Environmental Pollution 192 (2014) 147e153
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Sorption kinetics and equilibrium of the herbicide diuron to carbon nanotubes or soot in absence and presence of algae Fabienne Schwab a, b, Louise Camenzuli b, Katja Knauer c, Bernd Nowack a, Arnaud Magrez d, Laura Sigg e, Thomas D. Bucheli b, * a
Empa e Swiss Federal Laboratories for Materials Science and Technology, CH-9014 St. Gallen, Switzerland Agroscope, Institute for Sustainability Sciences ISS, CH-8046 Zurich, Switzerland Federal Office for Agriculture FOAG, CH-3003 Bern, Switzerland d EPFL e Ecole Polytechnique F ed erale de Lausanne, CH-1015 Lausanne, Switzerland e Eawag, Swiss Federal Institute of Aquatic Science and Technology, CH-8600 Duebendorf, Switzerland b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 February 2014 Received in revised form 12 May 2014 Accepted 26 May 2014 Available online xxx
Carbon nanotubes (CNT) are strong sorbents for organic micropollutants, but changing environmental conditions may alter the distribution and bioavailability of the sorbed substances. Therefore, we investigated the effect of green algae (Chlorella vulgaris) on sorption of a model pollutant (diuron, synonyms: 3-(3,4-Dichlorophenyl)-1,1-dimethylurea, DCMU) to CNT (multi-walled purified, industrial grade, pristine, and oxidized; reference material: Diesel soot). In absence of algae, diuron sorption to CNT was fast, strong, and nonlinear (Freundlich coefficients: 105.79e106.24 mg/kgCNT$(mg/L)n and 0.62e0.70 for KF and n, respectively). Adding algae to equilibrated diuron-CNT mixtures led to 15e20% (median) diuron redissolution. The relatively high amorphous carbon content slowed down ad-/desorption to/from the high energy sorption sites for both industrial grade CNT and soot. The results suggest that diuron binds readily, but e particularly in presence of algae e partially reversibly to CNT, which is of relevance for environmental exposure and risk assessment. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Bioavailability Sorption kinetics Black carbon Engineered nanomaterials Nanoparticles
1. Introduction Carbon nanotubes (CNT), a nano-scaled allotrope of carbon, can strongly sorb organic pollutants (OP) with a similar or higher affinity than other carbonaceous sorbents, depending on their high specific surface area (SSA), and their large delocalized electron systems (Pan and Xing, 2010b). Once released in the environment (Hendren et al., 2011), CNT may therefore change the fate and bioavailability of OP (Hofmann and von der Kammer, 2009; Pan and Xing, 2010b). Numerous different sorption mechanisms are discussed to explain and predict the fate of chemicals in the presence of CNT in equilibrium (Chen et al., 2011, 2008; Pan and Xing, 2008, 2010b; Wang et al., 2010, 2009; Wu et al., 2013). Less attention has been given to the kinetics of ad-, ab-, and desorption of OP on/from CNT, which is important to understand the release of OP from CNT as a secondary water contamination source. Initial studies suggest that
* Corresponding author. E-mail address: [email protected] (T.D. Bucheli). http://dx.doi.org/10.1016/j.envpol.2014.05.018 0269-7491/© 2014 Elsevier Ltd. All rights reserved.
many OP reversibly sorb to CNT on a time scale of hours (Chen et al., 2011, 2009; Oleszczuk et al., 2009; Pan and Xing, 2010a; Zhang et al., 2012). However, some pharmaceuticals' (Oleszczuk et al., 2009) and other OP's (Wu et al., 2013) sorption equilibrium to CNT was reached after 5 days only. It is currently not entirely clear why OP sorb that much slower to certain CNT than to others. One of the first studies on desorption of OP from CNT was performed by Oleszczuk et al. who showed that desorption kinetics of oxytetracycline and carbamazepine from CNT followed a twophase first order model consisting of a rapid and a slow desorbing fraction (Oleszczuk et al., 2009). Slightly slower desorption than sorption, and sorption hysteresis is proposed to be explainable by rearrangement of the CNT bundles, pore condensation, or the exothermic adsorption of OP to CNT (Pan and Xing, 2008). A more recent study suggested irreversible chemical reactions of the sorbate with carboxylic functional groups of the sorbent (Wu et al., 2013). Little is known about sorption in more complex, environmentally relevant setups, e.g. sorption in presence of natural organic matter (NOM) (Pan et al., 2013), or sorption in presence of organisms (Xia et al., 2010). Competitively sorbed NOM (Shi et al., 2010;
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Zuttel et al., 2002), or surface oxidation (Pan and Xing, 2010b; Wang et al., 2010), may strongly reduce the CNT sorption capacity, especially for aromatic or planar OP (Shi et al., 2010; Wang et al., 2010, 2009; Zhang et al., 2011). Then again, the presence of NOM may increase OP sorption to CNT, because it may enhance dispersion of the CNT, and thus increase the available CNT surface area (Pan et al., 2013). We found just one study which investigated the influence of organisms on sorption. Xia et al. suggested that the presence of Agrobacterium probably promoted desorption of phenanthrene from CNT in soil, or that the bacterium utilized sorbed phenanthrene (Xia et al., 2010). It is unclear what led to the increased availability of the OP, and if phenanthrene desorbed before it became bioavailable. Because algae are the major primary producers in aqueous environments, it is of particular interest how OP sorption to CNT is affected by them. Again, there is no information available on such interactions. Any biological activity in aqueous sorption experiments is usually suppressed by adding a biocide such as NaN3 (Shi et al., 2010). Information on the influence of organisms on OP sorption to CNT is needed to assess, for instance, the safety of applications aiming at removing OP from water by CNT. Generally, in view of the constantly growing CNT production volumes (Hendren et al., 2011), it would be useful to know the environmental exposure of micropollutants sorbed to CNT. Hence, the overall aim of our study was to systematically quantify the sorption processes in a pollutant-CNT-biota model system, and to test the hypothesis that algae may attenuate sorption similar to NOM. Experiments were performed with the widely used herbicide diuron (Cornelissen et al., 2005; Knauer et al., 2007), different types of CNT, soot as a reference sorbent, and the freshwater green alga Chlorella vulgaris. The specific goals were to a) quantify sorption thermodynamics and kinetics of diuron and CNT, b) quantify the impact of algae on the ongoing sorption processes in the pollutant-CNT-biota system, and c) compare the sorption of industrial, purified, oxidized and pristine CNT and the reference sorbent Diesel soot. Further, this paper aimed at providing mechanistic explanation for diuron sorption in a companion study showing enhanced toxicity of the herbicide in presence of CNT (Schwab et al., 2013). 2. Experimental section 2.1. Chemicals 3-(3,4-Dichlorophenyl)-1,1-dimethylurea (diuron, DCMU) and 3-(3,4dichlorophenyl)-1,1-dimethyl(D6)urea (D6-diuron), both >99% pure, were purchased from Labor Dr. Ehrenstorfer (Germany). For structures, see Table S1. Acetonitrile (99.99%) was obtained from SCHARLAU CHEMIE S.A. (Spain). All other chemicals were per analysis grade and obtained from Merck or SigmaeAldrich, Switzerland. Ultra-pure water (Milli-Q) was produced by a gradient A10 water purification system from Millipore (Volketswil, Switzerland). Nitrogen (99.99995%) was obtained from PanGas (Dagmarsellen, Switzerland).
2.2. Carbonaceous nanoparticles Purified pristine and oxidized CNT (ppCNT and poxCNT) were synthesized by catalytic chemical vapor deposition by EPFL Lausanne, Switzerland. Industrial pristine CNT (ipCNT) of similar size and shape were purchased from Cheap Tubes Inc., Brattleboro, VT 05301, USA. The average CNT diameter as determined by transmission electron microscopy ranged between 8 and 15 nm, and the length as determined by scanning electron microscopy between 0.5 and 2.0 mm. As native black carbon reference sorbent, a forklift Diesel soot standard (soot) with spherical primary particles in the range of 35 nm (Gustafsson et al., 2001) was used (Standard Reference Material 2975, National Institute of Standards and Technology, USA). Transmission electron microscopy images and detailed characterization data for all materials, and synthesis details are given in Fig. S1, Table S2, and in Schwab et al. (2011). The sorbent suspensions were prepared in 2-[4-(2-hydroxyethyl)piperazin-1-yl]ethanesulfonic acid (HEPES) buffered OECD algal test medium (OECD, 2006) 1.00 mM, pH 7.0 ± 0.3. Further details are provided in the supporting information (SI, sections “Preparation of Sorbent Suspensions”, and “Notes on the Sterile Preparation of the Particle Suspensions”).
