250 mg N/L of nitrite. BPA could be removed in the abiotic assays at pH 6, and two products, nitro-BPA and dinitro-BPA, were detected by UPLC-Q-TOF (Figure 2a) with the same retention time and m/z ratios as the N. europaea biodegradation assays. According to the MS/MS fragmentation pathway for the products shown in Figure 2b−d, the MS transition m/z 272 → 227 supported the proposed conversion of nitro-BPA to BPA and m/z 317 → 272 → 227 supported the proposed conversion of dinitro-BPA to nitro-BPA and nitro-BPA to BPA. 1H NMR spectra, 13C NMR spectra, and HMBC spectra were obtained for dinitro-BPA to provide additional structure information (Supporting Information Figure S3). The HMBC spectrum uses long-range JC−H coupling to correlated protons and carbons 2−4 bonds away. As shown in Supporting Information Figure S3c, the proton (8.06 ppm) showed a 3-bond coupling to carbon (42.02 ppm), which inferred nitro substitution at the ortho position of the hydroxyl group on each benzene ring. On the basis of the UPLC-Q-TOF and HMBC NMR analyses, the transformation process of BPA is shown in Figure 3. Abiotic batch study was conducted at 30 °C with a nitrite concentration of 250 mg N/L at pH 6.0, 7.0, and 8.0. The transformation rate at pH 6.0 was high; however, no significant BPA removal occurred at pH 7.0 or 8.0. Additional batch studies were conducted to compare the reaction rate for BPA nitration at pH 6.0 under a range of temperatures and nitrite concentrations. The first-order rate constants (k) were calculated from linear regression of the natural log of BPA concentration with time. At 30 °C, the k values were calculated as 0.002, 0.012, and 0.014 h−1 for 10, 100, and 250 mg N/L nitrite, respectively, with correlation coefficients in the range of 0.861−0.992. Under a nitrite concentration of 250 mg N/L, the k values were 0.010, 0.012, and 0.014 h−1 at temperatures of 10, 20, and 30 °C, respectively, with the correlation coefficients in the range of 0.942−0.992. These results suggested that the rate of nitration was pH dependent and increased with increasing temperatures and nitrite concentration, which was in accordance with previous nitration of the estrogens.24 Estrogenicity of Nitrated BPA. The YES assay was used to evaluate the estrogenicity of produced nitro-BPA and dinitro-BPA. To have a suitable BPA concentration for detection by the YES assay, another abiotic nitration reaction with higher initial BPA concentration was conducted. Samples were collected during the course of converting BPA to dinitroBPA, and their corresponding chromatograms are shown in Figure 4a−c. As shown in Figure 4d, the estrogenicity of

For acquiring nuclear magnetic resonance (NMR) information, the BPA transformation product dinitro-BPA was evaporated to dryness, reconstituted in CDCl3, and transferred to NMR tubes. 1H NMR, 13C NMR, and heteronuclear multiple-bond correlation spectroscopy (HMBC) NMR data were performed with an Avance III 600 MHz NMR Spectrometer (Bruker, USA). For the WWTP study, samples were determined by HPLCQqQ MS using a Shimadzu HPLC system (Shimadzu, Japan) interfaced to an ABI QqQ mass spectrometer (ABI, USA). A Dionex C18 column (Acclaim C18, 3.0 × 50 mm, 2.2 μm) was used with a flow rate of 0.5 mL/min. The mobile phases were 5 mM ammonia acetate in water (A) and methanol (B). The gradient initially was 50% methanol, held for 1 min, and adjusted linearly to 90% at 5 min, held for 2 min, and back to 50% at 7.1 min, held for 2 min. The MS was operated in negative ESI mode using multiple reaction monitoring (MRM) mode. The monitored target and reference ions are shown in Supporting Information Table S1, where declustering potentials (DP), entrance potentials (EP), collision energies (CE), and collision cell exit potentials (CXP) are also shown. The method detection limits for BPA and dinitro-BPA were 0.008 and 0.0008 μg/L, respectively. Other chemical analysis methods are described in detail in the Supporting Information.

