Yingqing
Deng
a,
Brian
Eitzer
b,
Jason C.
White
*b and
Baoshan
Xing
*a
aStockbridge School of Agriculture, University of Massachusetts Amherst, Amherst, Massachusetts 01003, USA. E-mail: bx@umass.edu
bDepartment of Analytical Chemistry, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, Connecticut 06511, USA. E-mail: Jason.White@ct.gov
First published on 30th November 2016
Pre-existing pharmaceutical residues in agricultural soils may encounter engineered nanomaterials, resulting in poorly understood co-contamination interactions. In this study, the bioaccumulation and translocation of the pharmaceutical residue carbamazepine (100 μg L−1) in collard greens (Brassica oleracea) was evaluated upon concurrent exposure to pristine or carboxyl-functionalized multiwall carbon nanotubes (pCNTs or cCNTs) at 50 mg L−1 under hydroponic exposure and at 500 mg kg−1 in soil-grown conditions. B. oleracea toxicity was more evident under hydroponic exposure, with growth inhibtion dependent on carbamazepine concentrations; however, biomass enhancement was noted in cCNTs-treated plants. Without CNTs, B. oleracea accumulated and translocated significant amounts of carbamazepine; up to 2500 μg kg−1 in the leaves and 300 μg kg−1 in the roots, depending on growth condition. The co-exposure of carbon materials notably suppressed carbamazepine accumulation in both hydroponic and soil systems. Specifically, root carbamazepine content in soil-grown plants was suppressed 29%, 53% and 89% by pCNTs, cCNTs and AC, respectively. Generally, the adsorption capacity of the carbon materials correlated well with the suppression of carbamazepine accumulation. The results also suggest that functionalization of CNTs enhanced carbamazepine translocation potential and significantly affected nanomaterial/co-contaminant interactions as compared to its pristine analog. These findings show that the CNTs in the environment may significantly affect the bioavailability and translocation pattern of coexisting organic contaminants.
Environmental significanceThere is limited information on nanomaterial interactions with co-contaminants, including the subsequent impact on biological uptake of these materials. We evaluated the impact of multiwall carbon nanotube (CNT) co-exposure on the fate of the pharmaceutical carbamazepine in a model plant. The work involved two exposure conditions, employed activated carbon as a control, and evaluated the role of functionalization on carbamazepine fate within the plant. The plants accumulated significant amounts of carbamazepine; up to 2500 μg kg−1 in the leaves and 300 μg kg−1 in the roots. CNT co-exposure suppressed carbamazepine accumulation; the adsorption capacity of the carbon correlated well with the suppression of pharmaceutical accumulation. CNT functionalization enhanced carbamazepine translocation and significantly affected nanomaterial/co-contaminant interactions as compared to its pristine analog. |
In recent years, concern over the ecological risk of nanomaterials has expanded from direct effects on biota to the impact on co-existing contaminant fate and effects. Adsorption studies have shown that CNTs affect the fate and transport of sorbed organic contaminants in the environment, which may subsequently alter bioavailability and toxicity.9 For example, single-wall CNTs exhibited high adsorption capacity for phenanthrene and reduced toxicity of the residue to algae (P. subcapitata); however, the presence of four other multiwall CNTs had no effect on phenanthrene toxicity.10 In another study with diuron, the presence of CNTs reduced the adverse effects of the herbicide on green algae Chlorella vulgaris.11 In addition, previous studies have revealed that CNTs may penetrate cell walls and membranes, raising the possibility of these materials serving as molecular transporters and consequently affecting contaminant bioaccumulation.12,13 Although concerns over CNT impacts on co-contaminant fate in terrestrial systems are significant, relatively little work has been done in this area. Petersen et al. reported decreased pyrene accumulation (25–50%) by earthworms (Eisenia foetida) in two soils amended with 3000 mg kg−1 CNTs.14 Wild et al. reported that in wheat roots exposed to multiwall CNTs, root cap cells pierced by the nanomaterial accumulated phenanthrene approximately 50% faster than roots not exposed to CNTs.15 In another study with four crop species, multiwall CNTs were found to decrease the accumulation of the weathered pesticides chlordane and DDx (DDT + metabolites) from soil in a dose-dependent fashion.16 It is clear that the literature on nanomaterial/co-contaminant interactions is both limited and contradictory; without a further understanding of these processes through significant additional investigations, an accurate assessment of nanomaterial risk in terrestrial systems will not be possible.
