Complex toxicological interaction between ionic liquids and pesticides to Vibrio qinghaiensis sp.-Q67

Rui Qua, Shu-Shen Liu*ab, Fu Chenc and Kai Lia
aKey Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China. E-mail: ssliuhl@263.net; Tel: +86-021-65982767
bState Key Laboratory of Pollution Control and Resource Reuse, College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China
cCollege of Pharmaceutical Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China

Received 18th December 2015 , Accepted 14th February 2016

First published on 15th February 2016


Abstract

Ionic liquids (ILs) and pesticides may coexist in ecosystems, because more and more people try to extract pesticides from various samples using ILs. Many studies have indicated that the toxicities of ILs and pesticides are time-dependent. However, people know little about the time-dependent toxicity of the mixtures of ILs and pesticides. Hence, the toxicities of two pesticides, two ILs and 20 binary pesticide–IL mixture rays at seven exposure times, 0.25, 2, 4, 6, 8, 10 and 12 h, to Vibrio qinghaiensis sp.-Q67 were determined by time-dependent microplate toxicity analysis. The effect residual ratio (ERR) was used to quantitatively evaluate the toxicological interaction between pesticide and IL. Ten mixture rays exhibited synergism or antagonism at different exposure times. Toxicological interaction is mixture ratio-dependent and time-dependent. These findings suggest that mixtures of IL and pesticide pose a threat to the aquatic environment. People should pay more attention to the environmental effect of mixtures of IL and pesticide.


Introduction

The presence of pesticides in soils (lithosphere), surface water (hydrosphere) and rainwater (atmosphere) have been well documented.1–4 Pesticide contamination has become a worldwide problem, because they exhibit harmful effects on sensitive non-target organisms such as humans and wildlife populations.5 It was well known that the effect of a pesticide on a non-target organism depends not only on its concentration but also on the exposure time. For example, Zhu et al. found that aminotriazine has no short-term toxicity but has an obvious long-term toxicity.6 In order to improve risk assessments, we have to understand how the toxicity of pesticides changes with time.7

To effectively analyze the effects of pesticides on organisms, it is necessary to extract and concentrate pesticides from various environmental samples through various extractants such as ionic liquids (ILs).8–10 For example, Parrilla Vazquez et al.11 used a mixture of CH3OH and 1-octyl-3-methyl-imidazolium hexafluorophosphate to extract benzoylurea insecticides from wastewater. Zhang et al.12 used 1-butyl-3-methylimidazolium tetrafluoroborate ([bmim]BF4) to extract triazine herbicides in vegetable samples. Although ILs were considered green solvents due to their negligible vapor pressure and reduced inflammability,13 the toxicities of some ILs with long side-chain on aquatic organism cannot be ignored due to high toxicity to aquatic organism. In recent years, there were many reports on the toxicities of ILs.14–16 Not only that, we also found that some ILs have different concentration-response profiles (CRPs) at different times.17,18 For example, the CRPs of 1-ethyl-3-methylimidazolium chloride ([emim]Cl) and 1-butyl-3-methylimidazolium chloride ([bmim]Cl) on Vibrio qinghaiensis sp.-Q67 (V. qinghaiensis) are from monotonically increasing sigmoid-type curves to non-monotonic biphasic curves (see Fig. 1) when the exposure time is from 15 min to 12 h.17


image file: c5ra27096k-f1.tif
Fig. 1 Illustration of biphasic (J-shaped) concentration–response curve where Emin refers to the minimum effect or maximum stimulatory effect, ECmin to the concentration at the effect of Emin, a refers to the concentration at the effect of Emin/2 in the falling section (negative slope), b to the slope at the point (a, Emin/2), p to the median effective concentration, q to the slope at the point (p, 50), and ZEP is called as the zero effect point, i.e., the concentration at the effect of E = 0.

Hormesis (Fig. 1) having low-concentration stimulation and high-concentration inhibition19 is a very common phenomenon20,21 and contaminants always co-occur in ecosystems.22 Hence, it is worth understanding how compounds inducing hormesis interact with other compounds. Despite the increasing number of mixture toxicity researches about ionic liquids23,24 and many reports on the combined toxicities of pesticides,25,26 few people investigate the mixture toxicity of IL and another chemical. Zhang et al. found that the mixture of aldicarb and 1-benzyl-3-methylimidazolium tetrafluoroborate on the inhibition of bioluminescence of V. qinghaiensis exhibits antagonism, but they didn't study time-dependent combined toxicity of ionic liquid and pesticide.27