2.3. Green algae cultivation Chlorella vulgaris, strain 211-11b (Culture Collection of Algae, SAG, University of €ttingen, Germany), was cultivated in the OECD algal test medium (OECD, 2006). In Go short, axenic cultures grew at 24 ± 0.5 C, 100 rpm, an illumination of 80 ± 15 mEm2 s1 (daylight lamps, Sylvania Gro-Lux F15W/Gro T8, Infors, Switzerland), and under a light:dark regime of 16:8 h. Algae used for tests were harvested in the exponential growth phase, and the cell density was counted using a haemocytometer chamber. More details on the incubation conditions are available elsewhere (OECD, 2006; Schwab et al., 2011). 2.4. CNT and soot suspensions The used CNT and soot in the standardized suspensions and their detailed behavior in the algal medium were characterized as described previously (Schwab et al., 2013, 2011). The polydispersity of the CNT suspensions was monitored using dynamic light scattering (DLS) in a range of 1e10 000 nm (Zetasizer Nano ZS, Malvern, UK) at the same experimental conditions as used for the ternary sorption experiments. Three replicates per treatment were measured. Finally, sorbent-algae suspensions were examined microscopically. For more details see SI, section “Dry and Suspended CNT Characterization.” 2.5. Binary sorption experiments All sorption isotherms with CNT or soot and diuron were obtained using a batch equilibration technique at 24 ± 2 C. Screw cap glass vials (22 mL) were used. To each vial, well homogenized sorbent stock suspension was added and diluted with algal growth medium to obtain, after addition of the diuron stock solution, a final nominal concentration of 10.0 mgCNT/L and 5.00 mgsoot/L, respectively. The exact sorbent concentration in the stock suspensions was calculated in each experiment from the weighed in mass of CNT or soot. Nine to ten different initial diuron concentrations in a range of 0.73e2994 mg/L were prepared by spiking different volumes of a diuron working stock solution to the CNT suspensions. The concentration range covered more than three orders of magnitude to account for the expected nonlinear sorption behavior of CNT. All concentrations were tested at least in duplicates, and control treatments at least in triplicates. We reduced the replicate number to two, for the sake of a higher number of tested concentrations. These test suspensions were prepared sterilely without biocide, despite of the increase of variability of the data this inflicts, to avoid killing the algae in the subsequent ternary sorption experiments (details in section “Notes to the sterile preparation of the particle suspensions” in the SI). Finally, the vials containing the sorbent-diuron mixture were sealed with polytetrafluoroethylene (PTFE) lined screw caps, additionally covered with Parafilm®, wrapped in aluminum foil and then pre-equilibrated on an orbital laboratory shaker. The mixtures were kept for 20 h at 175 rpm (to keep the sorbents in full suspension; see OECD, 2000) in the dark at 24 ± 2 C, and under equal conditions for 28 d to study sorption of diuron under non-equilibrium and equilibrium conditions, respectively. 2.6. Ternary sorption experiments To examine the change of sorption after perturbation of the system by living green algae, 7e37 104 cells/mL of C. vulgaris were added to 20 h-, or 28 d-kept diuron-CNT mixtures (equilibration conditions alike the binary sorption experiments). The added algae culture volume was controlled to change the total volume in the vials by 1.8%. For incubation, all vials were placed vertically inside of an illuminated sterile bench (15 ± 5 mEm2 s1) at room temperature to prevent contamination of the samples and to provide light for the algae. These conditions were chosen to keep the viability (photosynthetic activity) of the green algae constant in the control treatments (Schwab et al., 2013). After incubation the diuronCNT mixtures with green algae, the subsequent changes of the diuron concentration were measured after 3, 6, 15, and 24 h (sampling and quantification described in section “Diuron Analysis”). The robustness of this setup was verified by repeating some ternary sorption experiments under different incubation conditions (in 50.0 mL Erlenmeyer flasks at 100 rpm and 80 ± 15 mEm2 s1). 2.7. Sorption isotherms Sorbed diuron for both binary and ternary sorption experiments was calculated by mass balance using the initial and final quantified aqueous diuron concentrations (see section “Diuron Analysis”). The algae-affected “sorption isotherms” are denoted in this study by the term “perturbed isotherms”, where the perturbation was the incubation with C. vulgaris. Five common isotherm models were evaluated for fit to the data (Pikaar et al., 2006; Xia and Ball, 2000). All details on the modeling are provided in the SI, Table S5, sections “Modeling of (Perturbed) Sorption Isotherms”, “Details on the Different Sorption Models”, and “Details on the Goodness of the Fit of the Different Sorption Models”. Details on calculation of the fraction of additionally sorbed or re-dissolved diuron are provided in the SI. 2.8. Adsorption kinetics Batch adsorption experiments (50.0 mL per replicate) were performed in 50 mL screw-capped glass vials. Pristine purified CNT, ipCNT, and soot were tested (poxCNT
F. Schwab et al. / Environmental Pollution 192 (2014) 147e153
1.2E+07
A
purified pristine CNT industrial pristine CNT
1.0E+07 8.0E+06
cs (μg/kgCNT )
behaved in pre-trials identically to ppCNT). In each vial, sorbent stock suspension, algal growth medium, and diuron were combined to result in final concentrations of 10 mgCNT/L (ppCNT and ipCNT), 5.0 mgsoot/L, and 100 mg/L diuron. After addition of diuron, all vessels were immediately sealed and shaken on an orbital laboratory shaker at 24 ± 2 C in the dark. The dissolved diuron concentration was measured in these batches for the first time one min after the addition of diuron, and repeatedly thereafter until all sorbent-diuron mixtures had reached equilibrium. All time points were measured at least in duplicates. Selected time points were re-measured in a second repetition of the experiment to assure the reproducibility of the results. The kinetics of sorption was modeled using the empirical pseudo-second order model (PSOM, Equations S1eS3), and by the empirical pseudo-first order model (PFOM, Oleszczuk et al., 2009; Pan and Xing, 2010a; Zhang et al., 2012). Details on the fitting of the sorption kinetics are provided in the SI.
149
6.0E+06 4.0E+06
2.9. Desorption kinetics
2.0E+06 0.0E-01 0
Diuron concentrations of both the binary and ternary sorption experiments, as well as the kinetics trials, were measured by high performance liquid chromatography coupled with a tandem mass spectrometer (HPLC-MSMS). For this, 2 mL aliquots of each replicate of the solute-sorbent(-algae) mixtures were filtered to remove the CNT and/or algae through a 0.4 mm PTFE syringe filter (Millipore, Switzerland). The filtrate was spiked with deuterated internal diuron standard (D6diuron, sample storage conditions: 4 C, darkness, ipCNT > soot could be explained by the different accessibility of adsorption sites (e.g. aromatic sheets) for diuron. The amorphous carbon covering the aromatic sheets of the low purity ipCNT and soot (Table S2) may have limited fast diffusion of diuron to these sites. In agreement with that, the sorption kinetics of diuron to ipCNT was ~7 times slower than that of biphenyl and phenanthrene to CNT in Zhang et al. (2012), and also slower than the one of atrazine to CNT (Chen et al., 2009). Moreover, the sorption kinetics of diuron to the high purity ppCNT was comparable to the values found in the literature for CNT of similar purity (Deng et al., 2012). The fitted PSOM equilibrium sorption capacities cs,t¼∞ of 3.3 [2.3, 4.3]95% g/kgsoot, 4.5 [4.2, 4.7]95% g/kgCNT for ppCNT, and 9.4 [9.0, 9.8]95% g/kgCNT for ipCNT correlated highly (Pearson correlation coefficient of 0.9996, p < 0.018) with the SSA of these materials (Table S2), and were comparable when normalized to this parameter (36.4 mg/m2soot, 30.5 mg/m2CNT for ppCNT, and 21.4 mg/m2CNT for ipCNT). This finding points again to a sorption mechanism that is mainly dependent on the surface of the materials (see above). The obtained sorption capacities for CNT were comparable to recent findings for biphenyl and phenanthrene sorbed to multi-walled CNT (Zhang et al., 2012).