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RESULTS Transformation of BPA by N. europaea under the Batch and Continuous Conditions. Biodegradation of BPA (1 mg/L) was observed in the batch experiment as shown in Figure 1. Under the test concentration, BPA did not have

Figure 1. Biodegradation of BPA by N. europaea. Error bars represent the range of two replicates.

significant toxic effects on N. europaea since the cell growth, nitrite production, and pH changes were not influenced in the presence of BPA during degradation (Supporting Information Figure S1). Degradation byproducts were formed since unknown peaks were observed on the HPLC chromatograms (Supporting Information Figure S2). To understand the mechanisms involved in BPA degradation by N. europaea, UPLC-Q-TOF analysis was conducted to identify the generated products. Besides BPA, only two additional products were detected with m/z ratios of 272 and 317. On the basis of the m/ z of the parent ions, the products were tentatively identified to be nitro- and dinitro-BPA (data not shown). Although N. europaea is known to express AMO to cometabolize a wide range of substrates,12−15 predicted cometabolic transformation 4444

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Figure 2. Selected ion chromatograms of abiotic BPA nitration (a), and mass spectra of BPA (m/z 227) (b), nitro-BPA (m/z 272) (c), and dinitroBPA (m/z 317) (d).

Figure 3. Proposed transformation products of BPA.

had less estrogenicity than their parent compounds (Supporting Information Figures S4 and S5). WWTP Observations. For wastewater samples from September 2011 the nitrite concentrations in the beginning and end of the oxidation ditch were 0.08 and 0.34 mg N/L with pH at 7.66. BPA was detected in the influent, beginning of the oxidation ditch, end of the oxidation ditch, and final effluent with a concentration of 2.14, 1.67, 0.71, and 0.50 μg/L, respectively (Supporting Information Table S2). BPA removal efficiency was 77% in this local WWTP, while more than 58% BPA was removed in the oxidation ditch. Nitro-BPA and dinitro-BPA were not detected in the influent (data not shown). Low signals of nitro-BPA and dinitro-BPA close to the noise level were observed in the beginning of the oxidation ditch (Figure 6b and 6f). However, both nitro-BPA and dinitroBPA were detected at the end of the oxidation ditch (Figure 6c and 6g) and the final effluent (Figure 6d and 6h), indicating there was nitration of BPA in the oxidation ditch treatment process. Both nitro-BPA and dinitro-BPA were also detected at the end of the oxidation ditch for wastewater samples from August 2011 (Supporting Information Figure S6). The

samples decreased as the nitration reaction continued and the estrogenicity approached the background level of DMSO when all BPA was converted to dinitro-BPA. Since the phenolic ring is important for binding to the estrogen receptor, 25 incorporating additional nitro groups onto the phenolic rings of BPA might induce steric hindrance to reduce the binding ability of nitro- and dinitro-BPA and cause the lowered estrogenicity. Abiotic Nitration of of nNP and nOP. We further conducted abiotic assays to test the possibility of nitration of nNP and nOP. As shown in Figure 5a and 5d, nitrite reacted with nNP and nOP and transformation products were observed with UPLC-Q-TOF. Only one product was detected for both nNP and nOP assays, with a m/z ratio of 264 for nNP and 250 for nOP. The MS/MS fragmentation pathway for the products, m/z 264 → 219 and 250 → 205, proved formation of nitronNP and nitro-nOP, respectively (Figure 5b,c and 5e−f). The lack of dinitro products is most likely due to only one phenolic group in nNP and nOP compared to BPA. Similar to nitrated BPA, the YES assay also showed that nitrated nNP and nOP 4445

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Figure 4. Chromatograms of samples used for YES assays (a−c), and results from YES assays performed on the corresponding samples (d). Error bars represent the standard deviation of 6 replicates.

concentration of dinitro-BPA in the end of the oxidation ditch and final effluent was 0.0019 and 0.0037 μg/L, which accounted for 0.3% and 0.7% of the remaining BPA. Although quantitative analysis of nitro-BPA could not be achieved since we were unable to synthesize pure nitro-BPA standard, our results with dinitro-BPA and the signal intensities from MS inferred that nitration should be a minor transformation pathway of BPA in the WWTP.

