The role of nitrobenzene on the yield of trihalomethane formation potential in aqueous solutions with Microcystis aeruginosa

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The role of nitrobenzene on the yield of trihalomethane formation potential in aqueous solutions with Microcystis aeruginosa Zhiquan Liu, Fuyi Cui*, Hua Ma, Zhenqiang Fan, Zhiwei Zhao State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (SKLUWRE, HIT), PO Box 2650, Harbin 150090, China

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abstract

Article history:

Algae are one of the most important disinfection by-product (DBP) precursors in aquatic

Received 14 July 2011

environments. The contents of DBP precursors in algae are influenced by not only envi-

Received in revised form

ronmental factors but also some xenobiotics. Trihalomethane formation potential (THMFP)

12 September 2011

in both the separate and interactive pollution of Microcystis aeruginosa and Nitrobenzene

Accepted 21 September 2011

(NB) was investigated in batch experiment to discover the effects of xenobiotics on the

Available online 1 October 2011

yield of DBP precursors in the algal solution. The results show that in the separate NB solution, NB did not react with Cl2 to form trihalomethane (THM), whereas in the algae

Keywords:

solution, THMFP had a significant positive linear correlation with M. aeruginosa density in

Microcystis aeruginosa

both solution and extracellular organic matter (EOM). The correlation coefficients were

THMFP

0.9845 ( p ¼ 3.567  104) and 0.9854 ( p ¼ 1.406  104), respectively. According to regression

Nitrobenzene

results, about 77.9% of the total THMFP came from the algal cells, while the rest came from EOM. When the interactive pollution of M. aeruginosa and NB occurred, the growth of algae was inhibited by NB. The density of M. aeruginosa in a high concentration NB solution (280 mg/L) was only 71.1% of that in the solution without NB after 5 days of incubation. However, THMFP in the mixture (algae and NB) and the EOM did not change significantly, and the productivity of THMFP by the algae (THMFP/108cells) increased with the increase in NB concentration. There was a significant linear correlation between THMFP/108cell and NB concentration (r ¼ 0.9117, p < 0.01), which shows the contribution of the algae to THM formation was enhanced by NB. This result might be caused by the increased protein productivity and the biodegradation of NB by M. aeruginosa. ª 2011 Elsevier Ltd. All rights reserved.

1.

Introduction

Chlorination of drinking waters can produce trihalomethanes (THMs), haloacetic acids (HAAs) and other types of disinfection by-products (DBPs) (Oliver, 1983). Previous research has indicated that natural organic matter (NOM) in aquatic environment (Li et al., 2000; Gang et al., 2003), such as humic and

fulvic acid, and algae (Graham et al., 1998; Plummer and Edzwald, 1998, 2001) are precursors of these by-products. The production rate of DBPs by algae varies depending on the algal biomass, algae species and algal growth phase. Moreover, it has been confirmed that both algal cells and extracellular organic matter (EOM) can be chloridised to form DBPs, and that the yield of the DBPs from the cells is greater

* Corresponding author. Tel.: þ86 451 86282098. E-mail address: [email protected] (F. Cui). 0043-1354/$ e see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2011.09.043

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than that from the EOM (Wachter and Andelman, 1984; Oliver and Shindler, 1980; Huang et al., 2009). Oliver and Shindler (1980) showed that the majority of the precursors came from algal cells or cell fragments. Industrial and agricultural growth has caused a large number of synthetic organic compounds to be discharged into the aquatic environment. Xenobiotics transferred into algal cells by bioaccumulation and bio-absorption might inhibit the reproduction of algae (Thies et al., 1996; Warshawsky et al., 1990; Sijm et al., 1998). Both xenobiotics and algae can cause direct or indirect problems in drinking water, and these problems may be more serious when interactive pollution occurs. The production of DBPs during chlorination is one of these problems. However, while the relationship between DBPs and algae has been thoroughly studied (Wachter and Andelman, 1984; Oliver and Shindler, 1980; Huang et al., 2009; Karimi and Singer, 1991; Hoehn et al., 1984), there is very little research on the effect of xenobiotics on the yield of DBPs in algal solutions. Nitrobenzene (NB) is used extensively in industrial manufacturing synthetic resins, pesticides, dyes, drugs, pharmaceuticals, and so forth. Large areas of soil and ground water have been contaminated by these xenobiotics (Patil and Shlnde, 1988; Kulkarni and Chaudhari, 2007), which may affect the growth of algae and cause DBP problems. Prior studies showed that it was difficult to form THMs in the presence of NB (Guo and Lin, 2009), which implies that NB should not affect the THM productivity of algae if there is no interaction between them. For this reason, NB was selected in this paper to study the effect of xenobiotics on the yield of DBPs by Microcystis aeruginosa, a species of cyanophytes that can cause algal blooms. The trihalomethane formation potential (THMFP) in both separate and interactive pollution scenarios was investigated.

