Environ. Sci. Technol. 2005, 39, 8369-8373
Sorption of Aromatic Organic Pollutants to Grasses from Water JASON P. BARBOUR,† J A M E S A . S M I T H , * ,† A N D CARY T. CHIOU‡ Department of Civil Engineering, University of Virginia, P.O. Box 400742, Charlottesville, Virginia 22904-4742, and U.S. Geological Survey, Box 25046, Mail Stop 408, Denver Federal Center, Denver, Colorado 80225
The influence of plant lipids on the equilibrium sorption of three aromatic solutes from water was studied. The plantwater sorption isotherms of benzene, 1,2-dichlorobenzene, and phenanthrene were measured over a large range of solute concentrations using sealed vessels containing water, dried plant material, and solute. The plant materials studied include the shoots of annual rye, tall fescue, red fescue, and spinach as well as the roots of annual rye. Seven out of eight sorption isotherms were linear with no evidence of competitive effects between the solutes. For a given plant type, the sorption coefficient increased with decreasing solute water solubility. For a given solute, sorption increased with increasing plant lipid content. The estimated lipid-water partition coefficients of individual solutes were found to be significantly greater than the corresponding octanol-water partition coefficients. This indicates that plant lipids are a more effective partition solvent than octanol for the studied aromatic compounds. As expected, the solute lipid-water partition coefficients were log-linearly related to the respective water solubilities. For the compounds studied, partitioning into the lipids is believed to be the primary sorption mechanism.
Introduction The contamination of soil and subsurface water by petroleum hydrocarbons, industrial chemicals, and pesticides can result in subsequent plant contamination. Pollutants enter the plants through the root system and can be translocated to other parts of the plant, causing a potential human health risk if the plants are used for foods. Interest in this topic has increased in recent years as scientists and engineers have proposed using plants to remediate shallow soil, wetlands, stormwater runoff, and groundwater systems (e.g., phytoremediation) (1-9) and to document groundwater contamination (10, 11). Pollutant uptake by plants occurs by passive and/or active transport (12). Active transport proceeds in a direction that opposes the chemical potential gradient and is typically caused by metabolic energy requirements that cause nutrient cations to penetrate plant membranes (12, 13). Passive transport proceeds in the direction of the chemical potential gradient (13). With the exception of a few chemicals that mimic natural hormones (e.g., 2,4-dichlorophenoxyacetic * Corresponding author phone: (434) 924-7991; fax: (434) 9822951; e-mail:
[email protected]. † University of Virginia. ‡ U.S. Geological Survey. 10.1021/es0504946 CCC: $30.25 Published on Web 09/30/2005
2005 American Chemical Society
acid (14)), there is no evidence of active transport of anthropogenic organic compounds by plants as the pollutant moves through the epidermis and into the plant’s vascular system (12). For passive transport of poorly water soluble organic compounds, it has been noted that the single most important plant characteristic is the plant lipid content (3, 12-20). Organic solutes in water enter the plant through root hairs and then pass through the permeable cortex cell walls and the capillary void spaces between cortex cells (12). Water and organic solutes must then pass through the Casparian strip, which is a waxy (lipid) material that is formed around the anticlinal walls of specialized endodermis cells (12). After crossing the Casparian strip, water and solutes are transported to the stems and leaves via the plant’s vascular system (e.g., the xylem and phloem) by a fluid potential gradient (12). Water and solute that are not metabolized or sequestered by the plant are eventually released to the atmosphere through stomatal pores on the leaves (21). During transport through the plant, some organic solutes partition into plant lipids and other components, thereby retarding their transport through the plant. Despite the recognized importance of plant lipids in the uptake and accumulation of organic solutes by plants, there are relatively few studies that have attempted to correlate pollutant uptake to plant lipid content or to determine experimentally if lipid-water partitioning is the primary sorption mechanism. Previous studies on the equilibrium sorption of organic solutes to plants have typically been completed by adding plant, water, and pollutant to a sealed reactor and allowing sufficient time for equilibration. For example, Briggs et al. (15, 16) studied the uptake of O-methylcarbamoyloximes and substituted ureas by dried, macerated roots and shoots of barley. Burken and Schnoor (3) investigated the sorption of 12 organic pollutants to fresh, whole poplar roots. Trapp et al. (22) studied the sorption of 10 organic compounds to dried splints derived from common oak (Quercus robur) and basket willow (Salix viminalis) branches. All aforementioned studies investigated only one concentration level of target compounds with no attempt to correlate the sorption capacity with plant composition. Chaumat et al. (23) studied the sorption of three herbicides to isolated plant cuticles and presented both lipid contents and multipoint sorption isotherms. Although not specifically highlighted, there was an apparent positive correlation between the partition coefficients and the total lipid contents in this study. A study of aquatic plants and algae by Nzengung et al. (24) also used multipoint isotherms, but did not incorporate plant lipid content data. Whereas the influence of lipids on plant uptake of organic compounds has yet to be more thoroughly investigated, studies by Barak et al. (25) and Mackay and Gshwend (26) have shown a positive relation between sorption and lignin content. The present study investigates the equilibrium sorption of three sparingly soluble aromatic compounds to three species of grass. The results are evaluated in terms of the lipophilicity of the compound and the composition of the plant.