The aim of this paper is to examine what toxicological interaction will happen in the mixture of a IL and pesticide. Two pesticides, metalaxyl (MET) and simetryn (SIM),1,28–31 selected are widespread in water environment and two ILs, 1-ethyl-3-methylimidazolium chloride [emim]Cl and 1-ethyl-3-methylimida-zolium bromide ([emim]Br), not only are high water-soluble but also can induce hormesis.18 Considering that freshwater is closely related to people's daily lives and the pollutants in freshwater will directly (drinking and bathing) or indirectly (if water is used to irrigation, it is likely to contaminate soil and crops) affect human health, V. qinghaiensis, a freshwater bioluminescent bacterium, was selected as test organism. To investigate the effect of exposure time on combined toxicity, we used the time-dependent microplate toxicity analysis (t-MTA)17 to determine the toxicity and employed the effect residual ratio (ERR)32 method to evaluate the toxicological interaction at different effect levels.

Experimental

Test materials

Two ionic liquids, [emim]Br and [emim]Cl, were purchased from Acros (Belgium) and two pesticides, MET and SIM, from Dr Ehrenstorfer (Germany). All solutions were prepared with Milli-Q water and stored in darkness at 4 °C before test. Some physico-chemical properties and the concentrations of stock of the chemicals were listed in Table 1.
Table 1 Some physiochemical properties, CAS registration number and stock solutions of four chemicals
No. Chemicals Abbr. CAS RN M.W.a Purity (%) Stock (mol L−1)
a M.W.: molecular weight.
1 1-Ethyl-3-methylimidazolium bromide [emim]Br 65039-08-9 191.0 98.0% 2.24 × 10−1
2 1-Ethyl-3-methylimidazolium chloride [emim]Cl 65039-09-0 146.6 97.0% 2.82 × 10−1
3 Metalaxyl MET 57837-19-1 279.3 98.7% 7.16 × 10−3
4 Simetryn SIM 1014-70-6 213.3 97.5% 1.77 × 10−3


Four binary mixture systems, [emim]Br–MET, [emim]Cl–MET, [emim]Br–SIIM and [emim]Cl–SIIM, were constructed by one IL and one pesticide combination. For each mixture system, five rays (noted as R1, R2, R3, R4 and R5) were designed by the direct equipartition ray design (EquRay) procedure.33 The mixture ratios (pi,j),34 the ratio of the concentration of the jth component in the ith ray to the total concentration of the ray, of various components in 20 mixture rays and the concentrations of stocks were listed in Table 2.

Table 2 Concentration ratios (pi,j) of various components and the concentrations of stocks for twenty mixture rays
No. Mixture ray pi,j (i = 1,2,…,20; j = 1,2,3,4) (%) Concentration of stock (mol L−1)
[emim]Br [emim]Cl MET SIM
1 [emim]Br–MET-R1 98.00   2.00   4.93 × 10−2
2 [emim]Br–MET-R2 95.15   4.85   4.21 × 10−2
3 [emim]Br–MET-R3 90.74   9.26   3.43 × 10−2
4 [emim]Br–MET-R4 83.06   16.94   2.60 × 10−2
5 [emim]Br–MET-R5 66.22   33.78   1.69 × 10−2
6 [emim]Br–SIM-R1 99.21     0.79 4.51 × 10−2
7 [emim]Br–SIM-R2 98.04     1.96 3.50 × 10−2
8 [emim]Br–SIM-R3 96.16     3.84 2.57 × 10−2
9 [emim]Br–SIM-R4 92.60     7.40 1.72 × 10−2
10 [emim]Br–SIM-R5 83.35     16.65 9.19 × 10−3
11 [emim]Cl–MET-R1   98.03 1.97   6.01 × 10−2
12 [emim]Cl–MET-R2   95.22 4.78   4.95 × 10−2
13 [emim]Cl–MET-R3   90.87 9.13   3.90 × 10−2
14 [emim]Cl–MET-R4   83.27 16.73   2.84 × 10−2
15 [emim]Cl–MET-R5   66.57 33.43   1.78 × 10−2
16 [emim]Cl–SIM-R1   99.22   0.78 9.92 × 10−1
17 [emim]Cl–SIM-R2   98.07   1.93 9.81 × 10−1
18 [emim]Cl–SIM-R3   96.21   3.79 9.62 × 10−1
19 [emim]Cl–SIM-R4   92.70   7.30 9.27 × 10−1
20 [emim]Cl–SIM-R5   83.56   16.44 8.36 × 10−1


Test organism and culture

The freeze-dried V. qinghaiensis was purchased from Beijing Hamamatsu Corp., Ltd. (Beijing, China). Medium formula for V. qinghaiensis and the culture condition are the same as those in the literature.18