2.

Materials and methods

2.1.

Materials

keep the algae in its exponential growth phase. The observed M. aeruginosa were individual spherical cells instead of colonies, which is quite different from M. aeruginosa that are observed in natural waters. The algae in the exponential growth phase were centrifuged and the algal pellets were resuspended with distilled water for further experimentation. The resuspended algal pellets were incubated in a 500-mL conical beaker with one-tenth of the full strength BG11 medium and with or without NB. The total volume of the algal solution was 250 mL. All the samples and algal stock solutions were incubated in an illuminating incubator with a temperature of 25  1  C. Cool white fluorescent-light was provided with 3300lx of illumination in a 14 h light/10 h dark cycle. Algal density was monitored by cell number counting with a microscope (Olympus BX41) according to the method adopted in Ma’s paper (Ma et al., 2009). Duplicate measurements were taken and the arithmetical means (SD) were obtained and used as the final density.

2.3. Extracellular and intracellular organic matter separation The algal solution was centrifuged for 20 min at a speed of 8000r/min. The supernatant contained EOM and was collected to assess the contribution of the algae to THM formation and the concentration of proteins and carbohydrates. The concentration of the EOM was correlated to the algal density in original algal solution instead of the dissolved organic carbon (DOC) which could be easily compared with the THMFP of the algal cells (approximately 4.5e6.5  108 cells/L). The pellets were resuspended in the same volume of distilled water and were subjected to sonication (Sonics 130 W/50 Hz, USA) in an ice bath with the amplitude of 100% for six 30-s periods separated by 15-s intervals. The suspension was centrifuged for 20 min at a speed of 8000r/min and the supernatant contained intracellular organic matter (IOM) that was used for the protein and carbohydrate analyses.

2.4. The stock culture of M. aeruginosa was purchased from the Institute of Hydrobiology at the Chinese Academy of Sciences. Nitrobenzene (CAS: 98-95-3), methyl tert-butyl ether (MTBE, CAS: 1634-04-4) and inorganic reagents were purchased from Tianjin Kermel Chemical Reagent Co. Ltd. All the chemical reagents were of analytical grade except MTBE (GR). The needed standard materials, CHCl3, CHBr2Cl, CHBrCl2 and CHBr3, were purchased from J&K Scientific Ltd. A Pierce BCA Protein Assay Kit was purchased from Thermo Fisher Scientific, Inc.

2.2.

Algal culturing

The purchased stock culture of M. aeruginosa was treated by a method adopted from Semple and Cain (1996) to obtain axenic M. aeruginosa. Axenic stock culture of M. aeruginosa was incubated in a 1000-mL flat bottomed flask with a cotton plug containing approximately 500 mL of BG11 medium (Stanier et al., 1971) to ensure sufficient CO2 exchange. Approximately half of each algal suspension was discarded and the same volume of BG11 medium was added every 15 days to

Chlorination and THMs analysis

THMs were detected by gas chromatography with electron capture detection by a modified EPA method (EPA 551.1), as described by Wang et al. (2009). The pH of all the samples (including the NB solution, algal solution, the mixture of NB, algae and EOM) was adjusted to 7 by HCl before chlorination. A phosphate buffer was added to maintain the pH. The samples were incubated in the dark at 25  1  C. The doses of chlorine and the reaction time were determined by experimentation to obtain the maximum production of THMs, which is THMFP. High density algal solutions were diluted with distilled water and the THMFP was calculated by the following formula: C ¼ ðC0  Cw Þ  n þ Cw

(1)

where C is the THMFP concentration in original samples (mmol/L), C0 is the THMFP concentration in diluted samples (mmol/L), Cw is the THMFP concentration in distilled water (mmol/L) and n is the dilution factor. THMFP in the algal solution and in the EOM were measured, and the difference

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2.5.

