Effect of algal organic matter (AOM) extracted from Microcystis aeruginosa on photo-degradation of Diuron

Chemical Engineering Journal 281 (2015) 265–271

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Effect of algal organic matter (AOM) extracted from Microcystis aeruginosa on photo-degradation of Diuron Lei Li a,⇑, Haicheng Guo a, Chen Shao b, Shuili Yu a,⇑, Daqiang Yin c, Naiyun Gao a, Ning Lu d a

State Key Laboratory of Pollution Control and Resource Reuse, College of Environmental Science & Engineering, Tongji University, Shanghai 200092, China Shanghai Municipal Engineering Design Institute (Group) Co., Ltd, Shanghai 200092, China c Key Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environment Science and Engineering, Tongji University, Shanghai 200092, China d Nation Engineering Research Center of Urban Water Resources, Shanghai 200082, China b

h i g h l i g h t s  Effect of intra- and extracellular algal organic matters on photo-degradation of Diuron.  The quantitative contributions of different reactive oxygen species on degradation.  EEM spectrum of intra- and extracellular organic matters during the degradation.  Corresponding kinetics of herbicide removal in response to pH.

a r t i c l e

i n f o

Article history: Received 23 March 2015 Received in revised form 16 June 2015 Accepted 19 June 2015 Available online 25 June 2015 Keywords: Algal organic matter Intracellular organic matter Extracellular organic matter Phycocyanin Photo-excited-state matter

a b s t r a c t The presence of algal organic matter (AOM) and emerging organic contaminants in surface drinking water sources has received increasing attention recently. Nevertheless, interactions between these two harmful co-existing compounds in water sources have rarely been reported. This study investigated the influence of AOM, including intracellular organic matter (IOM) and extracellular organic matter (EOM), on the photo-degradation of Diuron, under UV and visible light (VL) irradiation. Kinetics analyses indicated that both the direct and indirect photolysis of Diuron followed a pseudo-first-order reaction (R2 > 0.98). Diuron was rapidly removed under UV irradiation accompanied by minor impacts from AOM. Under VL irradiation, the photo-excited phycocyanin in the IOM was capable of accelerating Diuron degradation, whereas the coexistence of other organic compounds in the IOM inhibited the reaction due to a screening effect, resulting in a slower overall rate of Diuron degradation. By comparison, EOM promoted the reactions when pH exceeded 5.0. The AOM-mediated generation of triplet DOM (3DOM⁄) accounted for 82% and 64% of the Diuron removal in the presence of IOM and EOM, respectively. Spectral excitation–emission matrices produced by AOM in solutions demonstrated the primary mechanisms of the co-existing AOM on Diuron degradation. Ó 2015 Elsevier B.V. All rights reserved.

1. Introduction Emerging contaminants, including pharmaceuticals and personal care products (PPCPs), endocrine-disrupting chemicals (EDCs) and biocides, have been frequently detected at alarming concentrations in rivers, lakes and reservoirs [1–4]. Worse still, many of these contaminants are recalcitrant to the conventional physicochemical processes in wastewater treatment. In recent years, solar-mediated photo-degradation has been regarded as the predominant degradation pathway of these chemicals in ⇑ Corresponding authors. E-mail addresses: [email protected] (L. Li), [email protected] (S. Yu). http://dx.doi.org/10.1016/j.cej.2015.06.091 1385-8947/Ó 2015 Elsevier B.V. All rights reserved.

aquatic systems. However, this process may affect the fate of other co-existing organic pollutants in water via indirect photolysis due to the generation of reactive oxygen species (ROSs) including the hydroxyl radical (OH), singlet oxygen (1DO2), and triplet excited-state dissolved organic matter (3DOM⁄) produced by co-existing DOM in water [5–10]. Algal organic matter (AOM) created by frequent cyanobacterial blooms has become a major DOM component in reservoirs and lakes [11–13]. AOM is usually classified as either intracellular organic matter (IOM) or extracellular organic matter (EOM) and is primarily composed of polysaccharides, proteins and lipids [14–18]. Specifically, cyanobacteria produce a series of intracellular pigments, of which phycocyanin accounts for a major portion.