8.0 log cs (μg/kgsorbent)
7.0 6.5 6.0 5.5 5.0 4.5 4.0
-1
0
1
2
3
2
3
log c w (μg/L)
3.0 log (cs/SSA) (μg/msorbent2)
2.5
3.2. Sorption in absence of algae The estimated Freundlich parameters for diuron and all four materials equilibrated for 28 d are presented in Table 1 (results for 20 h in SI, Table S7 and Fig. S4, detailed discussion of the modeling in SI). The Freundlich constant KF of soot was with 104.55±0.13 mg/ kgsoot$(mg/L)n (average±95% confidence interval) comparable to the KF from Sobek et al. for diuron sorption to soot (104.33±0.04 mg/ kgsoot$(mg/L)n) measured in half cell systems (Sobek et al., 2009). The small difference of 5% between the two KF demonstrates that the present experimental setup produced reproducible results. The ipCNT sorbed diuron ~0.5 orders of magnitude stronger (KF ¼ 106.24±0.10 mg/kgCNT$(mg/L)n) than ppCNT (KF ¼ 105.84±0.15 mg/
A
7.5
B
2.0 1.5 1.0 0.5 0.0 -0.5 -1.0
-1
0
1
log c w (μg/L) Fig. 2. Selected sorption isotherms of the herbicide diuron to purified pristine carbon nanotubes (CNT, C), purified oxidized CNT (B), industrial pristine CNT ( ), and the reference sorbent soot ( ) with Freundlich fits (for fitting parameters, see Table 1), normalized to sorbent mass (A), and specific surface area (SSA, B). All sorbentesorbate mixtures were equilibrated for 28 d without addition of biocide. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Table 1 Freundlich fitting parameters (log KF: Freundlich sorption coefficient, n: nonlinearity constant) for all non-perturbed isotherms (i.e. before addition of algae, highlighted with 2 bold letters) and for all perturbed isotherms (3, 6, 15, and 24 h incubation with algae). As a measure of the goodness of the fit, the adjusted correlation coefficient Radj is shown. All sorbentesorbate mixtures were equilibrated for 28 d. log KF (mg/kgsorbent$(mg/L)n) Av Purified pristine CNT
Purified oxidized CNT
Industrial pristine CNT
Soot
Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae
5.84 5.79 5.72 5.69 5.76 5.84 5.72 5.51 5.57 5.62 6.24 6.28 6.30 6.25 6.28 4.55 4.18 4.32 4.34 4.33
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
R2adj
n ()
95% conf. int.
Rel. error (%)
Av
0.15 0.13 0.18 0.11 0.21 0.14 0.15 0.28 0.15 0.23 0.10 0.11 0.09 0.08 0.09 0.13 0.16 0.23 0.25 0.17
1.3 1.1 1.5 0.9 1.7 1.2 1.3 2.5 1.2 2.0 0.7 0.9 0.7 0.6 0.7 1.3 1.9 2.6 2.7 1.9
0.62 0.65 0.65 0.66 0.61 0.67 0.68 0.80 0.69 0.70 0.64 0.59 0.59 0.62 0.59 0.97 1.10 1.03 0.99 1.02
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
95% conf. int.
Rel. error (%)
0.11 0.09 0.12 0.07 0.13 0.10 0.10 0.19 0.09 0.15 0.06 0.07 0.06 0.05 0.06 0.08 0.09 0.14 0.14 0.10
8.5 6.5 9.2 5.0 10.4 7.1 6.9 11.4 6.1 10.4 4.7 5.6 4.6 4.2 4.7 3.7 3.9 6.3 6.6 4.5
0.820 0.919 0.796 0.960 0.780 0.863 0.905 0.725 0.933 0.794 0.956 0.941 0.957 0.963 0.956 0.973 0.975 0.925 0.934 0.965
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Fig. 3. Re-dissolved diuron (medians and non-outlier range) after different incubation times of algae with 28 d pre-equilibrated diuron-sorbent mixtures, and the four sorbents under investigation. Nonparametric comparison of multiple independent groups (KruskaleWallis one-way analysis of variances, N ¼ 84e99), p ¼ 0.0002e0.04 for 15 h, p ¼ 0.000002e0.02 for 24 h. *: Significantly higher than one group. **: Significantly higher than two groups. Reading example: After 15 h, the redissolved diuron of purified pristine CNT is significantly higher than after 3 h and 6 h (i.e., two groups). Absolute concentration changes provided in Fig. S6.
kgCNT$(mg/L)n) and poxCNT (KF ¼ 105.84±0.14 mg/kgCNT$(mg/L)n). The ppCNT and poxCNT again sorbed diuron >1 order of magnitude stronger than soot. The oxidation of poxCNT did, as in the kinetics experiments, not affect the sorption strength significantly: Both ppCNT and poxCNT exhibited similar KF and n. The sorption was for both CNT rather nonlinear (ppCNT: n ¼ 0.62 ± 0.11, poxCNT: n ¼ 0.67 ± 0.10) as compared to soot (n ¼ 0.97 ± 0.08). The different KF of purified and ipCNT were most importantly, likely mainly a result of the different SSA of the sorbents, and not by different sorption mechanisms. This interpretation is further supported by a plot of the sorption isotherms normalized by the SSA (Fig. 2B), in which all isotherms of CNT collapse on one non-significantly different isotherm. Hydrogen bonding and Lewis acid-base based sorption mechanisms due to the carboxylic groups seem thus rather unlikely. Electrostatic interactions are also not expected to occur, because diuron is neutrally charged at pH 7.00. Therefore, it seems most probable that diuron bound to the CNT via pep stacking on the highly condensed aromatic sheet regions, present both in CNT and soot. This binding mechanism is supported by the fact that diuron is a rather polar molecule (dipole moment is 7.55 Debye, (Chen et al., 2011). After surface saturation of the CNT, lower-energy sorption sites for the neutrally charged diuron such as defects in the aromatic sheets, interstitial and groove regions between CNT bundles, and residual amorphous carbon may be occupied, resulting in the observed nonlinear sorption (Figs. 2 and S4, Pan and Xing, 2008, 2010b; Pikaar et al., 2006). Likewise, the lower sorption of diuron to soot as compared to the CNT could be explained by the lower SSA of soot, the high content of oxygen (Table S2) on the soot surface, and attenuation of diuron sorption due to the amorphous carbon covering the CNT
surfaces, similar to the attenuation of the sorption by NOM (Shi et al., 2010; Wang et al., 2010, 2009; Zhang et al., 2011). This explanation is supported by the finding of Knauer et al. (2007) who found for combusted (i.e. amorphous carbon free) soot a very high KF of 105.7 mg/kgsoot$(mg/L)n. This KF is comparable to those of ppCNT and poxCNT (Table 1), suggesting that the condensed carbon sheets of combusted soot, once accessible, bind diuron in a similar way as the aromatic sheets of CNT. 3.3. Microscopic investigations of algae-CNT suspensions Brightfield microscopy revealed that the majority of algal cells attached to CNT agglomerates (Table S3, Fig. S5B). Mixing of the suspensions enhanced this agglomeration. In agreement with previous work (Schwab et al., 2013), and the results presented above, both the ppCNT and poxCNT heavily agglomerated with algae (Fig. S5B). The ipCNT were better dispersed, but still formed agglomerates >100 mm with algae. In contrast, soot and algae rarely attached to each other (max. diameter of agglomerates ~15 mm). No morphological changes of the cells exposed to any of the tested particles were observed, in agreement with previous studies (Schwab et al., 2011; Wei et al., 2010). 3.4. Sorption equilibrium change in presence of algae and evolution with time After 24 h of incubation of algae and the 28 d-equilibrated diuron-CNT mixtures, medians 15e20% (non-outlier range up to 40% maximum change) of the sorbed diuron re-dissolved from the ppCNT and poxCNT (Fig. 3). Re-dissolution occurred only in
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presence of algae, as shown in equally treated control experiments with equilibrated diuron-CNT mixtures without algae (see section “No Effect of Algal Exudates”). Given that algal cells intensively agglomerated with CNT, even if very low CNT concentrations were present in suspension, we conclude that the attachment of algae to CNT led to more competition for sorption sites, similar as observed for humic acid and CNT (Wang et al., 2009). As a consequence, diuron re-dissolved. Exudates clearly did not affect the sorption (see section below). Evidence for re-dissolution due to addition of algae is also provided by increased diuron algal toxicity caused by locally elevated diuron concentrations (Schwab et al., 2013). This explanation is supported by the microscopic investigations mentioned above, which showed that ppCNT and poxCNT agglomerated most extensively with algal cells, leading to highly competitive sorption, and therefore more diuron release than in ipCNT and soot. The variability for soot was again higher due to the lower absolute soot concentration, but the trends in Fig. 3 point to minimal diuron re-dissolution, presumably because algae did not attach to soot. Again, the ppCNT and poxCNT behaved similarly, suggesting little effect of the oxygen functional groups. The ipCNT behaved similar to soot: both did not lead to significant amounts of re-dissolved diuron. More details on the temporal change of the sorption equilibrium after addition of algae are given in the SI (Table S7, Figs. S7, S8, chapter “Change of KF with time”). 3.5. No effect of algal exudates Diuron uptake/sorption by algae, or by algal exudates, was found in the control experiments (SI, section “Quality Assurance”) to be negligible, presumably, due to the more than two orders of magnitude stronger sorption of diuron to CNT than to algae/exudates, the relative short incubation of the mixture with algae (24 h), and the >11 times lower concentration of algae/exudates than CNT/ soot. A worst-case calculation of the maximal percentage of diuron sorbed by algal exudates resulted in a maximal concentration of 0.13% only (assuming the algae produced their own weight in exudates, and assuming a worst-case log(KOC) for diuron of 3.5 (Schwarzenbach et al., 2003)). This calculation also shows that increasing the algal biomass by a factor of 10e1000, as it is possible during massive algal blooms, would elevate the maximal percentage of diuron sorbed by exudates to 1.2e55.7%. Results at such high algal densities are more difficult to interpret, because at densities of several million cells/mL, the algae start to inhibit their own growth. 