Figure 5. Selected ion chromatograms (a) and mass spectra of nOP (m/z 205) (b) and nitro-nOP (m/z 250) (c); selected ion chromatograms (d) and mass spectra of nNP (m/z 219) (e) and nitro-nNP (m/z 264) (f).

DISCUSSION Removal of 17α-ethinylestradiol (EE2) was observed in the activated sludge treatment process with a long enough solids retention time for nitrification.26,27 EE2 nitration through abiotic process was then confirmed in the laboratory using batch tests in the presence of AOB, although cometabolic byproducts were also detected.18,19 Our experiments showed that BPA could be transformed in the batch N. europaea culture via abiotic nitration reactions between the produced nitrite and BPA. Byproducts were identified as nitro- and dinitro-BPA using LC-MS/MS and NMR analysis. Similar reactions of abiotic nitration were observed for nNP and nOP since nitronNP and nitro-nOP were detected. Cometabolic degradation was not observed because no predicted byproduct was identified. However, as shown in the biodegradation of EE2 by N. europaea, a metabolite containing carboxylation in the ring of EE2 was observed and its reaction mechanism was difficult to explain.18 Therefore, we still cannot exclude the possibility of formation of metabolites other than nitrated byproducts, which were not predicted and not detected by LCMS/MS in this study. This possibility will also explain the somewhat increased rates of BPA removal observed in the presence of N. europaea compared with abiotic nitration when pH was between 7 and 8 as shown in Figure 1. Previous studies

reported that N. europaea could degrade a wide range of phenolic compounds12,16,21 under batch tests and hypothesized that degradation was catalyzed by AMO via cometabolic reactions. However, they did not consider the possibility of the abiotic nitration reaction observed in this study. As shown in our batch N. europaea studies, nitrite concentrations could increase to more than 200 mg N/L and pH values could decrease to 6 after 3 days. Batch N. europaea degradation test will favor abiotic nitration since nitration could be enhanced at lower pH and higher concentration of nitrite. In this study, nitration of BPA was efficient in the presence of a high concentration of ammonia and N. europaea or in the presence of a high concentration of nitrite at pH 6. The nitrated BPA derivatives also occurred in a full-scale WWTP equipped with an oxidation ditch biological treatment process, although the nitrite levels were much lower and pH levels were higher than the batch condition. While our results suggested that nitration might be only a minor transformation pathway of BPA in the WWTP, this work provides implication in that in certain wastewater treatment systems such as shortcut nitrification− denitrification, where accumulation of nitrite concentration could occur,28 nitration of BPA might potentially be more important for its removal. Since BPA is a known EDCs and the YES assay showed that the formed nitrated BPA had much less

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Figure 6. MRM chromatograms of dinitro-BPA (precursor ion m/z = 317) (a−d) and nitro-BPA (precursor ion m/z = 272) (e−h). (a and e) Standard solution prepared by abiotic reaction, (b and f) beginning of the oxidation ditch, (c and g) end of the oxidation ditch, and (d and h) the final effluent.

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estrogenic activity as compared with its parent compound BPA, more efforts should be done to study the role of nitration for removal of BPA under different biological treatment processes. Moreover, nitration of acetaminophen (APAP) was reported in the nitrifying activated sludge with transformation from APAP to nitro-APAP.29 Abiotic nitration has been observed for 2,4-dichlorophenol in a French river delta,30 possibly induced by the photoproduced NO2 radical. Therefore, in addition to the nitrated BPA, nitration of APAP and 2,4-dichlorophenol have been observed in the constructed or natural environments. Currently, little is known about the properties of these nitrated derivatives of phenolic compounds. Detection of these compounds in the environment should be of concern since the nitrophenols have shown genotoxic and carcinogenic properties.31 Therefore, future studies are needed to explore the fate and toxicity of these nitrated phenolic compounds and understand their potential effects to our ecological systems.