The current study focused on co-contamination between carbon nanotubes and a pharmaceutical compound in a model agricultural soil. Carbamazepine was chosen as a representative pharmaceutical residue because of its frequent detection and persistence in water bodies.17 Carbamazepine was detected in WWTP effluents up to 0.95 μg L−1 and in biosolids at 281.2 μg kg−1.18–20 It has also been reported that carbamazepine would irreversibly bind to soil and therefore exhibit low leaching potential.21,22 In addition, carbamazepine has a moderate octanol–water partitioning coefficient (logKow 2.45) and will remain non-ionic under soil conditions (pKa 13.4); as such, the residue has a significant potential to accumulate in plants through biosolids application or reclamation of treated water.23,24 Here, collard greens (B. oleracea) were exposed to carbamazepine in the presence of CNTs under both hydroponic and soil-grown conditions. To assess the effect of carbamazepine–CNTs interactions on B. oleracea, biomass was monitored under all conditions and carbamazepine bioaccumulation was determined through liquid chromatography with high-resolution mass spectrometry (LC-HRMS). The adsorption of carbamazepine onto CNTs was also evaluated under abiotic conditions. The results of this study will further our understanding of the interactions between nanomaterials and organic contaminants in agricultural soils and provide critical information concerning risk from the presence of nanomaterials in the environment.
An additional experiment was conducted in which the regular rinsing was replaced with surfactant washing assisted with sonication (sodium dodecyl benzene sulphonate, SDBS, 0.5%, 30 min). The sonication was performed identically to the previously described method. SDBS was chosen from preliminary tests and due to its reported high ability to suspend CNTs.34 Individual roots were divided in half and were treated separately with regular washing and the surfactant/sonication procedure. The root samples after the two different washing procedures were further extracted by the QuEChERS procedure and were analyzed as described below.
Under hydroponic conditions, plant biomass was affected as a function of treatment (Table 1). In the presence of carbamazepine only, B. oleracea biomass decreased by 25% at the highest exposure concentration (10 mg L−1). However, overt visible damage at the leaf margins and modified morphology were evident at concentrations as low as 1 mg L−1. Upon exposure to pCNTs alone, reductions in B. oleracea biomass were evident mainly in the roots; but the total plant biomass was not significantly affected at 42 d (Table 1, row 1). Previous studies addressing carbon nanotube phytotoxicity have produced contradictory findings. With regard to hydroponic conditions, Lin et al. reported that CNTs (pristine, multi-wall) did not affect root growth of five plant species, including Brassica napus (rape), Raphanus sativus (radish), Lactuca sativa (lettuce), Zea mays (corn) and Cucumis sativus (cucumber), at concentrations as high as 2000 mg L−1.35 However, adverse effects from multi-wall CNTs exposure were observed in other studies, including growth inhibition and cell death in Amaranthus tricolor (red spinach) at 125–1000 mg L−1, decreased biomass of Cucurbita pepo (zucchini) at 1000 mg L−1, and suppressed growth with electrolyte leakage in Amaranthus tricolor, Lactuca sativa and Cucumis sativus at 1000 mg L−1.36–38 In general, CNTs phytoxocity was observed at higher and likely unrealistic exposure concentrations. The CNTs level used in the current study was only 50 mg L−1 (hydroponic assay); a lack of apparent phytotoxicity from this level of exposure is not surprising.