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Phycocyanin is a type of water-soluble conjugated biliprotein with a structure similar to a porphyrin and is known to display a wide range of photo-induced activity [19] due to the formation of the triplet excited state of phycocyanin3 under light irradiation, as represented by Eq. (1). light

1

3

Phycocyanin ƒƒƒƒƒƒ! phycocyanin ! phycocyanin

ð1Þ

Phycocyanin3 is capable of reacting either with molecular oxygen, leading to the formation of various ROSs, as in Eq. (2), or directly with various substrates (Subs) in solution, as in Eq. (3). The mechanisms represented by Eqs. (2) and (3) can lead to the photo-oxidation of organic matter in aquatic systems [20]. 3

energy=electrontransfer

Phycocyanin þ 3 O2 ƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒ! ROS 3

energy=electron transfer

ð2Þ 0=þ=

Phycocyanin þ Subs ƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒ! phycocyanin

3==þ

photochemical reactor (Xujiang Co., Nanjing, China), which was equipped with a 500 W xenon light (with emissions centered at 900 nm) and a 300 W high-pressure mercury lamp (with emissions centered at 360 nm) that simulated visible light (VL) and UV irradiation, respectively (Fig. S2). For the direct photolysis experiments, the Milli-Q water was spiked solely with Diuron at an initial concentration of 0.025 mM. IOM, EOM or FA (corresponding to a dissolved organic carbon (DOC) concentration of 6 mg L1) was added as a background material when investigating the indirect photolysis of Diuron. The solutions were prepared in 50 mL quartz tubes at initial pH levels of 2, 5, 7, and 9, which were adjusted using HCl and NaOH. All of the experiments were conducted at a temperature of 20 °C, which was maintained by a circulating constant-temperature water bath. Data regarding the rates of photochemical degradation were obtained by withdrawing aliquots of samples at regular time intervals.

þ Subs

ð3Þ

The generation of ROSs as mediated by phycocyanin has been previously reported to accelerate the photo-degradation of microcystins, which are algal toxins [19–21]. Unfortunately, little is known regarding the effects that other photochemically produced ROSs from AOM have on the removal of other types of co-existing organic matters in aquatic systems. In the present study, one of the most commonly used herbicides, Diuron (N0 -[3,4-dichlorophenyl]-N,N-dimethylurea), was selected to represent these emerging contaminants in surface waters. Studies on photo-degradation of Diuron and other herbicides have been reported in literatures [22–24], but influences of the co-existing AOM on photolysis processes were still unknown. Herein, the kinetics of direct and indirect photolysis of Diuron under various irradiation sources were investigated in the presence of IOM and EOM extracted from one of the most abundant cyanobacteria, Microcystis aeruginosa, and in the presence of natural aquatic organic matter, represented by fulvic acid (FA). In addition, variations in the spectral excitation–emission matrices (EEMs) of these types of organic matter before and after the reactions were identified to further clarify the mechanisms of the photolysis of Diuron.

2.2.2. Roles of various species of radicals Sorbic acid (0.18 mM, a 3DOM⁄ scavenger) [26] and 2-propanol (65 mM, an OH scavenger) [27] were added to quantify the contributions of 3DOM⁄ and OH to the photolysis, respectively. 2.2.3. Analytical method The concentration of Diuron was determined at a wavelength of 254 nm by HPLC; the chromatograph (e2695, Waters, US) was equipped with a UV–visible detector and a Symmetry C18 column (dimensions of 250 mm  4.6 mm, 5 lm; Waters). Isocratic elution was used with the mobile phase consisting of Milli-Q water and acetonitrile (v/v = 35:65). The calibration curve of Diuron (R2 > 0.99) was obtained by measuring a series of concentrations of Diuron standard solutions, and the detection limit was 0.05 mg L1. The DOC associated with the DOM (EOM, IOM and FA) was quantified using a TOC analyzer (TOC-L, Shimazu, Japan). 2.2.4. Fluorescence spectroscopy The excitation–emission matrices (EEMs) (200–700 nm) of each sample before and after photolysis were acquired using a fluorescence spectrophotometer (Cary Eclipse, Varian, US). The data was analyzed using Sigmaplot (Sigmaplot Software Inc., US).