ASSOCIATED CONTENT

* Supporting Information S

Additional information as noted in the text. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: (86)-592-6190768; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Dr. Xian Zhang and Mr. Lifeng Lin for their help in LC-MS analysis and compound identification. We thank Ms. Huiying Huang for her help in acquiring and analyzing NMR data. We also acknowledge Professor Oliver Hao for his comments on the manuscript. This work was supported by the Hundred Talents Program of the Chinese Academy of Sciences, Special Program for Key Basic Research of the Ministry of Science and Technology, China (2010CB434802), the CAS/ 4447

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of 17α-ethinylestradiol by Nitrosomonas europaea in batch and continuous flow bioreactors. Environ. Sci. Technol. 2009, 43, 3549− 3555. (19) Gaulke, L. S.; Strand, S. E.; Kalhorn, T. F.; Stensel, H. D. 17αethinylestradiol transformation via abiotic nitration in the presence of ammonia oxidizing bacteria. Environ. Sci. Technol. 2008, 42, 7622− 7627. (20) Kim, J. Y.; Ryu, K.; Kim, E. J.; Choe, W. S.; Cha, G. C.; Yoo, I.K. Degradation of bisphenol A and nonylphenol by nitrifying activated sludge. Process Biochemistry 2007, 42, 1470−1474. (21) Roh, H.; Subramanya, N.; Zhao, F.; Yu, C.-P.; Sandt, J.; Chu, K.H. Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 2009, 77, 1084−1089. (22) Hyman, M. R.; Arp, D. J. 14C2H2- and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J. Biol. Chem. 1992, 267, 1534−1545. (23) Routledge, E. J.; Sumpter, J. P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ. Toxicol. Chem. 1996, 15, 241−248. (24) Gaulke, L. S.; Strand, S. E.; Kalhorn, T. F.; Stensel, H. D. Estrogen nitration kinetics and implications for wastewater treatment. Water Environ. Res. 2009, 81, 772−778. (25) Baker, M. E.; Chang, D. J.; Chandsawangbhuwana, C. 3D Model of Lamprey estrogen receptor with estradiol and 15α-hydroxyestradiol. PLoS ONE 2009, 4, e6038. (26) Andersen, H.; Siegrist, H.; Halling-Sorensen, B.; Ternes, T. A. Fate of estrogens in a municipal sewage treatment plant. Environ. Sci. Technol. 2003, 37, 4021−4026. (27) Clara, M.; Kreuzinger, N.; Strenn, B.; Gans, O.; Kroiss, H. The solids retention time - a suitable design parameter to evaluate the capacity of wastewater treatment plants to remove micropollutants. Water Res. 2005, 39, 97−106. (28) Ruiz, G.; Jeison, D.; Rubilar, O.; Ciudad, G.; Chamy, R. Nitrification-denitrification via nitrite accumulation for nitrogen removal from wastewaters. Bioresour. Technol. 2006, 97, 330−335. (29) Chiron, S.; Gomez, E.; Fenet, H. Nitration processes of acetaminophen in nitrifying activated sludge. Environ. Sci. Technol. 2010, 44, 284−289. (30) Chiron, S.; Minero, C.; Vione, D. Occurrence of 2,4dichlorophenol and of 2,4-dichloro-6-nitrophenol in the Rhone River Delta (Southern France). Environ. Sci. Technol. 2007, 41, 3127−3133. (31) Eichenbaum, G.; Johnson, M.; Kirkland, D.; O’Neill, P.; Stellar, S.; Bielawne, J.; DeWire, R.; Areia, D.; Bryant, S.; Weiner, S.; DesaiKrieger, D.; Guzzie-Peck, P.; Evans, D. C.; Tonelli, A. Assessment of the genotoxic and carcinogenic risks of p-nitrophenol when it is present as an impurity in a drug product. Regul. Toxicol. Pharmacol. 2009, 55, 33−42.

SAFEA International Partnership Program for Creative Research Teams (KZCX2-YW-T08), and the Science and Technology Planning Project of Xiamen, China (3502Z20102017).

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