Carbamazepine concentration | Leaf | Root | Total | |||
---|---|---|---|---|---|---|
Control | pCNT 50 mg L−1 | Control | pCNT 50 mg L−1 | Control | pCNT 50 mg L−1 | |
a Each data point is the average of 8 individual measurements. Data analysis was performed through two-way ANOVA with Tukey's test. The interactions between two factors (carbamazepine and pCNTs) were found insignificant. Thus within columns (carbamazepine), values followed by different letters are significantly different at p < 0.05. Within rows (pCNTs), values marked with asterisks (*) are statistically different from values in control column with *p < 0.05 and **p < 0.01. | ||||||
0 μg L−1 | 14.8 ± 1.8 A | 13.5 ± 2.6 A | 9.2 ± 3.2 A | 6.8 ± 1.5 A | 24.0 ± 4.3 A | 20.3 ± 3.9 A |
100 μg L−1 | 14.0 ± 1.1 A | 12.2 ± 2.4 A | 6.4 ± 1.6 A | 6.3 ± 1.4 A | 20.4 ± 2.5 A | 19.7 ± 1.3 A |
500 μg L−1 | 12.9 ± 3.3 A | 12.8 ± 0.6 A | 7.4 ± 1.3 A | 6.5 ± 0.8 A | 20.3 ± 3.9 A | 20.8 ± 0.5 A |
1 mg L−1 | 14.2 ± 2.5 A | 14.0 ± 1.4 A | 7.6 ± 2.1 A | 4.6 ± 0.7 A* | 21.8 ± 4.5 A | 18.5 ± 1.4 A* |
5 mg L−1 | 13.6 ± 2.1 A | 13.3 ± 2.7 A | 6.3 ± 0.7 B | 3.7 ± 0.7 B** | 19.8 ± 2.4 A | 17.0 ± 3.6 A* |
10 mg L−1 | 12.5 ± 1.5 A | 13.2 ± 2.4 A | 5.5 ± 1.5 B | 4.3 ± 1.0 B* | 18.0 ± 2.7 B | 17.5 ± 3.1 A |
We do note that a more limited number of studies have addressed CNT toxicity as a function of surface modification. As shown in this study (Table 2), pCNTs at 50 mg L−1 had no significant adverse effect on biomass production under hydroponic conditions, while cCNTs exposure in the absence of carbamazepine significantly increased leaf biomass by 28% and total plant biomass by 25%. In several previous studies, oxidized or functionalized CNTs were also reported to promote plant growth. Mondal et al. found that oxidized multi-wall CNTs stimulated shoot and root growth; the authors suggested the use of oxidized CNTs as a beneficial growth promoter.39 Notably, there was no parallel exposure to pristine CNTs at identical concentrations. Similarly, root elongation and biomass increases were also reported in Triticum aestivum (wheat) treated with oxidized CNTs.40 While the underlying mechanisms of CNTs surface chemistry effects on plant physiology are unknown, the difference between the two CNTs with regards to biomass production in this study could possibly be linked to water transpiration differences. In a similar hydroponic study, the cumulative transpiration of water in maize exposed to 50 mg L−1 of cCNTs for 18 d was almost twice as much as that in the unexposed and pCNTs-exposed maize.41 Khodakovskaya et al. reported up-regulation of the water-channel LeAqp2 gene in Solanum lycopersicum (tomato) after exposure to COOH-functionalized CNTs.42 Villagarcia et al. also compared the expression of water channel proteins in Solanum lycopersicum exposed to carbon nanotubes functionalized with different groups and observed a strong correlation between protein expression and CNTs surface functionalization.43 In the current study, cCNTs had greater dispersion stability and promoted plant growth, possibly due to enhanced water uptake capacity. In contrast, the pCNTs had no distinct impact on plant growth, likely because agglomerates were more readily formed and the actual CNTs exposure concentration was lowered.