3.6. Desorption kinetics in absence of algae Diuron desorption occurred within ~4 h (Fig. 4A). The obtained data fitted well to the two-phase desorption kinetics model (Equation S7). A fraction of 39.6 ± 1.5% (Frapid, ±standard error) of the diuron rapidly desorbed from the ppCNT, and Fslow was consequently 60.4 ± 1.5%. This implies that, if equilibrium conditions change, for example, if a solid phase extraction cartridge leaches CNT, or a CNT-containing effluent gets diluted, a considerable fraction of diuron sorbed to CNT may again be released to the aqueous environment on a relevant time scale. However, it should be noted that in the present desorption kinetics experimental setup, the used CNT were saturated with diuron. The observed 39.6 ± 1.5% is therefore the maximal expectable rapid desorbing fraction of diuron sorbed to CNT. Under environmental conditions as in the above shown ternary sorption experiments, CNT are not saturated with diuron and smaller fractions of diuron therefore release. The rate constants krapid and kslow were 0.66 ± 0.07 h1, and 0.002 ± 0.002 h1, respectively, revealing that compared to the k2* of the sorption kinetics (see above), the desorption process of diuron from CNT was slower. Compared to literature data, the
Fig. 4. Fraction of desorbed diuron from purified pristine carbon nanotubes (ppCNT) as a function of time. Fits: Two-phase desorption kinetics model. A: Desorption from CNT alone (C), pooled data from two independent experiments. B: Desorption from CNT in presence of algae added before the first desorption step ( ), or added once before one of the desorption steps 2e8 (A). For further details, see text. Note that the match of the solid line in B with some of the symbols is coincidence. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
desorption kinetics of diuron from CNT is still ~4e15 times faster than e.g. the desorption of carbamazepine and oxytetracycline from similar CNT (Oleszczuk et al., 2009). The observed desorption hysteresis is in accordance with results of other studies for compounds of similar structure, polarity or size (Oleszczuk et al., 2009; Pyrzynska et al., 2007). 3.7. Desorption kinetics in presence of algae In Fig. 4B, the desorption kinetics of diuron from CNT after addition of algae before the first desorption step, and added once at a given desorption step (2e8) is shown. The diuron desorption kinetics in presence of algae was almost identical to the one in absence of algae (krapid ¼ 0.7 ± 0.2 h1, kslow ¼ 0.002 ± 0.004 h1). With 41 ± 4% (mean ± standard error), the fraction of rapidly desorbing diuron was also not significantly different from the fraction of diuron desorbed in absence of algae. This shows that under non-equilibrium conditions, the effect of the presence of algae was overridden by the tendency of the system to re-establish sorption equilibrium. The standard error was slightly higher, mainly due to a replicate sample in which >60% diuron desorbed (Fig. 4B). Outlier tests and repeated measurements of this sample showed that it could not be excluded from the evaluation.
F. Schwab et al. / Environmental Pollution 192 (2014) 147e153
Notably, adding algae before the first desorption step (Fig. 4B, B symbols), instead of before the later steps (Fig. 4B, A symbols), increased the fraction of rapidly desorbing diuron: ~32% more diuron desorbed. The fraction of rapidly desorbing diuron here was 31.3 ± 1.4%, krapid was 0.61 ± 0.07 h1, and kslow was 0.002 ± 0.002 h1. Since the overall confidence bands of all three curves are not significantly different, this result should not be overinterpreted. 4. Conclusions Overall, the findings of this study show that changing environmental conditions, such as algal blooms, or effluent dilution, may affect the sorption equilibrium of pollutants bound to CNT significantly. This renders the behavior of pollutant-CNT mixtures in environment less predictable. The presence of algae led to moderate 15e20% (maximally 40%) of re-dissolution of sorbed micropollutant (represented here by diuron), despite of the strong sorbent properties of CNTs. Notably, industrial grade CNT, which are most likely to enter environment, showed higher sorption capacities and released almost no diuron in contrast to purified CNT, most likely due to their high amorphous carbon content and surface area. During the desorption experiment, ~31e41% of the diuron desorbed within hours from diuron-saturated CNT, which increases the environmental exposure of the herbicide. Without dilution, the major part of diuron (80e85%) remains strongly sorbed to the CNT with high KF, which greatly reduces environmental exposure of the herbicide. A common hypothesis is that the sorbed part of diuron should further be unavailable for aquatic organisms. We tested this hypothesis in a companion study on the viability of algae in presence of diuron-CNT mixtures (Schwab et al., 2013). The present proof-of-principle study has the limitation that it was performed with one algae and one pesticide only. Future studies using pesticides of increasing polarity and aromaticity, and more different algae species could help to understand the broader significance of the present results. Acknowledgment We thank the Swiss National Science Foundation (project no. 200021-118028, 200020-134688 for the funding of the study and the Federal Office for the Environment for additional financial szlo Forro is acknowledged for the synsupport. The group of La thesis and characterization of the dry CNT. Further, we gratefully acknowledge the research group of Hans-Ruedi Forrer (Agroscope €ppi ISS) who made their laboratory available for us, and Nicola Scha for assistance with the TOC graph. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2014.05.018. References Chen, G.C., Shan, X.Q., Pei, Z.G., Wang, H.H., Zheng, L.R., Zhang, J., Xie, Y.N., 2011. Adsorption of diuron and dichlobenil on multiwalled carbon nanotubes as affected by lead. J. Hazard. Mater. 188, 156e163. Chen, G.C., Shan, X.Q., Zhou, Y.Q., Shen, X.E., Huang, H.L., Khan, S.U., 2009. Adsorption kinetics, isotherms and thermodynamics of atrazine on surface oxidized multiwalled carbon nanotubes. J. Hazard. Mater. 169, 912e918. Chen, J.Y., Chen, W., Zhu, D., 2008. Adsorption of nonionic aromatic compounds to single-walled carbon nanotubes: effects of aqueous solution chemistry. Environ. Sci. Technol. 42, 7225e7230.
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Cornelissen, G., Haftka, J., Parsons, J., Gustafsson, O., 2005. Sorption to black carbon of organic compounds with varying polarity and planarity. Environ. Sci. Technol. 39, 3688e3694. Deng, J., Shao, Y.S., Gao, N.Y., Deng, Y., Tan, C.Q., Zhou, S.Q., Hu, X.H., 2012. Multiwalled carbon nanotubes as adsorbents for removal of herbicide diuron from aqueous solution. Chem. Eng. J. 193, 339e347. Gustafsson, O., Bucheli, T.D., Kukulska, Z., Andersson, M., Largeau, C., Rouzaud, J.N., Reddy, C.M., Eglinton, T.I., 2001. Evaluation of a protocol for the quantification of black carbon in sediments. Glob. Biogeochem. Cycles 15, 881e890. Hendren, C.O., Mesnard, X., Droge, J., Wiesner, M.R., 2011. Estimating production data for five engineered nanomaterials as a basis for exposure assessment. Environ. Sci. Technol. 45, 2562e2569. Hofmann, T., von der Kammer, F., 2009. Estimating the relevance of engineered carbonaceous nanoparticle facilitated transport of hydrophobic organic contaminants in porous media. Environ. Pollut. 157, 1117e1126. Knauer, K., Sobek, A., Bucheli, T.D., 2007. Reduced toxicity of diuron to the freshwater green alga Pseudokirchneriella subcapitata in the presence of black carbon. Aquat. Toxicol. 83, 143e148. Organisation for Economic Co-operation and Development (OECD): Paris, F, 2006. Freshwater Alga and Cyanobacteria, Growth Inhibition Test, 201. Organisation for Economic Co-operation and Development (OECD): Paris, F, 2000. Guidance Document on Adsorption e Desorption Using a Batch Equilibrium Method, 106. Oleszczuk, P., Pan, B., Xing, B.S., 2009. Adsorption and desorption of oxytetracycline and carbamazepine by multiwalled carbon nanotubes. Environ. Sci. Technol. 43, 9167e9173. Pan, B., Xing, B.S., 2008. Adsorption mechanisms of organic chemicals on carbon nanotubes. Environ. Sci. Technol. 42, 9005e9013. Pan, B., Xing, B.S., 2010a. Adsorption kinetics of 17 alpha-ethinyl estradiol and bisphenol A on carbon nanomaterials. I. Several concerns regarding pseudofirst order and pseudo-second order models. J. Soils Sediments 10, 838e844. Pan, B., Xing, B.S., 2010b. Manufactured nanoparticles and their sorption of organic chemicals. Adv. Agron. 108, 137e181. Pan, B., Zhang, D., Li, H., Wu, M., Wang, Z., Xing, B., 2013. Increased adsorption of sulfamethoxazole on suspended carbon nanotubes by dissolved humic acid. Environ. Sci. Technol. 47, 7722e7728. Pikaar, I., Koelmans, A.A., van Noort, P.C.M., 2006. Sorption of organic compounds to activated carbons. Evaluation of isotherm models. Chemosphere 65, 2343e2351. Pyrzynska, K., Stafiej, A., Biesaga, M., 2007. Sorption behavior of acidic herbicides on carbon nanotubes. Microchim. Acta 159, 293e298. Schwab, F., Bucheli, T.D., Camenzuli, L., Magrez, A., Knauer, K., Sigg, L., Nowack, B., 2013. Diuron sorbed to carbon nanotubes exhibits enhanced toxicity to Chlorella vulgaris. Environ. Sci. Technol. 