Time-dependent toxicity test

The toxicities of four chemicals and their 20 binary mixture rays to V. qinghaiensis were determined by the time-dependent microplate toxicity analysis (t-MTA).17 It should be indicated that the present paper is different from the report by Zhang et al.17 in two aspects. One is that the determination of the relative light unit (RLU) is on the Power-Ware microplate spectrophotometer (American BIO-TEK Company) at 22 ± 1 °C rather than the SpectraMax M5 (Molecular Devices Corp.) in the literature. The other one is that the set of time points is at 0.25, 2, 4, 6, 8, 10 and 12 h. Inhibition ratio of bioluminescence was used to characterize the toxicity, noted as E:
 
image file: c5ra27096k-t1.tif(1)
where I0 is the average RLU of V. qinghaiensis exposed to controls and I indicates the average RLU of V. qinghaiensis exposed to the treatment groups. The microplate toxicity test had to be repeated at least three times, each time did three duplicated microplate and each concentration is set three parallelisms in every microplate, to ensure the toxicity test precision.

Concentration–response curve fitting

For the monotonic concentration–response/toxicity curve (CRC), the concentration–toxicity data of a chemical or mixture ray were fitted to Logit or Weibull function.35 At the same time, the 95% observation-based confidence intervals (OCI) of CRC fitted were calculated.36

For the non-monotonic biphasic (like J-shaped) CRC, concentration–toxicity data were fitted to the five parameters logistic equation (eqn (2)).37 The physical meaning of five parameters in the logistic equation was illustrated in Fig. 1.

 
image file: c5ra27096k-t2.tif(2)

Toxicity interaction characterization

In this study, the ERR32 was used to quantify the toxicological interaction (synergism or antagonism) of mixture rays at various effect levels. Considering the OCI, the value of ERRx at a specific effect (x) can be computed as follows:
 
image file: c5ra27096k-t3.tif(3)
where ECI is the effect (toxic response) corresponding to the upper limit (when antagonism occurs) or lower limit (when synergism occurs) of the OCI, Eprd is the effect value predicted by an additive reference model such as concentration addition (CA) at the same concentration (ECx). When ERRx >, =, and < 0, say the mixture ray at the effect of x being synergism, additive action, and antagonism. CA was selected because it has gained large acceptance and has been proposed as reasonable default approach for regulatory purposes.38

Results and discussion

Difference in the time-dependent toxicity

The CRCs of two ILs are monotonic S-shaped at four exposure times, 0.25, 2, 4, 6 h, but non-monotonic J-shaped at the other two times of 8 and 12 h. Plots of five concentration parameters (EC10, EC50, EC70, ZEP and ECmin) and one effect parameter (Emin) describing CRC features vs. exposure times were shown in Fig. 2A and B. The EC10s of two ILs increase from 0.25 to 2 h and become stable after 4 h. The EC50 and EC70 of two ILs increase from 0.25 to 2 h, and decrease from 2 to 6 h, and then become stable after 6 h. The Emins of [emim]Cl and [emim]Br increase at the beginning and then decrease gradually, the maximum stimulation effect occurred at 10 h. The ZEPs and ECmins of two ILs remain unchanged from 8 to 12 h. The most appropriate model, values of parameters (EC10, EC50, EC70, ZEP ECmin, and Emin) were listed in the Table S1.
image file: c5ra27096k-f2.tif
Fig. 2 Plots of EC10 (image file: c5ra27096k-u1.tif), EC50 (image file: c5ra27096k-u2.tif), EC70 (image file: c5ra27096k-u3.tif), ZEP (image file: c5ra27096k-u4.tif), ECmin (image file: c5ra27096k-u5.tif), and Emin (image file: c5ra27096k-u6.tif) versus time for ionic liquids, [emim]Br (A) and [emim]Cl (B).

The CRCs of two pesticides are typical monotonic S-shaped at any exposure time and can be described by Weibull function. Plots of the pEC10, pEC50 and pEC70 of two pesticides vs. time were shown in Fig. 3A and B. For MET, the pEC10, pEC50 and pEC70 increase at beginning and are basically unchanged after 2 h. For SIM, pEC10, the pEC50 and pEC70 don't change over exposure times. The fitted CRC model, statistics, EC10, EC50 and EC70 at seven exposure times were listed in Table S2. The pEC50 of SIM changes over the time, which is consistent with results reported by Wang et al.39 In the present study, both ionic liquids induce hormesis at some exposure times, but the maximum stimulatory effects are different from the literatures. Zhang found that the maximum stimulation of [emim]Cl and [emim]Br at 12 h are 60.7%17 and 104%.18 Wang and we purchased freeze-dried V. qinghaiensis from the same producers, but Zhang purchased it from the other, this is probably the main reason for this results.


image file: c5ra27096k-f3.tif
Fig. 3 Plots of EC10 (image file: c5ra27096k-u7.tif), EC50 (image file: c5ra27096k-u8.tif), and EC70 (image file: c5ra27096k-u9.tif) versus time for pesticides MET (A) and SIM (B).