Protein and carbohydrate analyses

Proteins were detected by the bicinchoninic acid (BCA) method (Pierce BCA Protein Assay Kit, Thermo Scientific, USA). Carbohydrates were detected by the phenolesulphuric acid method (DuBois et al., 1956), and the concentration was calculated in mg of glucose per 108 cells. Both proteins and carbohydrates in the EOM and the IOM were monitored.

25 Algal solution EOM 20 Total THMs(µmol/L)

between them was assumed to be the THMFP of the cells. The lack of bromine caused chloroform to be detected in all the samples. All the measurements were taken in triplicate and the arithmetical means (SD) were obtained and used as the final values.

15

10

5

0 0

3.

Results and discussions

3.1.

Chlorination conditions

2

4 6 Time (day)

8

10

Fig. 2 e Total THM in the algal solution and the EOM for different reaction times (1.1 3 108 cells/L, 1600 mgCl2/L, 25 ± 1  C, pH 7, in the dark).

In prior research (Graham et al., 1998; Plummer and Edzwald, 2001; Oliver and Shindler, 1980; Nguyen et al., 2005; Huang et al., 2009), chlorine doses were usually chosen to ensure a substantial residual amount of chlorine (>3 mg/L or more) in accordance with standard methods. However, the THMs in the samples always increased with the reaction time and the chlorine dose, which indicates that organic matter in algal solutions were not thoroughly chlorinated. In this paper, the doses of chlorine and the reaction time were determined by experimentation to ensure that the reaction was thoroughly completed. Experiments were conducted with a cell density of 1.1  108 cells/L under standardized pH (pH ¼ 7) and temperature (25  1  C) in the dark with different chlorine doses and reaction times. THMs were detected in the algal solutions and in the EOM. The results showed that with the same reaction time (3 days), the amount of THMs increased with the chlorine dose for low doses (less than 200 mg/L) and that dose of 200 mg/L is sufficient for chlorination (Fig. 1). With the same chlorine dose (1600 mg/L), the maximum amount of THMs was obtained after 7 days of reaction time (Fig. 2). According to the results, the actual dose is

confirmed to be 1600 mg/L, which ensures that thorough chlorination is completed in 7 days. When the density of algae is higher than 1.1  108 cells/L, the sample is diluted with distilled water until the density is lower than 1.1  108 cells/L, and then, the THMFP is calculated by formula (1). The chlorination experiments were performed to study the potential for by-products formation by algae in the separate and interactive pollution scenarios of M. aeruginosa and NB. High doses of Cl2 were used to ensure that all of the THMFP had been chloridised. Thus, the chlorination conditions were quite different from those applied to actual drinking water and do not reflect the real production of THMs under the actual conditions.

3.2.

THMFP in separate pollution samples

3.2.1.

THMFP in NB solution

NB solutions were chloridised under the pre-set conditions described in 2.4 and 3.1. The total THMFP in NB solutions

1.0 25 Algal solution EOM

0.8 Total THMs (µmol/L)

Total THMs(µmol/L)

20 15 10 5

0.6 0.4 0.2 0.0

0 0

300

600

900 1200 [Cl2](mg/L)

1500

1800

Fig. 1 e Total THM in the algal solution and the EOM for different chlorine doses (1.1 3 108 cells/L, 3 days, 25 ± 1  C, pH 7, in the dark).

0

50

100

150

200

250

300

350

concentration of NB(µg/L) Fig. 3 e Total THM in the NB solution (Chlorination conditions: 1600 mgCl2/L, 7 days, 25 ± 1  C, pH 7, in the dark).

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350

Total THMs EOM

3.2.2.

Linear fit of Total THMs Linear fit of EOM

Total THMs (µmol/L)

300

y=12.42x 2 R =0.959

250 200 150

y=2.74x 2 R =0.955

100 50 0 0

5

10 15 20 8 Algal density (10 cells/L)

25

30

Fig. 4 e Total THMFP in the algal solution and the EOM (no NB; THMFP is obtained by the formula 0 C [ (C L Cw) 3 n D Cw; Chlorination conditions: 1600 mgCl2/L, 7 days, 25 ± 1  C, pH 7, in the dark).

ranged from 0.58 to 0.71 mmol/L (Fig. 3), which was approximately equal to that of distilled water (0.65  0.043 mmol/L). No linear correlation was found between the THMFP and the NB concentration (r ¼ 0.2258, p ¼ 0.6264). This result indicated that NB could not react with chlorine to form THMs, and that the total THMFP of NB solution came from the solvent, rather than the NB. It also implied that the dosage of NB in the algal solution would not affect the yield of THMFP produced by the algae, if there was no interaction between the algae and the NB. Because of the high concentration of THMFP in distilled water, the formula in section 2.4 was used to eliminate the interference due to the distilled water.