Treatment | Hydroponics 28 d | Soil 42 d | ||||
---|---|---|---|---|---|---|
Leaf | Root | Total | Leaf | Root | Total | |
a Each data point is the average of 8 individual measurements. Data analysis was performed through two-way ANOVA with Tukey's test. Values marked with asterisks (*) are statistically different from control with *p < 0.05. Carbamazepine was applied at 100 μg L−1; pCNTs and cCNTs were tested at 50 mg L−1 in hydroponics and 0.5 mg g−1 in soil. | ||||||
Control | 7.1 ± 1.4 | 2.6 ± 0.5 | 9.7 ± 2.6 | 7.8 ± 2.0 | 2.9 ± 0.8 | 10.7 ± 2.6 |
Carbamazepine | 7.6 ± 1.4 | 2.7 ± 0.7 | 10.3 ± 3.5 | 6.9 ± 1.0 | 2.9 ± 0.8 | 9.9 ± 1.2 |
pCNTs | 6.7 ± 2.2 | 2.3 ± 0.5 | 9.0 ± 3.0 | 7.4 ± 0.9 | 3.3 ± 0.6 | 10.7 ± 1.6 |
pCNTs + carbamazepine | 7.5 ± 1.5 | 2.7 ± 0.6 | 10.2 ± 3.4 | 6.7 ± 1.4 | 2.4 ± 0.8 | 9.1 ± 2.1 |
cCNTs | 9.1 ± 2.7* | 3.0 ± 0.7 | 12.1 ± 3.6* | 6.8 ± 1.3 | 2.9 ± 0.8 | 9.7 ± 2.6 |
cCNTs + carbamazepine | 7.4 ± 2.4 | 2.7 ± 0.7 | 10.1 ± 3.5 | 6.5 ± 1.2 | 2.4 ± 0.5 | 8.9 ± 1.5 |
In addition to exposure under single analyte conditions (carbamazepine or CNTs), the results from hydroponic co-exposure scenario indicated that the interaction between carbamazepine and CNTs did not have a significant effect on biomass production. In contrast to the hydroponic scenario, leaf, root and total plant biomass in soil were unaffected by any of the treatments (Table 2). In soil, CNTs aggregation and attachment to soil particles likely significantly reduced the accessibility of the nanomaterial to root tissues. These differential findings based on experimental or exposure conditions highlight the importance of evaluating phytotoxicity under conditions of environmental relevance.
Co-exposure to carbon materials significantly altered carbamazepine accumulation and translocation within B. oleracea. As shown in Fig. 1 (hydroponics), carbamazepine leaf concentrations were decreased in the presence of carbon materials. Compared to carbamazepine only exposure, co-exposure to pCNTs and cCNTs reduced carbamazepine leaf content by 21% and 41%, respectively. The activated carbon treatment dramatically reduced leaf carbamazepine levels (93%) as compared to controls. Not surprisingly, the carbamazepine root concentration was significantly elevated by carbon co-exposure after routine root washing. Specifically, the carbamazepine root concentrations in the presence of pCNTs, cCNTs and AC were 6.6, 3.1 and 6.0 times greater than the control. The elevated root carbamazepine levels were likely due to the substantial deposition of carbon nanomaterials that had previously adsorbed the co-contaminant carbamazepine prior to root surface association. Even though surfactant washing and sonication removed significant amounts of carbamazepine from CNTs-treated roots, the remaining residue content in root was still significantly greater than the controls (Fig. 3). The results showed that more carbamazepine was incorporated into roots with the presence of CNTs. However, in general, carbamazepine accumulation in the whole plant (as well as edible leaves) was suppressed by CNTs and AC co-exposure. In addition to transfer factors, the bioconcentration factors (BCF, concentration in tissues/concentration in growth media) were calculated due to the variability in root concentrations (ESI,† Table S1). The transfer potential of carbamazepine from root to leaf was significantly lowered by carbon co-exposure. In particular, the TF was decreased from 24.4 (control) to 2.5, 3.5 and 0.2 in the pCNTs, cCNTs and AC treatments, respectively. As evident from the root and leaf BCF values, root accumulation of carbamazepine was enhanced by carbon co-exposure while the leaf bioaccumulation potential was lowered. Regardless of the difference among carbon material type, the in planta distribution pattern of the pharmaceutical was dramatically altered in the presence of carbon materials under hydroponic conditions. The application of carbon could decrease the risk of human exposure to selected pharmaceuticals from crops grown in contaminated media. With respect to optimizing crop protection in contaminated environments, AC is a better agent than CNTs under these growth conditions.