Five of 20 binary mixture rays exhibiting hormesis

The CRCs of five mixture rays in [emim]Br–MET, [emim]Cl–MET, [emim]Br–SIM and [emim]Cl–SIM systems were displayed in Fig. S2–S5, respectively. In the four mixture systems, the maximum stimulatory effect increases with the mixture ratio of IL. The R1 and R2 in [emim]Cl–MET system as well as R1 of [emim]Cl–SIM system exhibit hormesis at 12 h. The R1 and R2 in [emim]Br–SIM show hormesis at 10 and 12 h. The EC10, EC50, EC70, ZEP, ECmin and Emin of the mixture rays were displayed in Fig. S1.

In [emim]Br–MET systems, EC10 of R1, R2 and R3 increase from 0.25 to 12 h. EC10 of R4 and R5 are unchanged during the exposure times. EC50 and EC70 of R1 and R2 increase from 0.25 to 2 h, but those of R3, R4 and R5 decrease. EC50 and EC70 of R1, R2, R3 and R4 increase after 4 h, while R5 is unchanged after 2 h.

In [emim]Cl–MET systems, the tendency of EC50 and EC70 between 0.25 and 2 h are similar with [emim]Br–MET. After 2 h, EC50 and EC70 of five rays are stable. EC10 of R1, R2 and R3 ​increase from 0.25 to 12 h. EC10 of R4 and R5 are unchanged during the exposure times.

In [emim]Br–SIM systems, EC50 and EC70 of R1, R2, R3 and R4 decrease after 4 h, while R5 are relatively constant after 4 h. The EC10 of R1 and R2 increase from 0.25 to 12 h, but the EC10 of R3, R4 and R5 are constant. The ZEP and ECmin of R1 and R2 are constant. The Emin of R1 and R2 both increase over time.

In [emim]Cl–SIM systems, the EC10 of R1, R2 and R3 increase from 0.25 to 12 h. EC10 of R4 and R5 are relatively constant. The EC50 and EC70 of five mixtures rays remain relatively unchange except at 2 h.

Toxicological interaction between pesticide and ionic liquid

Toxicological interactions of all mixture rays at various inhibitory effects are identified by using CA. For [emim]Br–SIM and [emim]Cl–SIM systems, the combined toxicities of all rays at different effect levels and different times are additive, i.e., toxicological interaction has no mixture ratio-, concentration- and time-dependence. However, there are complex toxicological interactions in the other two mixture systems, [emim]Br–MET and [emim]Cl–MET. The values of ERR describing quantitatively interaction were listed in Table 3.
Table 3 Effect residual ratios of different effect levels of [emim]Br–MET and [emim]Cl–MET mixture rays at seven exposure timesa
Ray Effect (%) [emim]Br–MET [emim]Cl–MET
0.25 h 2 h 4 h 6 h 8 h 10 h 12 h 0.25 h 2 h 4 h 6 h 8 h 10 h 12 h
a —: there is no significant deviation between CA prediction and observation.
R1 10
20
30 8.28 9.86
40 29.79 24.13 8.16
50 37.30 8.29 27.24 2.44 14.65
60 37.15 17.57 24.00 3.04 2.05 7.84 19.82 6.03
70 33.23 26.24 6.40 18.87 6.38 2.92 11.15 18.52 8.03
80 24.89 28.65 12.13 11.20 5.96 2.57 9.20 16.49 11.82
R2 10 −89.77
20 −59.09
30 10.71 14.58
40 22.92 25.62    
50 26.35 5.94 28.74 2.90   1.94
60 23.90 10.54 26.43 6.92   4.84
70 18.13 21.03 0.82 21.83 8.92 2.90 6.25 2.89
80 8.62 22.14 5.24 14.28 7.82 3.31 5.30 0.03
R3 10 −91.99
20 −69.87 −67.39
30   −53.30 −52.08  
40 16.57 −40.29 7.81
50 26.58 −31.06 11.98
60 30.56 3.22 13.36
70 31.04 8.84 12.83 3.09
80 26.60 12.45 11.06 5.06
R4 10 −99.93 −95.08 −94.08 −68.94 −68.94
20 −73.49 −70.17 −68.60 −57.76 −47.92 −47.92
30 −44.28 −58.67 −56.83 −55.19 −44.99 −37.08 −37.08
40 −35.00 −47.47 −46.71 −45.72 −35.84 −29.74 −29.74
50 4.18 −38.71 −38.73 −37.75 −28.55 −23.77 −23.77
60 9.79 −31.29 −31.73 −31.11 −21.91 −18.63 −18.63
70 13.25 −25.47 −25.29 −14.24 −14.24
80 14.72 2.41
R5 10 −62.59
20 −47.09
30 −44.24 −39.36
40 −29.33 −37.84 −35.48 −33.67 −33.52 −33.52 −33.28 −26.21 −26.21
50 −25.97 −33.04 −31.95 −30.18 −29.13 −29.42 −29.79 −24.51 −24.51
60 −23.04 −29.02 −28.63 −26.91 −23.56 −25.93 −26.62 −22.71 −22.71
70 −19.94 −24.90 −25.11 −23.75 −19.65 −22.41 −23.09 −20.29 −20.29
80 −16.38 −20.33 −20.94 −19.93 −14.89 −18.49 −19.02 −17.09 −17.09