8

60

6 40 4 20

2

0 0

50

100

150

200

250

8

Total THMs(mmol/L)

10 Algal density (×10 cells/L)

Algal density In the mixture of algae and NB in EOM of the mixture

80

0 300

THMFP in the M. aeruginosa solution

The concentration gradient of M. aeruginosa was obtained by incubating a low density of algae in conical beakers for different periods (10e20 days) to avoid the influence of dilution. The initial algal densities were lower than 108 cells/L. Chlorination and calculations were carried out as described in sections 2.4 and 3.1. The results are shown in Fig. 4. THMFP yields increased with increasing algal density, and there was a significant positive linear correlation between THMFP and algal density for solutions that included both algal solution and EOM; the related coefficients were 0.9845 ( p ¼ 3.567  104) and 0.9854 ( p ¼ 1.406  104), respectively. This result indicates that M. aeruginosa is an important precursor of disinfection by-products in the aquatic environment, as also found in previous research (Graham et al., 1998; Plummer and Edzwald, 2001; Oliver and Shindler, 1980; Nguyen et al., 2005). According to the results of regression, every 108 algal cells could yield 12.42 mmol THM (include the cells and the EOM), while the corresponding amount of EOM could only yield 2.74 mmol THM, which is approximately 22.1% of the total THMFP. The results are in agreement with previously published results (Plummer and Edzwald, 2001; Huang et al., 2009). The fact that the cells have higher THM formation than the EOM implies that it is necessary to remove algal cells physically before oxidation to reduce THM production. In some previous studies (Huang et al., 2009; Kanokkantapong et al., 2006), researchers have found that the composition and production of DBPs is influenced by the interaction of the algal cells with the EOM, and they have provided several explanations. However, the chlorine dosage was not mentioned in these explanations. Chlorination was usually performed that the residual of chlorine was no less than 0.5e3 mg/L and the reaction time was no more than 7 days, in accordance with practical situations. In those cases, the reactions were terminated without complete oxidation (Plummer and Edzwald, 1998, 2001; Wachter and Andelman, 1984; Oliver and Shindler, 1980) and the products may have been affected by the consumption of chlorine. This could explain why Kanokkantapong et al. (2006) found that the majority of HAAs formation changed from dichloroacetic acid in individual organic fractions to monochloroacetic acid in the mixture (Kanokkantapong et al., 2006). Huang et al. (2009) found that the yields of THMs in mixtures of algal cells and EOM were less than that in just the cells, even less than that in only EOM solutions (residual of chlorine>0.5 mg/L). This founding can also be explained by the lack of chlorine, which can be further supported by the phenomenon that the difference between the yields of THMs in the mixture, in the cells and in the EOM after a 1-day chlorination period is less obvious than the difference in the yield after a 7-day period, as shown in Huang’s paper. For this reason, excess chlorine was used in our experiment to reduce the amount of interference. The residual chlorine was usually more than 100 mg/L.

Concentration of NB (µg/L) Fig. 5 e Effect of NB on the yield of THMs and the reproduction of Microcystis aeruginosa (5 days incubation; 0 THMFP is obtained by the formula C [ (C L Cw) 3 n D Cw; Chlorination conditions: 1600 mgCl2/L, 7 days, 25 ± 1  C, pH 7, in the dark).

3.3. THMFP in interactive pollution of M. aeruginosa and NB The solutions with NB and algae were prepared by mixing the stock culture of M. aeruginosa and NB working solution. The

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Table 1 e Productivity of THMs in the mixture, the EOM and the cells (Chlorination conditions: 1600 mgCl2/L, 7 days, 25 ± 1  C, pH 7, in the dark). THMs productivity (mean  SD, mmol/108 cells)

Initial NB concentration (mg/L)

In the mixture

0 40 80 160 200 240 280

10.31 11.50 11.22 11.50 11.83 12.68 13.46

In the EOM

 2.10  1.81  1.10  2.10  1.11  1.97  1.94

% in EOM In the cells

2.36  0.51 2.68  0.44 2.43  0.40 3.11  0.39 2.45  0.21 2.98  0.90 3.86  0.30

7.95 8.82 8.78 8.38 9.38 9.70 9.60

 1.61  1.42  0.86  1.84  0.93  1.13  1.64

22.92% 23.31% 21.71% 27.07% 20.73% 23.52% 28.66%

THMs/cell in the cells was obtained as the difference of that in the mixture and in the EOM.