Although all carbon materials similarly suppressed carbamazepine uptake into edible tissues under hydroponic conditions, there are distinct differences based on carbon type. Since the interaction between carbamazepine and carbon materials was predominantly adsorption, the different suppression effect by carbon materials could possibly be explained through this process. The kinetics of this molecular process was evaluated in planted and un-planted systems (Fig. 2). In un-planted reactors, the carbamazepine content in the nutrient solution declined rapidly (within the first 12 h) in the presence of CNTs and AC, and gradually stabilized after 24 h. With B. oleracea seedlings present, carbarmazepine concentrations continued to decline after 24 h. In calculating the adsorbed amount Qt, a pseudo-second-order kinetics model was found to best represent carbamazepine interaction on carbon materials (regression coefficients above 0.999 for three adsorbents). As previously reported for multilayer loading, carbamazepine adsorption on CNTs was likely governed by hydrophobic interactions and π–π electron-donor–acceptor interactions.48 In comparison to CNTs, the conventional activated carbon displayed relatively slower adsorption but higher capacity at equilibrium. The higher capacity could likely be explained through higher specific surface area in AC (1380 m2 g−1) than CNTs (500 m2 g−1). The AC used in this study provided a large number of adsorption sites with a well-developed internal microporosity and therefore significantly reduced the actual exposure concentration of carbamazepine to the plants. As a consequence, the leaf carbamazepine concentration under the AC co-exposure was much lower than with the CNTs and carbon-free exposure.
Notably, cCNTs in this study were different from pCNTs with regard to the adsorption capacities and the subsequent impact on carbamazepine bioaccumulation. The pCNTs and cCNTs had similar properties, including size, length and SSA; the primary exception being the COOH (3.8%) modification. As observed in Fig. 2, cCNTs adsorbed more carbamazepine than pCNTs. The adsorbed carbamazepine on pCNTs and cCNTs reached 4.6 and 5.8 mg g−1 respectively, although we do note that these values may be underestimated due to interferences from nutritional salts in solution or to insufficient agitation from aeration. The surfaces of pCNTs were hydrophobic and had poor wettability in the growth media; in contrast, functionalization of CNTs with COOH groups altered the surface charge and the hydrophobicity. These changes resulted from COOH groups further increased adsorption capacity and affinity, likely by increasing particle stability with a greater negative charge and with hydrogen bonding with the carbamazepine carboxamide groups.49 It is widely recognized that CNT functional groups significantly affect adsorption properties.50 However, few studies have further connected the adsorption properties of CNTs to their impact on the bioaccumulation of co-existing contaminants. In this study, cCNTs had a higher capacity for carbamazepine adsorption and exhibited a significantly greater suppression effect on total carbamazepine bioaccumulation as compared to pCNTs.
With adsorption and uptake data considered collectively, the carbamazepine concentrations in leaf and total plants were decreasing with increasing adsorption capacity of the carbon materials; meaning that the suppression effect in uptake correlated well with the carbon material adsorption capacity. This finding does not align with some published assertions that CNTs could enhance the uptake of adsorbed secondary contaminants.15 As reported in a similar hydroponic co-exposure test, phenanthrene was accumulated in wheat roots more quickly in the presence of CNTs, likely resulting from nanomaterial-induced physical damage to the cell wall.15 It was clear in the current study that CNTs-bound carbamazepine was carried to the root surface upon tube deposition. Consequently, the carbamazepine was more accessible to the root tissue. However, the tertiary interactions between plant root, CNTs and carbamazepine did not lead to a higher in planta accumulation of the residue. In fact, as noted above, the CNTs resulted in reduced leaf and overall carbamazepine content. The lack of effective CNT transport out of the roots is not surprising and has been noted previously; Larue et al. reported a transfer factor of radio labelled-CNTs in wheat and rapeseed as low as 4.7 × 10−6.51 Furthermore, Lin et al. investigated the accumulation NOM-coated CNTs in rice and noted minimal translocation to aerial tissues.26 Although the current study did not include an assessment of in planta CNT content, indirect results with carbamazepine transport suggest minimal potential. Instead of CNTs penetrating and introducing carbamazepine into plants, greater amounts of the pharmaceutical seem to be retained in the growth media or on root surfaces through adsorption on to CNTs. Notably, the increased retention of carbamazepine in the root tissues could have significant food safety implications for crops with edible tubers or other similar tissues.