47, 7012e7019. Schwab, F., Bucheli, T.D., Lukhele, L., Magrez, A., Nowack, B., Sigg, L., Knauer, K., 2011. Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ. Sci. Technol. 45, 6136e6144. Schwarzenbach, R.P., Gschwend, P.M., Imboden, D.M., 2003. Environmental Organic Chemistry, second ed. John Wiley & Sons, Inc., Hoboken, New Jersey. Shi, B.Y., Zhuang, X.Y., Yan, X.M., Lu, J.J., Tang, H.X., 2010. Adsorption of atrazine by natural organic matter and surfactant dispersed carbon nanotubes. J. Environ. Sci. (Beijing, China) 22, 1195e1202. Sobek, A., Stamm, N., Bucheli, T.D., 2009. Sorption of phenyl urea herbicides to black carbon. Environ. Sci. Technol. 43, 8147e8152. Wang, X.L., Liu, Y., Tao, S., Xing, B.S., 2010. Relative importance of multiple mechanisms in sorption of organic compounds by multiwalled carbon nanotubes. Carbon 48, 3721e3728. Wang, X.L., Tao, S., Xing, B.S., 2009. Sorption and competition of aromatic compounds and humic acid on multiwalled carbon nanotubes. Environ. Sci. Technol. 43, 6214e6219. Wei, L.P., Thakkar, M., Chen, Y.H., Ntim, S.A., Mitra, S., Zhang, X.Y., 2010. Cytotoxicity effects of water dispersible oxidized multiwalled carbon nanotubes on marine alga, Dunaliella tertiolecta. Aquat. Toxicol. 100, 194e201. Wu, W., Jiang, W., Zhang, W., Lin, D., Yang, K., 2013. Influence of functional groups on desorption of organic compounds from carbon nanotubes into water: an insight into the desorption hysteresis. Environ. Sci. Technol. 47, 8373e8382. Xia, G.S., Ball, W.P., 2000. Polanyi-based models for the competitive sorption of lowpolarity organic contaminants on a natural sorbent. Environ. Sci. Technol. 34, 1246e1253. Xia, X.H., Li, Y.R., Zhou, Z.I., Feng, C.L., 2010. Bioavailability of adsorbed phenanthrene by black carbon and multi-walled carbon nanotubes to Agrobacterium. Chemosphere 78, 1329e1336. 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Environmental Pollution journal homepage: www.elsevier.com/locate/envpol
Sorption kinetics and equilibrium of the herbicide diuron to carbon nanotubes or soot in absence and presence of algae Fabienne Schwab a, b, Louise Camenzuli b, Katja Knauer c, Bernd Nowack a, Arnaud Magrez d, Laura Sigg e, Thomas D. Bucheli b, * a
Empa e Swiss Federal Laboratories for Materials Science and Technology, CH-9014 St. Gallen, Switzerland Agroscope, Institute for Sustainability Sciences ISS, CH-8046 Zurich, Switzerland Federal Office for Agriculture FOAG, CH-3003 Bern, Switzerland d EPFL e Ecole Polytechnique F ed erale de Lausanne, CH-1015 Lausanne, Switzerland e Eawag, Swiss Federal Institute of Aquatic Science and Technology, CH-8600 Duebendorf, Switzerland b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 February 2014 Received in revised form 12 May 2014 Accepted 26 May 2014 Available online xxx
Carbon nanotubes (CNT) are strong sorbents for organic micropollutants, but changing environmental conditions may alter the distribution and bioavailability of the sorbed substances. Therefore, we investigated the effect of green algae (Chlorella vulgaris) on sorption of a model pollutant (diuron, synonyms: 3-(3,4-Dichlorophenyl)-1,1-dimethylurea, DCMU) to CNT (multi-walled purified, industrial grade, pristine, and oxidized; reference material: Diesel soot). In absence of algae, diuron sorption to CNT was fast, strong, and nonlinear (Freundlich coefficients: 105.79e106.24 mg/kgCNT$(mg/L)n and 0.62e0.70 for KF and n, respectively). Adding algae to equilibrated diuron-CNT mixtures led to 15e20% (median) diuron redissolution. The relatively high amorphous carbon content slowed down ad-/desorption to/from the high energy sorption sites for both industrial grade CNT and soot. The results suggest that diuron binds readily, but e particularly in presence of algae e partially reversibly to CNT, which is of relevance for environmental exposure and risk assessment. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Bioavailability Sorption kinetics Black carbon Engineered nanomaterials Nanoparticles
1. Introduction Carbon nanotubes (CNT), a nano-scaled allotrope of carbon, can strongly sorb organic pollutants (OP) with a similar or higher affinity than other carbonaceous sorbents, depending on their high specific surface area (SSA), and their large delocalized electron systems (Pan and Xing, 2010b). Once released in the environment (Hendren et al., 2011), CNT may therefore change the fate and bioavailability of OP (Hofmann and von der Kammer, 2009; Pan and Xing, 2010b). Numerous different sorption mechanisms are discussed to explain and predict the fate of chemicals in the presence of CNT in equilibrium (Chen et al., 2011, 2008; Pan and Xing, 2008, 2010b; Wang et al., 2010, 2009; Wu et al., 2013). Less attention has been given to the kinetics of ad-, ab-, and desorption of OP on/from CNT, which is important to understand the release of OP from CNT as a secondary water contamination source. Initial studies suggest that
* Corresponding author. E-mail address: [email protected] (T.D. Bucheli). http://dx.doi.org/10.1016/j.envpol.2014.05.018 0269-7491/© 2014 Elsevier Ltd. All rights reserved.
many OP reversibly sorb to CNT on a time scale of hours (Chen et al., 2011, 2009; Oleszczuk et al., 2009; Pan and Xing, 2010a; Zhang et al., 2012). However, some pharmaceuticals' (Oleszczuk et al., 2009) and other OP's (Wu et al., 2013) sorption equilibrium to CNT was reached after 5 days only. It is currently not entirely clear why OP sorb that much slower to certain CNT than to others. One of the first studies on desorption of OP from CNT was performed by Oleszczuk et al. who showed that desorption kinetics of oxytetracycline and carbamazepine from CNT followed a twophase first order model consisting of a rapid and a slow desorbing fraction (Oleszczuk et al., 2009). Slightly slower desorption than sorption, and sorption hysteresis is proposed to be explainable by rearrangement of the CNT bundles, pore condensation, or the exothermic adsorption of OP to CNT (Pan and Xing, 2008). A more recent study suggested irreversible chemical reactions of the sorbate with carboxylic functional groups of the sorbent (Wu et al., 2013). Little is known about sorption in more complex, environmentally relevant setups, e.g. sorption in presence of natural organic matter (NOM) (Pan et al., 2013), or sorption in presence of organisms (Xia et al., 2010). Competitively sorbed NOM (Shi et al., 2010;
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Zuttel et al., 2002), or surface oxidation (Pan and Xing, 2010b; Wang et al., 2010), may strongly reduce the CNT sorption capacity, especially for aromatic or planar OP (Shi et al., 2010; Wang et al., 2010, 2009; Zhang et al., 2011). Then again, the presence of NOM may increase OP sorption to CNT, because it may enhance dispersion of the CNT, and thus increase the available CNT surface area (Pan et al., 2013). We found just one study which investigated the influence of organisms on sorption. Xia et al. suggested that the presence of Agrobacterium probably promoted desorption of phenanthrene from CNT in soil, or that the bacterium utilized sorbed phenanthrene (Xia et al., 2010). It is unclear what led to the increased availability of the OP, and if phenanthrene desorbed before it became bioavailable. Because algae are the major primary producers in aqueous environments, it is of particular interest how OP sorption to CNT is affected by them. Again, there is no information available on such interactions. Any biological activity in aqueous sorption experiments is usually suppressed by adding a biocide such as NaN3 (Shi et al., 2010). Information on the influence of organisms on OP sorption to CNT is needed to assess, for instance, the safety of applications aiming at removing OP from water by CNT. Generally, in view of the constantly growing CNT production volumes (Hendren et al., 2011), it would be useful to know the environmental exposure of micropollutants sorbed to CNT. Hence, the overall aim of our study was to systematically quantify the sorption processes in a pollutant-CNT-biota model system, and to test the hypothesis that algae may attenuate sorption similar to NOM. Experiments were performed with the widely used herbicide diuron (Cornelissen et al., 2005; Knauer et al., 2007), different types of CNT, soot as a reference sorbent, and the freshwater green alga Chlorella vulgaris. The specific goals were to a) quantify sorption thermodynamics and kinetics of diuron and CNT, b) quantify the impact of algae on the ongoing sorption processes in the pollutant-CNT-biota system, and c) compare the sorption of industrial, purified, oxidized and pristine CNT and the reference sorbent Diesel soot. Further, this paper aimed at providing mechanistic explanation for diuron sorption in a companion study showing enhanced toxicity of the herbicide in presence of CNT (Schwab et al., 2013). 2. Experimental section 2.1. Chemicals 3-(3,4-Dichlorophenyl)-1,1-dimethylurea (diuron, DCMU) and 3-(3,4dichlorophenyl)-1,1-dimethyl(D6)urea (D6-diuron), both >99% pure, were purchased from Labor Dr. Ehrenstorfer (Germany). For structures, see Table S1. Acetonitrile (99.99%) was obtained from SCHARLAU CHEMIE S.A. (Spain). All other chemicals were per analysis grade and obtained from Merck or SigmaeAldrich, Switzerland. Ultra-pure water (Milli-Q) was produced by a gradient A10 water purification system from Millipore (Volketswil, Switzerland). Nitrogen (99.99995%) was obtained from PanGas (Dagmarsellen, Switzerland).