For the [emim]Br–MET systems, the ERR values of five mixture rays at the effect of 50% are positive (synergism) in the beginning and then decrease gradually and change sign as negative values (antagonism). For example, the ERR of R1 at the effect of 50% decreases gradually from 37.30 to 8.29 during 2 to 4 h and changes into zero (6–12 h). The ERR of R2 at the effect of 50% decreases from 26.35 to 5.94 (2–4 h) and changes into zero (6–12 h). The ERR of R5 at the effect of 50% is zero from 0.25 to 4 h and changes into negative (6–12 h).

In [emim]Cl–MET systems, the ERR of R1 is positive (2–12 h) except at 0.25 h. The ERR of R5 is negative at 0.25 h, and changes into zero (2–4 h), and negative (6–12 h). The ERRs of R1 and R2 are positive at most of the exposure times. The ERR of R3 is positive (2–4 h) and there is no deviation at other exposure times. The ERR of R4 is positive at 2 h and turns to negative (8–12 h).

Complex toxicological interaction was identified for [emim]Br–MET and [emim]Cl–MET at different exposure times. Toxicological interaction in the [emim]Br–MET and [emim]Cl–MET mixture system changed with the mixture ratios. For example, according to EC50, the R3 and R4 of [emim]Br–MET showed antagonism but R1 and R2 showed additive action at 12 h. A number of studies have proved that40,41 mixture ratio is an important factor to determine interaction.

Dilipkumar and Chuah42 indicated that the ratio of allelopathic crop water extracts in combination with herbicide is an important factor in influencing the potency of phytotoxic activity. Some people43 found that antagonism was larger for mixtures with higher proportions of mecoprop when they studied combined toxicity of mecoprop and terbuthylazine to Lemna minor. It should be pointed out that CA just predict the effective concentrations at the effects of greater than zero in this paper, because CA predictions are restricted to that the compounds also share an identical range of effects (the same minimum and maximum effect).44 We need further research to understand how to predict the hormesis effect of the mixture.

Toxicological interaction in the [emim]Br–MET and [emim]Cl–MET mixture system also changed over the exposure times. The results indicated that just examining concentration effect relationship of compounds is not enough, we need to understand the time-dependent toxicity if want to optimize risk assessments.45 Inhibition of bioluminescence in the V. qinghaiensis of the two ionic liquids, two pesticides and their mixtures changed over times. Organisms grow during the test could affect dilution and surface area to volume ratio, so that alter the toxicokinetics.46 Literatures47 indicated that even the organisms exposure to a binary mixture with stable concentration, the internal concentration usually change with time.

Conclusions

We determined time-dependent toxicities of two ILs and two pesticides, and their binary mixture rays to V. qinghaiensis. Both ILs induced hormesis at different exposure times but pesticides cannot provoke hormesis. Complex toxicological interaction of IL and pesticide at different exposure time was identified by using CA. The results indicated that the mixture of IL and pesticide are a potential threat to the environment. Using the ionic liquids to extract pesticides should be considered the ecological effects.

Acknowledgements

We are thankful to the National Natural Science Foundation of China (21177097, 21377097) and Specialized Research Fund for the Doctoral Program of Higher Education (20120072110052) for their financial support.

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Footnote

Electronic supplementary information (ESI) available. See DOI: 10.1039/c5ra27096k

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