While leaf and total carbamazepine content could be related to the adsorption capacities, the root carbamazepine concentration was more likely to be affected by the dispersion and sedimentation of carbon materials. In comparing the root carbamazepine concentrations, it is clear that the more effectively dispersed cCNTs yielded less carbamazepine onto the plant root surfaces than pCNTs did. In control roots exposed to carbamazepine alone, surfactant washing removed roughly 18% of the root carbamazepine (Fig. 3). In the presence of the nanotubes, the results show that a relatively large proportion of carbamazepine detected in roots could be rinsed off by SDBS with sonication; 80.6% and 75.5% from pCNTs and cCNT, respectively. There was no statistical difference in surfactant removal efficiencies between pCNTs and cCNTs treatment, but any tube-specific effects may have been masked by the different initial root carbamazepine concentrations (initial root carbamazepine from pCNTs was roughly two times of that from cCNTs). However, as mentioned above, the presence of CNTs did increase the un-removable fraction of carbamazepine in the root (P < 0.05), which may suggest that more of the residue was incorporated into root cells in the presence of the nanotubes. Although the mechanism of this increased retention is unknown, it is possible that cell wall pores were pierced or physically damaged by CNTs presence; evaluating these processes is a topic in need of additional study. In summary, it is clear that under hydroponic conditions, co-exposure to carbon materials significantly altered the fate of carbamazepine in B. oleracea.
Comparisons within the two types of CNTs showed that the pCNTs co-exposure resulted in 34% higher carbamazepine root uptake (μg) than cCNTs co-exposure. This difference is attributable to the higher adsorption capacity resulting from CNTs functionalization. Notably, Hamdi et al. also reported that the presence of CNTs significantly lowered pesticide (chlordane and p,p′-DDE) availability to Lactuca sativa L. (lettuce) seedlings.52 Specifically, the authors noted that amino-functionalized CNTs had a lower adsorption capability for pesticides than non-functionalized CNTs and consequently resulted in significantly greater levels of pesticide residues in lettuce roots and shoots.52 In this study, evidence from adsorption experiment showed that carbon materials with a higher adsorption capacity would present a greater suppression effect in carbamazepine uptake and result in a lower carbamazepine accumulation in planta.
The difference between pCNTs and cCNTs from soil-grown conditions was less significant than observed in the hydroponic experiment. However, the pCNTs and cCNTs modified the in planta distribution of contaminant differently. The presence of cCNT in soil resulted in a statistically greater root to leaf TF (11.7) than the carbon-free control (8.7), pCNTs (8.5) and AC (7.7) (Table S1†). Interestingly, in the hydroponic exposure, the cCNTs co-exposure resulted in the highest carbamazepine TF across all carbon materials. When co-exposed with functionalized cCNTs, carbamazepine had a greater potential to translocate to edible leaf tissues while pCNTs co-exposure tend to retain carbamazepine in the root tissues. Although overall carbamazepine content was suppressed by cCNTs, a potential food safety risks remains in consuming the contaminated leaf tissues. The difference between pristine and functionalized CNTs lead us to hypothesize that surface modification of CNTs may enhance the biocompatibility of CNTs and promote the mobility of the contaminant within the plant. The finding that cCNTs enhanced carbamazepine transfer factors while suppressing overall accumulation demonstrates that the complex nature of interactions of CNTs with coexistent contaminants. Further investigation is required to develop a mechanistic understanding of the interactions and to evaluate the risk to food safety.