Experimental Section Materials. Three aromatic hydrocarbons were chosen for this investigation to span a range of water solubilities: benzene (log Sw ) 3.25 mg/L) (27), 1,2-dichlorobenzene (2.18) (28), and phenanthrene (0.773) (29). [14C]Benzene and [14C]phenanthrene were obtained from Moravek Biochemicals, and [14C]-1,2- dichlorobenzene was obtained from SigmaAldrich. The unlabeled benzene (purity >99%), 1,2-dichloVOL. 39, NO. 21, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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robenzene (>99%), and phenanthrene (>98%) were obtained from Sigma-Aldrich. Benzene and 1,2-dichlorobenzene were added directly to water to establish the desired concentrations. Phenanthrene was dissolved in methanol and added to water such that the methanol mole fraction in water was less than 2 × 10-3. Previous research has shown cosolvency effects are negligible at these concentrations (3, 30). Plants used in the lipid quantification and sorption studies were annual rye (Lolium multiflorum Lam.), tall fescue (Lolium arundinaceium), and red fescue (Festuca rubra L.). The grass seeds were purchased from a local farm supply store. Baby spinach (Spinacia oleracea) was also tested to provide a specimen of intermediate lipid content. Iceberg lettuce (Lactuca sativa) and chives (Allium schoenoprasum) were used during the verification of the lipid extraction procedure. The spinach, lettuce, and chives were purchased from a local grocer. Lipid Quantification. Except as noted above, plants were grown hydroponically with 3 mm glass beads as the growth media for a period of 2 weeks. A feed solution containing 0.5 mL of Scott’s Miracle-Gro all-purpose plant food/L of water was circulated through the growth media at a rate of 2.5 mL/min. The seeds were sown at a density of approximately 7 seeds/cm2 and received 12 h of light per day from Sylvania Gro-Lux lighting. Plants were carefully removed from the growth media, separated into root, shoot, and seed components, and weighed. The root and shoot materials were then frozen at the temperature of liquid nitrogen (77 K), dried for 24 h in a vacuum chamber, and reweighed to determine the moisture content. The dried roots and shoots were then ground (separately), and 0.3-0.5 g samples were placed in 15 mL centrifuge tubes filled with 2:1 (v/v) chloroform/methanol. The tubes were placed on an orbital shaker at 200 rpm for 10 min, followed by centrifugation at 2000 rpm for 10 min. The supernatant was then filtered through Whatman no. 1 filter paper. The plant material was extracted twice more in this manner. The combined extract was then evaporated under a stream of liquid nitrogen and weighed. Finally, the lipid material was removed from the tubes by two sequential chloroform extractions. The tubes were reweighed, and the mass of lipids was determined by difference. All lipid analyses were performed in triplicate. This procedure used the same principles employed in other common extraction methods (31-35) and was verified with two plants (iceberg lettuce and chives) listed in the U.S. Department of Agriculture Nutrient Database (36). This procedure does not quantify lipids or lipid-like materials that are not chloroform-soluble. Sorption Studies. Varying amounts of freeze-dried plant material, water, and 14C-labeled solute were combined in 8.4 or 15.8 mL glass centrifuge tubes with Teflon-lined caps. The mass of plant used was approximately 0.4 g for benzene, 0.1 g for DCB, and 0.005 g for phenanthrene; these masses were chosen to allow between 25% and 75% of the added solute to be sorbed at equilibrium. The initial solute concentrations were 15.2-1042 mg/L for benzene, 12-123 mg/L for DCB, and 0.11-1.55 mg/L for phenanthrene. Water volumes were chosen to minimize headspace in each batch study and were approximately 8 mL for the 8.4 mL