2.2. Carbonaceous nanoparticles Purified pristine and oxidized CNT (ppCNT and poxCNT) were synthesized by catalytic chemical vapor deposition by EPFL Lausanne, Switzerland. Industrial pristine CNT (ipCNT) of similar size and shape were purchased from Cheap Tubes Inc., Brattleboro, VT 05301, USA. The average CNT diameter as determined by transmission electron microscopy ranged between 8 and 15 nm, and the length as determined by scanning electron microscopy between 0.5 and 2.0 mm. As native black carbon reference sorbent, a forklift Diesel soot standard (soot) with spherical primary particles in the range of 35 nm (Gustafsson et al., 2001) was used (Standard Reference Material 2975, National Institute of Standards and Technology, USA). Transmission electron microscopy images and detailed characterization data for all materials, and synthesis details are given in Fig. S1, Table S2, and in Schwab et al. (2011). The sorbent suspensions were prepared in 2-[4-(2-hydroxyethyl)piperazin-1-yl]ethanesulfonic acid (HEPES) buffered OECD algal test medium (OECD, 2006) 1.00 mM, pH 7.0 ± 0.3. Further details are provided in the supporting information (SI, sections “Preparation of Sorbent Suspensions”, and “Notes on the Sterile Preparation of the Particle Suspensions”).
2.3. Green algae cultivation Chlorella vulgaris, strain 211-11b (Culture Collection of Algae, SAG, University of €ttingen, Germany), was cultivated in the OECD algal test medium (OECD, 2006). In Go short, axenic cultures grew at 24 ± 0.5 C, 100 rpm, an illumination of 80 ± 15 mEm2 s1 (daylight lamps, Sylvania Gro-Lux F15W/Gro T8, Infors, Switzerland), and under a light:dark regime of 16:8 h. Algae used for tests were harvested in the exponential growth phase, and the cell density was counted using a haemocytometer chamber. More details on the incubation conditions are available elsewhere (OECD, 2006; Schwab et al., 2011). 2.4. CNT and soot suspensions The used CNT and soot in the standardized suspensions and their detailed behavior in the algal medium were characterized as described previously (Schwab et al., 2013, 2011). The polydispersity of the CNT suspensions was monitored using dynamic light scattering (DLS) in a range of 1e10 000 nm (Zetasizer Nano ZS, Malvern, UK) at the same experimental conditions as used for the ternary sorption experiments. Three replicates per treatment were measured. Finally, sorbent-algae suspensions were examined microscopically. For more details see SI, section “Dry and Suspended CNT Characterization.” 2.5. Binary sorption experiments All sorption isotherms with CNT or soot and diuron were obtained using a batch equilibration technique at 24 ± 2 C. Screw cap glass vials (22 mL) were used. To each vial, well homogenized sorbent stock suspension was added and diluted with algal growth medium to obtain, after addition of the diuron stock solution, a final nominal concentration of 10.0 mgCNT/L and 5.00 mgsoot/L, respectively. The exact sorbent concentration in the stock suspensions was calculated in each experiment from the weighed in mass of CNT or soot. Nine to ten different initial diuron concentrations in a range of 0.73e2994 mg/L were prepared by spiking different volumes of a diuron working stock solution to the CNT suspensions. The concentration range covered more than three orders of magnitude to account for the expected nonlinear sorption behavior of CNT. All concentrations were tested at least in duplicates, and control treatments at least in triplicates. We reduced the replicate number to two, for the sake of a higher number of tested concentrations. These test suspensions were prepared sterilely without biocide, despite of the increase of variability of the data this inflicts, to avoid killing the algae in the subsequent ternary sorption experiments (details in section “Notes to the sterile preparation of the particle suspensions” in the SI). Finally, the vials containing the sorbent-diuron mixture were sealed with polytetrafluoroethylene (PTFE) lined screw caps, additionally covered with Parafilm®, wrapped in aluminum foil and then pre-equilibrated on an orbital laboratory shaker. The mixtures were kept for 20 h at 175 rpm (to keep the sorbents in full suspension; see OECD, 2000) in the dark at 24 ± 2 C, and under equal conditions for 28 d to study sorption of diuron under non-equilibrium and equilibrium conditions, respectively. 2.6. Ternary sorption experiments To examine the change of sorption after perturbation of the system by living green algae, 7e37 104 cells/mL of C. vulgaris were added to 20 h-, or 28 d-kept diuron-CNT mixtures (equilibration conditions alike the binary sorption experiments). The added algae culture volume was controlled to change the total volume in the vials by 1.8%. For incubation, all vials were placed vertically inside of an illuminated sterile bench (15 ± 5 mEm2 s1) at room temperature to prevent contamination of the samples and to provide light for the algae. These conditions were chosen to keep the viability (photosynthetic activity) of the green algae constant in the control treatments (Schwab et al., 2013). After incubation the diuronCNT mixtures with green algae, the subsequent changes of the diuron concentration were measured after 3, 6, 15, and 24 h (sampling and quantification described in section “Diuron Analysis”). The robustness of this setup was verified by repeating some ternary sorption experiments under different incubation conditions (in 50.0 mL Erlenmeyer flasks at 100 rpm and 80 ± 15 mEm2 s1). 2.7. Sorption isotherms Sorbed diuron for both binary and ternary sorption experiments was calculated by mass balance using the initial and final quantified aqueous diuron concentrations (see section “Diuron Analysis”). The algae-affected “sorption isotherms” are denoted in this study by the term “perturbed isotherms”, where the perturbation was the incubation with C. vulgaris. Five common isotherm models were evaluated for fit to the data (Pikaar et al., 2006; Xia and Ball, 2000). All details on the modeling are provided in the SI, Table S5, sections “Modeling of (Perturbed) Sorption Isotherms”, “Details on the Different Sorption Models”, and “Details on the Goodness of the Fit of the Different Sorption Models”. Details on calculation of the fraction of additionally sorbed or re-dissolved diuron are provided in the SI. 2.8. Adsorption kinetics Batch adsorption experiments (50.0 mL per replicate) were performed in 50 mL screw-capped glass vials. Pristine purified CNT, ipCNT, and soot were tested (poxCNT
F. Schwab et al. / Environmental Pollution 192 (2014) 147e153
1.2E+07
A
purified pristine CNT industrial pristine CNT
1.0E+07 8.0E+06
cs (μg/kgCNT )
behaved in pre-trials identically to ppCNT). In each vial, sorbent stock suspension, algal growth medium, and diuron were combined to result in final concentrations of 10 mgCNT/L (ppCNT and ipCNT), 5.0 mgsoot/L, and 100 mg/L diuron. After addition of diuron, all vessels were immediately sealed and shaken on an orbital laboratory shaker at 24 ± 2 C in the dark. The dissolved diuron concentration was measured in these batches for the first time one min after the addition of diuron, and repeatedly thereafter until all sorbent-diuron mixtures had reached equilibrium. All time points were measured at least in duplicates. Selected time points were re-measured in a second repetition of the experiment to assure the reproducibility of the results. The kinetics of sorption was modeled using the empirical pseudo-second order model (PSOM, Equations S1eS3), and by the empirical pseudo-first order model (PFOM, Oleszczuk et al., 2009; Pan and Xing, 2010a; Zhang et al., 2012). Details on the fitting of the sorption kinetics are provided in the SI.