6

IOM EOM

2

y=0.0037x+1.96 2 R =0.228 0 0

50

100 150 200 Concentration of NB (µg/L)

Fig. 6 e Effect of NB on carbohydrate productivity by M. aeruginosa (after 5 days incubation).

IOM EOM

10

Linear Fit of IOM Linear Fit of EOM

y=-0.00014x+3.53 R2=0.025

4

approximately 24% of the total THMFP, which was a little higher than that in the algal solution without NB, and no linear correlation was found between the percentage and the NB concentration. The results of the correlation analysis imply that some organics were produced by the algae that could be chloridised to form THMs. These organics come from two possible pathways. The first pathway is that the organics may come from algal secretion. The results of prior studies have shown that antioxidant enzyme activities in algal cells could be enhanced by exposure to xenobiotics (Yang et al., 2002; Pugmacher et al., 1999). It could be inferred that some other types of organic matter that might be in the THMs’ precursor pool may be secreted when the algae is exposed to xenobiotics. The concentrations of proteins and carbohydrates in the EOM and in the IOM were investigated and the results are shown in Figs. 6 and 7. The presence of NB did not significantly affect the algae’s carbohydrate productivity (r ¼ 0.4778, p ¼ 0.3378 in IOM; r ¼ 0.07377, p ¼ 0.7634 in EOM), but it did increase protein productivity significantly (r ¼ 0.7700, p ¼ 0.0733 in IOM; r ¼ 0.9301, p ¼ 0.00716 in EOM). Hong et al. (2009) and Philippe et al. (2010) proved that amino acids are precursors of trihalomethane. Proteins, as combined amino acids, can also be in THMs precursor pool (Scully et al., 1988). In this case, the

Proteins productivity by M.aeruginosa 8 (mg/10 cells)

Carbohydrates productivity by M.aeruginosa 8 (mg glucose/10 cells)

initial density of algae was 3.81  108 cells/L while the initial concentration of NB ranged from 0 m/L to 280 m/L. After 5 days of incubation, THMFP in both solutions and the EOM of the mixture was detected. The reproduction of M. aeruginosa was obviously inhibited by NB (Fig. 5). After 5 days of incubation, the density of the algae decreased with increasing NB concentration, and the density of M. aeruginosa in high concentrations of the NB solution (280 mg/L) was only 71.1% of that in the solution without NB. However, THMFP in the mixture of algae and NB did not change significantly with the algal density. The result was also observed for THMFP in the EOM, as shown in Fig. 5. The specific productivity of THMFP, expressed as mmol/108 cells, was used to show the capacity of THMFP produced by algae, which increased with increasing NB concentrations in both the mixture and the EOM (Table 1). The results indicate that the yield of THMFP by algae was enhanced by the presence of NB although NB could not be chloridised to form THMs directly. There was a significant linear correlation between the THMFP/cells in the mixture and the NB concentration (r ¼ 0.9117, p < 0.01). However, the correlations between THMFP/cell in the EOM or in cells and the NB concentration were not as significant as with the NB concentration in the mixture (r ¼ 0.7305, p ¼ 0.0622; r ¼ 0.8358, p ¼ 0.0192, respectively). The THMFP coming from the EOM accounted for

250

8

Linear Fit of IOM Linear Fit of EOM

y=0.01038x+5.095 2 R =0.592

6

y=0.01001x+3.747 R2=0.865

4 2 0 0

50

100 150 200 Concentration of NB (µg/L)

Fig. 7 e Effect of NB on protein productivity by M. aeruginosa (after 5 days incubation).