2. Materials and methods

3. Results and discussion

2.1. Materials

3.1. Direct and indirect photo-degradation kinetics of Diuron

All of the chemicals used in the study were at least of analytical grade except as noted otherwise. Diuron (>99%) (Fig. S1) was purchased from Aladdin. Sorbic acid, 2-propanol, HCl and NaOH used for pH adjustment were purchased from Sinopharm Chemical Reagent Co., China. HPLC-grade acetonitrile was purchased from Sigma–Aldrich. Solutions for all of the experiments in this study were prepared using Milli-Q water. M. aeruginosa was obtained from the Institute of Hydrobiology, Chinese Academy of Sciences and was cultured in BG11 media in an incubator at 25 °C. AOM, including IOM and EOM, were extracted from M. aeruginosa during its exponential growth period using centrifugation and the freeze/thaw method [25]. The IOM and EOM solutions were desalinated and stored at 18 °C prior to use. Natural aquatic natural organic matter, represented by FA (2S101F), was obtained from the International Humic Substances Society (IHSS).

The kinetics of the direct photochemical degradation of Diuron, starting at various initial pH conditions, during irradiation with VL and UV are shown in Fig. 1. All of the reactions were shown to follow a pseudo-first-order kinetics pattern (R2 > 0.98) that can be represented by Eq. (4).

2.2. Analytical methods and experiment details 2.2.1. Direct and indirect photolysis Experiments involving both direct and indirect photolysis were performed on aqueous solutions of Diuron using an XPA serial

d½Diuron=dt ¼ kobs ½Diuron

ð4Þ

where kobs is the observed pseudo-first-order degradation constant. The rate constants of the reactions under UV irradiation were nearly one hundred times greater than those of the reactions under VL irradiation. The Diuron was virtually completely removed within 30 min under UV irradiation, whereas an average of only 41.75% was removed under VL irradiation after 6 h, which ascribed to the significantly greater absorbance by Diuron in the UV range than in the VL range (Fig. S3). The indirect photolysis of Diuron in the presence of AOM and FA was compared; the results are shown in Fig. 2 and Table 1. Phycocyanin in IOM and FA has been reported to act as a photo-sensitizer under sunlight irradiation and therefore may have facilitated the reactions by producing various ROSs, including 1 DO2, OH, and excited-state DOM, presumably 3DOM⁄ [28],

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0

0

-1 -2 ln [Ct]/[C0]

ln [Ct]/[C0]

-0.2

-0.4 pH=2 pH=5 -0.6

-3 -4

pH=2

-5

pH=5 pH=7

pH=7

-6

pH=9

pH=9

-7

-0.8 0

60

120

180 Time (min) (a)

240

300

0

360

5

10

15

20

25

30

Time (min) (b)

0

0

-0.2

-0.2 ln [Ct]/[C0]

ln [Ct]/[C0]

Fig. 1. Degradation of Diuron by direct photolysis at various initial pH levels under (a) visible light irradiation and (b) UV irradiation.

Control

-0.4

IOM EOM

-0.6

Control

-0.4

IOM EOM

-0.6

FA

FA -0.8

-0.8 0

60

120

180 240 Time (min)

300

0

360

60

120

-0.2

-0.2

Control IOM EOM

-0.6

-0.4

360

180 240 Time (min)

300

360

IOM EOM

-0.6

FA

-0.8 60

300

Control

FA 0

240

(b) 0

ln [Ct]/[C0]

ln [Ct]/[C0]

(a) 0

-0.4

180 Time (min)

120

180

240

300

360

-0.8 0

60

Time (min)

(c)

120

(d)

Fig. 2. Indirect photolysis of Diuron by intracellular organic matter (IOM), extracellular organic matter (EOM) and fulvic acid (FA) under visible light irradiation at various initial pH levels: (a) pH 2, (b) pH 5, (c) pH 7 and (d) pH 9.

Table 1 The removal rate of Diuron and the rate constants of the reactions in the absence and presence of 6 mg L1 DOM (IOM, EOM and FA) at an initial pH of 7 under visible light and UV irradiation. Irradiation condition

Control Removal rate (%)

IOM

EOM

FA

Rate constant (s1)

Removal rate (%)

Rate constant (s1)

Removal rate (%)

Rate constant (s1)

Removal rate (%)

Rate constant (s1)