Considering data from both hydroponic and soil exposures, carbon amendment into soil generally decreased the availability of carbamazepine and the degree of suppression was directly related to the adsorption properties of carbon materials. There are numerous studies reporting that activated carbon or biochar amendment decreases the mobility and bioavailability of contaminants in soil or sediments, including inorganic heavy metals (Zn, Cd) and hydrophobic organic compounds (PCB, DDT and PAHs).53–55 However, a comparison between conventional AC and carbon nanomaterials is less common, and the available literature on the effect nanomaterial presence on contaminant bioaccumulation is rather limited. With a lower adsorption capacity than AC, CNTs in this study were less effective at crop protection in the presence of the pharmaceutical residue. However, the adsorption capacity of AC is highly dependent on the production/activation process and the specific co-contaminant; CNTs may be more versatile with surface modification and improved adsorption properties, even though AC currently has a significant lower manufacturing cost than CNTs. A number of studies have focused on the concurrent exposure of nanomaterials and contaminants, although there was no use of activated carbon as a control. De La Torre-Roche et al. reported that pristine CNTs co-exposure at 500 mg kg−1 in soil did not affect weathered DDx (DDT + metabolites) and chlordane bioaccumulation in species including C. pepo (zucchini), Zea mays (corn), Glycine max (soybean) and Solanum lycopersicum (tomato), but that exposure to 1000 mg kg−1 or higher did significantly decrease contaminant uptake.16 As mentioned above, Hamdi et al. also reported that both non-functionalized and amino-functionalized CNTs lowered chlordane and p,p′-DDE accumulation but that the amino-functionalized tubes produced a more modest suppression effect.52 Conversely, carbon in the form of C60 has been shown to enhance contaminant bioaccumulation under certain conditions, including chlordane in soil-grown tomato and soybean, DDx in soil-grown zucchini and trichloroethylene in hydroponic poplar.16,56,57 In reviewing the literature, it is clear that the effect of carbon nanomaterials on the uptake of co-existing contaminants is highly variable, and the key factors of exposure concentration, plant species and nanomaterial type/surface chemistry ultimately control bioaccumulation. With interactions specifically involving CNTs, suppression of contaminant uptake in soil exposure with CNTs would be reasonably expected, and mechanistically, functionalization would alleviate or intensify the suppression effect based on the adsorption capacity of the particular contaminant. In environmentally relevant scenarios such as soil, the movement of CNTs was low; the contaminants bound to CNTs were more likely to remain ex planta through adsorption. The bioaccumulation of coexistent contaminant was therefore suppressed due to the actual decreased exposure concentrations. Furthermore, it is worth noting that functionalization of CNTs with COOH significantly improved the in planta translocation of co-existing contaminant in soil, although the mechanism remains unknown.
Overall, this study evaluated B. oleracea growth under a range of co-exposure conditions and quantified the bioaccumulation of carbamazepine in the presence of CNTs and AC, addressing concerns that carbon nanotubes may affect the bioaccumulation of secondary contaminants. With regard to plant growth, the inhibition of plant biomass production was dependent on carbamazepine concentrations in hydroponic conditions, while exposure to 50 mg L−1 cCNTs alone enhanced the plant growth. Suppression of carbamazepine uptake in the presence of carbon materials was observed in both hydroponic and soil conditions, which was likely due to the lowered actual carbamazepine exposure concentration after adsorption to the carbon material and retention in growth media. The extent of suppression was correlated with the adsorption capacities of carbon materials. Interestingly, COOH-functionalized CNTs affected plant carbamazepine uptake and distribution differently from its pristine analog, through enhanced adsorption capacity, better dispersion stability, and possibly increased biocompatibility. With elevated transfer factors, the carboxylated nanotubes demonstrated the potential ability to facilitate xylem-based transport of carbamazepine. Our findings demonstrate that the accumulation and distribution of pharmaceutical residues in crops varies greatly with exposure condition and the type and surface functionalization of carbon materials. In addition, the results presented in this study have significant implications for the use of carbon materials in agriculture and towards efforts to ensure crop protection and food safety.
Footnote |
† Electronic supplementary information (ESI) available. See DOI: 10.1039/c6en00419a |
This journal is © The Royal Society of Chemistry 2017 |