250

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increased proteins productivity can explain why the algal yield of THMs increased in interactive pollution of M. aeruginosa and NB. The second pathway is that the organics may come from the intermediate biodegradation of NB with M. aeruginosa. It has been proven that some species of algae are capable of heterotrophic growth on xenobiotics (Semple et al., 1999; Semple and Cain, 1996) and the biodegradation of NB with M. aeruginosa was also found in our research (data not shown). During the aerobic biodegradation of nitro-aromatic compounds, numerous phenolic hydroxyl groups are generated (Kulkarni and Chaudhari, 2007), which can be chloridised to form THMs (Galapate et al., 2001; Norwood et al., 1980). These intermediate compounds contained phenolic hydroxyl groups that may make a contribution to the increase of THMFP productivity in the interactive pollution of M. aeruginosa and NB. The fact that NB increases THMFP productivity by algae may not be a serious problem, but it is an important fact that cannot be overlooked by researchers who are interested in algal problems. Usually, researchers only pay attention to separate algae pollution, without considering the interference of xenobiotics. However, in the real-world situations, there is no separate algae pollution, only interactive pollution, and the algae may affected by some xenobiotics. Our study has shown the interaction between algae and xenobiotics really exists. Thus, it is necessary to understand the characteristics of interactive pollution of algae and xenobiotics and the effect of that interaction on water treatment.

4.

Conclusions

In this paper, the THMFP in both separate and interactive pollution of M. aeruginosa and NB were studied. The key findings of this research were listed below:  Nitrobenzene barely reacts with chlorine to form THMs.  M. aeruginosa is an important trihalomethane formation potential, and the algal cells can provide more THMFP than the EOM. Only approximately 22.4% of the total THMFP came from the EOM, according to the to the regression results.  The presence of NB can increase THMFP productivity by M. aeruginosa. These increased THMFP may come from both the increased proteins productivity and the intermediate biodegradation of NB by M. aeruginosa.

Acknowledgements This work was supported by a grant from the National Creative Research Groups (Grant No. 50821002) and the National Natural Science Foundation of China (Number: 50778048).

Appendix. Supplementary data Supplementary data related to this article can be found online at doi:10.1016/j.watres.2011.09.043.

references

DuBois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956. Colorimetric method for determination of sugars and related Substances. Analytical Chemistry 28 (3), 350e356. doi: 10.1021/ac60111a017. Galapate, R.P., Baes, A.U., Okada, M., 2001. Transformation of dissolved organic matter during ozonation: effects on trihalomethane formation potential. Water Research 35 (9), 2201e2206. Gang, D., Clevenger, T.E., Banerji, S.K., 2003. Relationship of chlorine decay and THMs formation to NOM size. Journal of Hazardous Materials A 96 (1), 1e12. Graham, N.J.D., Wardlaw, V.E., Perry, R., Jiang, J., 1998. The significance of algae as trihalomethane precursors. Water Science and Technology 37 (2), 83e89. Guo, K., Lin, F., 2009. A study of disinfection by-products formation characteristics in the chlorination reactions of aromatic organic compounds. Water Purification Technology 28 (3), 27e31 (in Chinese). Hoehn, R.C., Dixon, K.L., Malone, J.K., Novak, J.T., Randall, C.W., 1984. Biologically induced variations in the nature and removability of THM precursors by alum treatment. Journal of the American Water Works Association 76 (4), 134e141. Hong, H., Wong, M., Liang, Y., 2009. Amino acids as precursors of trihalomethane and haloacetic acid formation during chlorination. Archives of Environmental Contamination and Toxicology 56, 638e645. doi:10.1007/s00244-008-9216-4. Huang, J., Graham, N., Templeton, M.R., Zhang, Y., Collins, C., Nieuwenhuijsen, M., 2009. A comparison of the role of two blueegreen algae in THM and HAA formation. Water Research 43 (12), 3009e3018. Kanokkantapong, V., Marhaba, T.F., Wattanachira, S., Panyapinyophol, B., Pavasant, P., 2006. Interaction between organic species in the formation of haloacetic acids following disinfection. Journal of Environmental Science and Health, Part A: Toxic/Hazardous Substances & Environmental Engineering 41 (6), 1233e1248. Karimi, A.A., Singer, P.C., 1991. Trihalomethane formation in open reservoirs. Journal of the American Water Works Association 3 (3), 84e88. Kulkarni, M., Chaudhari, A., 2007. Microbial remediation of nitroaromatic compounds: an overview. Journal of Environmental Management 85, 496e512. doi:10.1016/j.jenvman.2007.06.009. Li, C., Benjamin, M.M., Korshin, G.V., 2000. Use of UV spectroscopy to characterize the reaction between NOM and free chlorine. Environmental Science & Technology 34 (12), 2570e2575. Ma, H., Cui, F., Liu, Z., Fan, Z., 2009. Pilot study on control of phytoplankton by zooplankton coupling with filter-feeding fish in surface water. Water Science and Technology 60 (3), 737e743. Nguyen, M.L., Westerhoff, P., Baker, L., Hu, Q., Esparza-Soto, M., Sommerfeld, M., 2005. Characteristics and reactivity of algaeproduced dissolved organic carbon. Journal of Environmental Engineering 131 (11), 1574e1582. Norwood, D.L., Johnson, J.D., Christman, R.F., 1980. Reactions of chlorine with selected aromatic models of aquatic humic material. American Chemical Society 14 (2), 187e190. Oliver, B.G., Shindler, D.B., 1980. Trihalomethanes from the chlorination of aquatic algae. Environmental Science & Technology 14 (12), 1502e1505. Oliver, B.G., 1983. Dihaloacetonitriles in drinking water: algae and fulvic acid as precursors. Environmental Science & Technology 17 (2), 80e83. Patil, S.S., Shlnde, V.M., 1988. Biodegradation studies of aniline and nitrobenzene in aniline plant waste water by gas chromatography. Environmental Science & Technology 22 (10), 1160e1165.