Visible light

36.96

(1.30 ± 0.40)  103

34.06

(1.10 ± 0.10)  103

39.75

(1.40 ± 0.15)  103

24.11

(0.70 ± 0.01)  103

UV

99.53

(1.79 ± 0.15)  101

99.13

(1.58 ± 0.05)  101

98.70

(1.48 ± 0.08)  101

94.06

(0.93 ± 0.04)  101

whereas EOM might not be as capable of producing 3DOM⁄ due to EOM’s lack of phycocyanin [15]. In contrast, those photo-sensitizers and other co-existing organic matter in AOM, such as proteins and polysaccharides, may suppress the degradation by screening out reactive wavelengths of light or by scavenging ROSs [29–32]. In addition, humic acid-like compounds, due to

their antioxidant properties, inhibit the degradation by reducing the oxidation intermediates of the Diuron back to their parent compounds. The slightly lower rate of Diuron removal in the presence of IOM, as shown in Table 1 and Fig. 2, indicates a similar set of conflicting roles of IOM, specifically those of facilitating and inhibiting

L. Li et al. / Chemical Engineering Journal 281 (2015) 265–271 0

0

-0.2

-0.2

ln [Ct]/[C0]

ln [Ct]/[C0]

268

-0.4 IOM only IOM + 2-propanol

-0.6

-0.4 EOM only EOM + 2-propanol

-0.6

EOM + sorbic acid

IOM + sorbic acid -0.8

-0.8 0

60

120

180

240

300

0

360

60

120

180

Time (min)

Time (min)

(a)

(b)

240

300

360

0

ln [Ct]/[C0]

-0.2

-0.4 FA only FA + 2-propanol

-0.6

FA + sorbic acid -0.8 0

60

120

180 240 Time (min)

300

360

(c) Fig. 3. Photo-degradation of Diuron under visible light irradiation at an initial pH of 7 in the presence of AOM and DOM and various quenching or enhancing agents: (a) IOM, (b) EOM and (c) FA.

Table 2 The contributions of various radical species to the degradation of Diuron at an initial pH of 7 in the presence of 6 mg L1 IOM, EOM and FA and the rate constants of the degradation after adding various scavengers. Radical species



OH

3

DOM⁄

IOM

EOM

Percent (%)

Rate constant (s1)

27.27 81.82

FA

Percent (%)

Rate constant (s1)

Percent (%)

Rate constant (s1)

(0.80 ± 0.01)  103

50.00

(0.70 ± 0.01)  103

28.57

(0.50 ± 0.01)  103

(0.20 ± 0.02)  103

63.57

(0.51 ± 0.01)  103

71.43

(0.20 ± 0.01)  103

Table 3 The removal rates of Diuron and the rate constants of the reactions in the absence and presence of 6 mg L1 AOM at various initial pH levels under visible light and UV irradiation. Irradiation condition

pH

Control Removal rate (%)

IOM Rate constant (s1) 3

EOM

Removal rate (%)

Rate constant (s1)

Removal rate (%)

Rate constant (s1)

3

Visible light

2.0 5.0 7.0 9.0

48.46 46.64 36.96 34.93

(1.80 ± 0.50)  10 (1.80 ± 0.02)  103 (1.30 ± 0.40)  103 (1.15 ± 0.05)  103

36.53 45.38 34.06 32.11

(1.25 ± 0.15)  10 (1.60 ± 0.12)  103 (1.10 ± 0.10)  103 (1.10 ± 0.01)  103

34.48 51.52 39.75 40.29

(1.20 ± 0.02)  103 (2.10 ± 0.28)  103 (1.40 ± 0.15)  103 (1.45 ± 0.05)  103

UV

2.0 5.0 7.0 9.0

99.64 99.80 99.53 98.79

(1.94 ± 0.13)  101 (2.13 ± 0.04)  101 (1.79 ± 0.15)  101 (1.44 ± 0.11)  101

99.53 99.54 99.13 97.55

(1.86 ± 0.18)  101 (1.93 ± 0.13)  101 (1.58 ± 0.05)  101 (1.23 ± 0.10)  101

99.34 99.74 98.70 97.90

(1.69 ± 0.15)  101 (2.02 ± 0.03)  101 (1.48 ± 0.08)  101 (1.29 ± 0.05)  101

photo-degradation. By comparison, the intense suppression of Diuron degradation in the presence of FA implies that the FA acted more as an inhibitor than a photo-sensitizer in this study, which was inconsistent with findings of previous studies, in which the presence of HA and FA greatly enhanced the decomposition of atorvastatin and amoxicillin under conditions of simulated sunlight [28,33]. This inconsistency may be ascribed to the different chemical structures and properties of the selected representative contaminants which probably affect the interactions during the indirect photolysis.