149
6.0E+06 4.0E+06
2.9. Desorption kinetics
2.0E+06 0.0E-01 0
Diuron concentrations of both the binary and ternary sorption experiments, as well as the kinetics trials, were measured by high performance liquid chromatography coupled with a tandem mass spectrometer (HPLC-MSMS). For this, 2 mL aliquots of each replicate of the solute-sorbent(-algae) mixtures were filtered to remove the CNT and/or algae through a 0.4 mm PTFE syringe filter (Millipore, Switzerland). The filtrate was spiked with deuterated internal diuron standard (D6diuron, sample storage conditions: 4 C, darkness, ipCNT > soot could be explained by the different accessibility of adsorption sites (e.g. aromatic sheets) for diuron. The amorphous carbon covering the aromatic sheets of the low purity ipCNT and soot (Table S2) may have limited fast diffusion of diuron to these sites. In agreement with that, the sorption kinetics of diuron to ipCNT was ~7 times slower than that of biphenyl and phenanthrene to CNT in Zhang et al. (2012), and also slower than the one of atrazine to CNT (Chen et al., 2009). Moreover, the sorption kinetics of diuron to the high purity ppCNT was comparable to the values found in the literature for CNT of similar purity (Deng et al., 2012). The fitted PSOM equilibrium sorption capacities cs,t¼∞ of 3.3 [2.3, 4.3]95% g/kgsoot, 4.5 [4.2, 4.7]95% g/kgCNT for ppCNT, and 9.4 [9.0, 9.8]95% g/kgCNT for ipCNT correlated highly (Pearson correlation coefficient of 0.9996, p < 0.018) with the SSA of these materials (Table S2), and were comparable when normalized to this parameter (36.4 mg/m2soot, 30.5 mg/m2CNT for ppCNT, and 21.4 mg/m2CNT for ipCNT). This finding points again to a sorption mechanism that is mainly dependent on the surface of the materials (see above). The obtained sorption capacities for CNT were comparable to recent findings for biphenyl and phenanthrene sorbed to multi-walled CNT (Zhang et al., 2012).
8.0 log cs (μg/kgsorbent)
7.0 6.5 6.0 5.5 5.0 4.5 4.0
-1
0
1
2
3
2
3
log c w (μg/L)
3.0 log (cs/SSA) (μg/msorbent2)
2.5
3.2. Sorption in absence of algae The estimated Freundlich parameters for diuron and all four materials equilibrated for 28 d are presented in Table 1 (results for 20 h in SI, Table S7 and Fig. S4, detailed discussion of the modeling in SI). The Freundlich constant KF of soot was with 104.55±0.13 mg/ kgsoot$(mg/L)n (average±95% confidence interval) comparable to the KF from Sobek et al. for diuron sorption to soot (104.33±0.04 mg/ kgsoot$(mg/L)n) measured in half cell systems (Sobek et al., 2009). The small difference of 5% between the two KF demonstrates that the present experimental setup produced reproducible results. The ipCNT sorbed diuron ~0.5 orders of magnitude stronger (KF ¼ 106.24±0.10 mg/kgCNT$(mg/L)n) than ppCNT (KF ¼ 105.84±0.15 mg/
A
7.5
B
2.0 1.5 1.0 0.5 0.0 -0.5 -1.0
-1
0
1
log c w (μg/L) Fig. 2. Selected sorption isotherms of the herbicide diuron to purified pristine carbon nanotubes (CNT, C), purified oxidized CNT (B), industrial pristine CNT ( ), and the reference sorbent soot ( ) with Freundlich fits (for fitting parameters, see Table 1), normalized to sorbent mass (A), and specific surface area (SSA, B). All sorbentesorbate mixtures were equilibrated for 28 d without addition of biocide. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Table 1 Freundlich fitting parameters (log KF: Freundlich sorption coefficient, n: nonlinearity constant) for all non-perturbed isotherms (i.e. before addition of algae, highlighted with 2 bold letters) and for all perturbed isotherms (3, 6, 15, and 24 h incubation with algae). As a measure of the goodness of the fit, the adjusted correlation coefficient Radj is shown. All sorbentesorbate mixtures were equilibrated for 28 d. log KF (mg/kgsorbent$(mg/L)n) Av Purified pristine CNT
Purified oxidized CNT
Industrial pristine CNT
Soot
Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae Before addition of algae 3 h incubation with algae 6 h incubation with algae 15 h incubation with algae 24 h incubation with algae
5.84 5.79 5.72 5.69 5.76 5.84 5.72 5.51 5.57 5.62 6.24 6.28 6.30 6.25 6.28 4.55 4.18 4.32 4.34 4.33
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
R2adj
n ()
95% conf. int.
Rel. error (%)
Av
0.15 0.13 0.18 0.11 0.21 0.14 0.15 0.28 0.15 0.23 0.10 0.11 0.09 0.08 0.09 0.13 0.16 0.23 0.25 0.17
1.3 1.1 1.5 0.9 1.7 1.2 1.3 2.5 1.2 2.0 0.7 0.9 0.7 0.6 0.7 1.3 1.9 2.6 2.7 1.9
0.62 0.65 0.65 0.66 0.61 0.67 0.68 0.80 0.69 0.70 0.64 0.59 0.59 0.62 0.59 0.97 1.10 1.03 0.99 1.02
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
95% conf. int.
Rel. error (%)
0.11 0.09 0.12 0.07 0.13 0.10 0.10 0.19 0.09 0.15 0.06 0.07 0.06 0.05 0.06 0.08 0.09 0.14 0.14 0.10
8.5 6.5 9.2 5.0 10.4 7.1 6.9 11.4 6.1 10.4 4.7 5.6 4.6 4.2 4.7 3.7 3.9 6.3 6.6 4.5
0.820 0.919 0.796 0.960 0.780 0.863 0.905 0.725 0.933 0.794 0.956 0.941 0.957 0.963 0.956 0.973 0.975 0.925 0.934 0.965
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151
Fig. 3. Re-dissolved diuron (medians and non-outlier range) after different incubation times of algae with 28 d pre-equilibrated diuron-sorbent mixtures, and the four sorbents under investigation. Nonparametric comparison of multiple independent groups (KruskaleWallis one-way analysis of variances, N ¼ 84e99), p ¼ 0.0002e0.04 for 15 h, p ¼ 0.000002e0.02 for 24 h. *: Significantly higher than one group. **: Significantly higher than two groups. Reading example: After 15 h, the redissolved diuron of purified pristine CNT is significantly higher than after 3 h and 6 h (i.e., two groups). Absolute concentration changes provided in Fig. S6.
kgCNT$(mg/L)n) and poxCNT (KF ¼ 105.84±0.14 mg/kgCNT$(mg/L)n). The ppCNT and poxCNT again sorbed diuron >1 order of magnitude stronger than soot. The oxidation of poxCNT did, as in the kinetics experiments, not affect the sorption strength significantly: Both ppCNT and poxCNT exhibited similar KF and n. The sorption was for both CNT rather nonlinear (ppCNT: n ¼ 0.62 ± 0.11, poxCNT: n ¼ 0.67 ± 0.10) as compared to soot (n ¼ 0.97 ± 0.08). The different KF of purified and ipCNT were most importantly, likely mainly a result of the different SSA of the sorbents, and not by different sorption mechanisms. This interpretation is further supported by a plot of the sorption isotherms normalized by the SSA (Fig. 2B), in which all isotherms of CNT collapse on one non-significantly different isotherm. Hydrogen bonding and Lewis acid-base based sorption mechanisms due to the carboxylic groups seem thus rather unlikely. Electrostatic interactions are also not expected to occur, because diuron is neutrally charged at pH 7.00. Therefore, it seems most probable that diuron bound to the CNT via pep stacking on the highly condensed aromatic sheet regions, present both in CNT and soot. This binding mechanism is supported by the fact that diuron is a rather polar molecule (dipole moment is 7.55 Debye, (Chen et al., 2011). After surface saturation of the CNT, lower-energy sorption sites for the neutrally charged diuron such as defects in the aromatic sheets, interstitial and groove regions between CNT bundles, and residual amorphous carbon may be occupied, resulting in the observed nonlinear sorption (Figs. 2 and S4, Pan and Xing, 2008, 2010b; Pikaar et al., 2006). Likewise, the lower sorption of diuron to soot as compared to the CNT could be explained by the lower SSA of soot, the high content of oxygen (Table S2) on the soot surface, and attenuation of diuron sorption due to the amorphous carbon covering the CNT
surfaces, similar to the attenuation of the sorption by NOM (Shi et al., 2010; Wang et al., 2010, 2009; Zhang et al., 2011). This explanation is supported by the finding of Knauer et al. (2007) who found for combusted (i.e. amorphous carbon free) soot a very high KF of 105.7 mg/kgsoot$(mg/L)n. This KF is comparable to those of ppCNT and poxCNT (Table 1), suggesting that the condensed carbon sheets of combusted soot, once accessible, bind diuron in a similar way as the aromatic sheets of CNT. 3.3. Microscopic investigations of algae-CNT suspensions Brightfield microscopy revealed that the majority of algal cells attached to CNT agglomerates (Table S3, Fig. S5B). Mixing of the suspensions enhanced this agglomeration. In agreement with previous work (Schwab et al., 2013), and the results presented above, both the ppCNT and poxCNT heavily agglomerated with algae (Fig. S5B). The ipCNT were better dispersed, but still formed agglomerates >100 mm with algae. In contrast, soot and algae rarely attached to each other (max. diameter of agglomerates ~15 mm). No morphological changes of the cells exposed to any of the tested particles were observed, in agreement with previous studies (Schwab et al., 2011; Wei et al., 2010). 3.4. Sorption equilibrium change in presence of algae and evolution with time After 24 h of incubation of algae and the 28 d-equilibrated diuron-CNT mixtures, medians 15e20% (non-outlier range up to 40% maximum change) of the sorbed diuron re-dissolved from the ppCNT and poxCNT (Fig. 3). Re-dissolution occurred only in