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 6 4 8 9 e6 4 9 5

Philippe, K.K., Hans, C., MacAdam, J., Jefferson, B., Hart, J., Parsons, S.A., 2010. Photocatalytic oxidation of natural organic matter surrogates and the impact on trihalomethane formation potential. Chemosphere 81, 1509e1516. doi:10.1016/ j.chemosphere.2010.08.035. Plummer, J.D., Edzwald, J.K., 1998. Effect of ozone on disinfection by-product formation of algae. Water Science and Technology 37 (2), 49e55. Plummer, J.D., Edzwald, J.K., 2001. Effect of ozone on algae as precursors for trihalomethane and haloacetic acid production. Environmental Science & Technology 35 (18), 3661e3668. Pugmacher, S., Wiencke, C., Sandermann, H., 1999. Activity of phase I and phase II detoxication enzymes in Antarctic and Arctic macroalgae. Marine Environmental Research 48 (1), 23e36. Scully Jr., F.E., Howell, G.D., Kravitz, R., Jewell, J.T., Hahn, V., Speed, M., 1988. Proteins in natural waters and their relation to the formation of chlorinated organics during water disinfection. Environmental Science & Technology 22 (5), 537e542. Semple, K.T., Cain, R.B., 1996. Biodegradation of phenols by the alga Ochromonas danica. Applied and Environmental Microbiology 62 (4), 1265e1273. Semple, K.T., Cain, R.B., Schmidt, S., 1999. Biodegradation of aromatic compounds by microalgae. FEMS Microbiology Letters 170 (2), 291e300.

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Sijm, D.T.H.M., Broersen, K.W., Roode, D.F.D., Mayer, P., 1998. Bioconcentration kinetics of hydrophobic chemicals in different densities of Chlorella pyrenoidosa. Environmental Toxicology and Chemistry 17 (9), 1695e1704. Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G., 1971. Purification and properties of unicellular blue-green algae (Order Chroococcales). Microbiology and Molecular Biology Reviews 35 (2), 171e205. Thies, F., Backhaus, T., Bossmann, B., Grimme, L.H., 1996. Xenobiotic biotransformation in unicellular green algae. Plant Physiology 112, 361e370. Wachter, J.K., Andelman, J.B., 1984. Organohalide formation on chlorination of algal extracellular products. Environmental Science & Technology 18 (11), 811e817. Wang, H., Liu, D., Zhao, Z., Cui, F., Zhu, Q., Liu, T., 2009. Factors influencing the formation of chlorination brominated trihalomethanes in drinking water. Journal of Zhejiang University e Science A 11 (2), 143e150. Warshawsky, D., Keenan, T.H., Reilman, R., 1990. Conjugation of benzo(a)pyrene metabolites by freshwater green alga Selenastrum capricornutum. Chemico-Biological Interactions 74, 93e105. Yang, S., Wu, R.S.S., Kong, R.Y.C., 2002. Biodegradation and enzymatic responses in the marine diatom Skeletonema costatum upon exposure to 2,4-dichlorophenol. Aquatic Toxicology 59 (3e4), 191e200.