3.2. The contributions of various ROSs to the reaction Scavengers were added to the solutions to qualitatively demonstrate the role of various reactive species; the results are shown in Fig. 3. The addition of the OH scavenger 2-propanol (65 mM) to the Diuron solution in the presence of DOM (EOM, IOM and HA) decreased the reaction rates by as much as 50%, which indicates that OH played an important role in the photo-degradation of the Diuron. Nevertheless, the incomplete suppression of the reaction with the addition of the OH scavenger indicates the

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L. Li et al. / Chemical Engineering Journal 281 (2015) 265–271 700

600

700 0 50 100 150 200

600

500 Ex (nm)

Ex (nm)

500

0 50 100 150 200

400

400

300

300

200 200

300

400

500

600

200 200

700

300

Em (nm)

400

500

(a1)

700

600

700

(a2)

700

600

600

Em (nm) 700

0 50 100 150 200

600

500 Ex (nm)

Ex (nm)

500

0 50 100 150 200

400

400

300

300

200 200

300

400

500

600

200 200

700

300

Em (nm)

400

500

Em (nm)

(a3)

(a4)

700

600

700 0 50 100 150 200

600

Ex (nm)

500

Ex (nm)

500

0 50 100 150 200

400

400

300

300

200 200

300

400

500

600

200 200

700

300

Em (nm)

500

600

700

600

700

Em (nm)

(b1)

(b2)

700

600

400

700 0 50 100 150 200

600

Ex (nm)

500

Ex (nm)

500

0 50 100 150 200

400

400

300

300

200 200

300

400

500

Em (nm) (b3)

600

700

200 200

300

400

500

Em (nm) (b4)

Fig. 4. EEMs produced by IOM and EOM under various pH conditions: IOM at (a1) pH 2, (a2) pH 5, (a3) pH 7 and (a4) pH 9; EOM at (b1) pH 2, (b2) pH 5, (b3) pH 7 and (b4) pH 9.

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involvement of other types of ROSs or direct decomposition of Diuron during the degradation. The rates of Diuron degradation in the presence of IOM and FA were observed to decrease by 27.27% and 28.57%, respectively. These decreases were considerably smaller than that associated with EOM (50%), as shown in Fig. 3 and Table 2, which implies that pigments in the IOM and colored substances in the FA were likely the major sensitizing components that generated the 3DOM⁄ and accelerated Diuron degradation. Sorbic acid, which is reportedly a strong triplet excited-state quencher, was added to the solar irradiation system to quantitatively measure the portion of 3DOM⁄ that participated in the reaction [26,28,34]. Significant decrease in the value of k, specifically 81.82%, 63.57% and 71.43%, in the presence of IOM, EOM and FA, respectively, indicated the substantial involvement of 3DOM⁄ in the Diuron degradation. The contributions of various radical species were calculated using Eqs. (5) and (6).