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presence of algae, as shown in equally treated control experiments with equilibrated diuron-CNT mixtures without algae (see section “No Effect of Algal Exudates”). Given that algal cells intensively agglomerated with CNT, even if very low CNT concentrations were present in suspension, we conclude that the attachment of algae to CNT led to more competition for sorption sites, similar as observed for humic acid and CNT (Wang et al., 2009). As a consequence, diuron re-dissolved. Exudates clearly did not affect the sorption (see section below). Evidence for re-dissolution due to addition of algae is also provided by increased diuron algal toxicity caused by locally elevated diuron concentrations (Schwab et al., 2013). This explanation is supported by the microscopic investigations mentioned above, which showed that ppCNT and poxCNT agglomerated most extensively with algal cells, leading to highly competitive sorption, and therefore more diuron release than in ipCNT and soot. The variability for soot was again higher due to the lower absolute soot concentration, but the trends in Fig. 3 point to minimal diuron re-dissolution, presumably because algae did not attach to soot. Again, the ppCNT and poxCNT behaved similarly, suggesting little effect of the oxygen functional groups. The ipCNT behaved similar to soot: both did not lead to significant amounts of re-dissolved diuron. More details on the temporal change of the sorption equilibrium after addition of algae are given in the SI (Table S7, Figs. S7, S8, chapter “Change of KF with time”). 3.5. No effect of algal exudates Diuron uptake/sorption by algae, or by algal exudates, was found in the control experiments (SI, section “Quality Assurance”) to be negligible, presumably, due to the more than two orders of magnitude stronger sorption of diuron to CNT than to algae/exudates, the relative short incubation of the mixture with algae (24 h), and the >11 times lower concentration of algae/exudates than CNT/ soot. A worst-case calculation of the maximal percentage of diuron sorbed by algal exudates resulted in a maximal concentration of 0.13% only (assuming the algae produced their own weight in exudates, and assuming a worst-case log(KOC) for diuron of 3.5 (Schwarzenbach et al., 2003)). This calculation also shows that increasing the algal biomass by a factor of 10e1000, as it is possible during massive algal blooms, would elevate the maximal percentage of diuron sorbed by exudates to 1.2e55.7%. Results at such high algal densities are more difficult to interpret, because at densities of several million cells/mL, the algae start to inhibit their own growth. 3.6. Desorption kinetics in absence of algae Diuron desorption occurred within ~4 h (Fig. 4A). The obtained data fitted well to the two-phase desorption kinetics model (Equation S7). A fraction of 39.6 ± 1.5% (Frapid, ±standard error) of the diuron rapidly desorbed from the ppCNT, and Fslow was consequently 60.4 ± 1.5%. This implies that, if equilibrium conditions change, for example, if a solid phase extraction cartridge leaches CNT, or a CNT-containing effluent gets diluted, a considerable fraction of diuron sorbed to CNT may again be released to the aqueous environment on a relevant time scale. However, it should be noted that in the present desorption kinetics experimental setup, the used CNT were saturated with diuron. The observed 39.6 ± 1.5% is therefore the maximal expectable rapid desorbing fraction of diuron sorbed to CNT. Under environmental conditions as in the above shown ternary sorption experiments, CNT are not saturated with diuron and smaller fractions of diuron therefore release. The rate constants krapid and kslow were 0.66 ± 0.07 h1, and 0.002 ± 0.002 h1, respectively, revealing that compared to the k2* of the sorption kinetics (see above), the desorption process of diuron from CNT was slower. Compared to literature data, the
Fig. 4. Fraction of desorbed diuron from purified pristine carbon nanotubes (ppCNT) as a function of time. Fits: Two-phase desorption kinetics model. A: Desorption from CNT alone (C), pooled data from two independent experiments. B: Desorption from CNT in presence of algae added before the first desorption step ( ), or added once before one of the desorption steps 2e8 (A). For further details, see text. Note that the match of the solid line in B with some of the symbols is coincidence. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
desorption kinetics of diuron from CNT is still ~4e15 times faster than e.g. the desorption of carbamazepine and oxytetracycline from similar CNT (Oleszczuk et al., 2009). The observed desorption hysteresis is in accordance with results of other studies for compounds of similar structure, polarity or size (Oleszczuk et al., 2009; Pyrzynska et al., 2007). 3.7. Desorption kinetics in presence of algae In Fig. 4B, the desorption kinetics of diuron from CNT after addition of algae before the first desorption step, and added once at a given desorption step (2e8) is shown. The diuron desorption kinetics in presence of algae was almost identical to the one in absence of algae (krapid ¼ 0.7 ± 0.2 h1, kslow ¼ 0.002 ± 0.004 h1). With 41 ± 4% (mean ± standard error), the fraction of rapidly desorbing diuron was also not significantly different from the fraction of diuron desorbed in absence of algae. This shows that under non-equilibrium conditions, the effect of the presence of algae was overridden by the tendency of the system to re-establish sorption equilibrium. The standard error was slightly higher, mainly due to a replicate sample in which >60% diuron desorbed (Fig. 4B). Outlier tests and repeated measurements of this sample showed that it could not be excluded from the evaluation.
F. Schwab et al. / Environmental Pollution 192 (2014) 147e153
Notably, adding algae before the first desorption step (Fig. 4B, B symbols), instead of before the later steps (Fig. 4B, A symbols), increased the fraction of rapidly desorbing diuron: ~32% more diuron desorbed. The fraction of rapidly desorbing diuron here was 31.3 ± 1.4%, krapid was 0.61 ± 0.07 h1, and kslow was 0.002 ± 0.002 h1. Since the overall confidence bands of all three curves are not significantly different, this result should not be overinterpreted. 4. Conclusions Overall, the findings of this study show that changing environmental conditions, such as algal blooms, or effluent dilution, may affect the sorption equilibrium of pollutants bound to CNT significantly. This renders the behavior of pollutant-CNT mixtures in environment less predictable. The presence of algae led to moderate 15e20% (maximally 40%) of re-dissolution of sorbed micropollutant (represented here by diuron), despite of the strong sorbent properties of CNTs. Notably, industrial grade CNT, which are most likely to enter environment, showed higher sorption capacities and released almost no diuron in contrast to purified CNT, most likely due to their high amorphous carbon content and surface area. During the desorption experiment, ~31e41% of the diuron desorbed within hours from diuron-saturated CNT, which increases the environmental exposure of the herbicide. Without dilution, the major part of diuron (80e85%) remains strongly sorbed to the CNT with high KF, which greatly reduces environmental exposure of the herbicide. A common hypothesis is that the sorbed part of diuron should further be unavailable for aquatic organisms. We tested this hypothesis in a companion study on the viability of algae in presence of diuron-CNT mixtures (Schwab et al., 2013). The present proof-of-principle study has the limitation that it was performed with one algae and one pesticide only. Future studies using pesticides of increasing polarity and aromaticity, and more different algae species could help to understand the broader significance of the present results. Acknowledgment We thank the Swiss National Science Foundation (project no. 200021-118028, 200020-134688 for the funding of the study and the Federal Office for the Environment for additional financial szlo Forro is acknowledged for the synsupport. The group of La thesis and characterization of the dry CNT. Further, we gratefully acknowledge the research group of Hans-Ruedi Forrer (Agroscope €ppi ISS) who made their laboratory available for us, and Nicola Scha for assistance with the TOC graph. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2014.05.018. References Chen, G.C., Shan, X.Q., Pei, Z.G., Wang, H.H., Zheng, L.R., Zhang, J., Xie, Y.N., 2011. Adsorption of diuron and dichlobenil on multiwalled carbon nanotubes as affected by lead. J. Hazard. Mater. 188, 156e163. Chen, G.C., Shan, X.Q., Zhou, Y.Q., Shen, X.E., Huang, H.L., Khan, S.U., 2009. Adsorption kinetics, isotherms and thermodynamics of atrazine on surface oxidized multiwalled carbon nanotubes. J. Hazard. Mater. 169, 912e918. Chen, J.Y., Chen, W., Zhu, D., 2008. Adsorption of nonionic aromatic compounds to single-walled carbon nanotubes: effects of aqueous solution chemistry. Environ. Sci. Technol. 42, 7225e7230.
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