Contribution OH ð%Þ ¼

k  k2proponal  100% k

Contribution3 DOM ð%Þ ¼

k  ksorbic acid  100%; k

ð5Þ

ð6Þ

where k represents the rate constants of each original reaction in the presence of DOM but without the addition of radical quenchers and k2-proponal and ksorbic acid represent the rate constants in the presence of the scavengers. The resulting data are summarized in Table 2. The sum of the contributions of 3DOM* and OH equaled or slightly exceeded 100%, which indicates the minor involvement of other ROSs (e.g., 1DO2) in this system. Evidently, the generation of 3DOM⁄ and OH accounted for the majority of the Diuron removal and 3DOM⁄ in this study. 3.3. Reaction constants and EEMs produced by AOM as a function of pH As shown in Fig. 1, the rate constants of the Diuron degradation steadily increased with successively lower initial pH levels (maximum pH of 9) and reached a maximum value at a pH of 5. At a pH of 5, the values of kobs under VL and UV irradiation were 1.80  103 s1 and 2.13  101 s1, respectively. Slight decreases in the rate constants were observed with further lowering of the initial pH level from 5 to 2. Nevertheless, the effects of pH levels on the degradation of Diuron were reportedly small compared to their effects on the photo-degradation of other contaminants [35,36], possibly due to the neutral state of the Diuron molecule within certain pH ranges. In Fig. 2, the reaction constants of the Diuron degradation as a function of the initial pH in the presence of EOM, IOM and FA exhibited a pattern similar to that of direct photo-degradation (Fig. 1). At pH levels of 5, 7 and 9, the total amounts of degradation in the presence of EOM were increased by as much as 26% compared to the control group. Given that EOM was not as capable of producing 3DOM⁄, as were IOM and FA, due to EOM’s lack of phycocyanin, as discussed in Section 3.1, the intermediate oxidant promoting the Diuron degradation was most likely OH rather than 3 DOM⁄. In contrast, the reaction rates were slightly decreased, i.e., <20%, at initial pH levels of 5, 7 and 9 in the presence of IOM, whereas this decrease amounted to 30.56% at an initial pH of 2; this pattern indicates that the IOM’s function as an inhibitor was predominant over its function as a photo-sensitizer and therefore led to a greater decrease in the reaction rate versus the control group. Considering that the DOC of IOM is normally 3–5 times more than that of EOM in natural waters according to the authors’ previous publication [15], the presence of AOM (both IOM and EOM) can result in a slower overall rate of Diuron degradation.

Detailed comparisons of kobs for the indirect and direct degradation reactions under UV and VL irradiation are listed in Table 3. Previous studies have demonstrated that EEM fluorescence spectroscopy is a powerful, rapid, and sensitive tool for AOM characterization [37,38]. The EEMs of AOM in response to various pH levels are shown in Fig. 4. The peaks at an Ex/Em of 275/340 nm belong to the aromatic amino acid tryptophan and protein-like compounds, and the peak at an Ex/Em of 230/340 nm corresponds to tyrosine, another amino acid. Other peaks were assigned to so-called humic acid or fulvic acid-like matter, which correspond to the Ex/Em regions of 355/455 and 275/450 nm, respectively [39]. IOM produced intense peaks located in the Ex/Em regions of 600/650 and 350/650 nm, which represent considerable concentrations of phycocyanin and chlorophyll-a [40]. Additional peaks that plot in the lower right corner remain unknown and require further investigation. As shown in Fig. 4, the Em/Ex intensities produced by phycocyanin and chlorophyll-a and other protein-like compounds in the IOM at pH 2 were much smaller than those produced at other pH levels. The variations in the EEM peak intensities in various regions produced by the EOM at various pH values exhibited a similar pattern. The large reduction in EEM peaks produced by both EOM and IOM at low pH values indicates a loss of photo-sensitizers, which is consistent with the considerable decrease in the rates of Diuron photo-degradation at pH 2, as discussed in the first half of this section. 4. Conclusions The kinetics of Diuron photo-degradation in the presence of AOM extracted from M. aeruginosa were investigated in this study. Diuron was rapidly removed under UV irradiation accompanied by minor impacts from AOM. Under VL irradiation, the photo-excited phycocyanin in the IOM was capable of accelerating the degradation of Diuron, whereas the coexistence of other organic compounds in the IOM inhibited the reaction due to a screening effect, leading to a slower overall rate of Diuron degradation in the presence of IOM. By comparison, EOM promoted the reactions when the pH exceeded 5. Because the DOC of IOM is normally 3-5 times than that of EOM in the natural environment, the presence of M. aeruginosa and AOM may interfere with the photo-degradation and the ultimate fate of Diuron in aquatic systems. The environmental fates of other types of organic pollutants, such as pharmaceuticals and endocrine-disrupting chemicals, in the presence of AOM warrant further study. Acknowledgments This research was financially supported by the National Natural Science Foundation of China (51308398), National Water Pollution Control and Treatment Key Technologies R&D Program (No. 2012ZX07403-001), State Key Laboratory of Pollution Control and Resource Reuse Foundation (PCRRY12002), and Shanghai Pujiang Program (No. 14PJ1432400). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.cej.2015.06.091. References [1] N. Nakada, H. Shinohara, A. Murata, K. Kiri, S. Managaki, N. Sato, H. Takada, Removal of selected pharmaceuticals and personal care products (PPCPs) and endocrine-disrupting chemicals (EDCs) during sand filtration and ozonation at a municipal sewage treatment plant, Water Res. 41 (2007) 4373–4382.

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