tubes and 14.2 mL for the 15.8 mL tubes. The organic solute concentration was assayed using a Packard 1900TR liquid scintillation analyzer. Measurement of the initial and final solute concentrations in the water phase allowed calculation of the solute concentration in the plant phase. For select experiments, the water and plant phases were both analyzed to complete a mass balance and ensure that the “difference” method was justified. For each isotherm experiment, blank and background reactors were prepared for quality assurance. Blank reactors contained solute and water, but no plant material, and were used to 8370
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TABLE 1. Plant Composition Data for Plant Materials Used in the Batch Sorption Studies plant part
water content, %
lipid content, lipid content, fresh basis, % dry basis, %
annual rye roots annual rye shoots tall fescue shoots red fescue shoots baby spinach shoots
93.8 ( 0.6 92.9 ( 0.3 90.7 ( 0.2 88.9 ( 0.2 89.8 ( 0.6
0.13 ( 0.003 0.56 ( 0.020 0.62 ( 0.033 0.85 ( 0.074 0.54 ( 0.022
2.2 ( 0.04 7.9 ( 0.28 6.7 ( 0.36 7.7 ( 0.67 5.3 ( 0.21
FIGURE 1. Lipid content (dry basis) of annual rye shoots as a function of time for whole shoots and for the lowest 8 cm of the shoots. Error bars represent the standard deviation of three replicates. measure losses. Background reactors contained plant and water, but no solute, and were used to detect background radiation and/or contamination. Kinetic sorption experiments were completed to determine the time required for equilibrium studies. Organic solute concentrations in a subset of water samples for each solute/plant combination were also quantified by gas chromatography to confirm that no transformation of the compound had occurred. It was assumed that any degradation products formed in the plant would be in equilibrium with the water and could be detected in this manner. Sorption data were analyzed using the IsoFit software developed at the University of Buffalo. The data were fit to linear, Freundlich, and Langmuir isotherms using uniform weighting.
Results The lipid content (fresh basis) of iceberg lettuce was determined to be 0.11 ( 0.003%, in agreement with the reported value of 0.11 ( 0.026% (based on eight reported values) in the USDA Nutrient Database (36). For chives, the lipid content was determined to be 0.61 ( 0.001%, versus the reported value of 0.73 ( 0.11% (based on three reported values). The ages of the chives in our test and those reported by the USDA are unknown, but it is possible that age differences contributed to the observed variability. The grass plants germinated within 3-4 d and showed no signs of decreasing plant density, leaf abscission, or chlorosis at the time of harvest. Plants randomly selected 2 weeks after sowing had average shoot heights of 6.9, 8.9, and 14.1 cm for red fescue, tall fescue, and annual rye, respectively. Annual rye shoots attained an average height of 19.7 cm at 4 weeks and 36.0 cm at 6 weeks. The water content of the shoots varied from 88.9% to 92.9%, while the lipid content (dry basis) varied from 6.7% to 7.9% (Table 1). For annual rye roots, the water content was 93.8 ( 0.6% while the lipid content (dry basis) was 2.2 ( 0.04%. There was little difference between the lipid contents of the grass shoots, when compared on a dry basis (Table 1). However, the roots of annual rye were shown to have a lipid content one-fourth that of shoots of the same age and plant type. The lipid content (dry basis) of annual rye shoots decreased with age (Figure 1). However, when only the lowest 8 cm of the shoots was tested, the lipid
FIGURE 2. Equilibration of phenanthrene with the shoots of annual rye. Error bars represent the standard deviation of three replicates. content was approximately constant, with some inconsistency among the 4 week samples. Kinetic plant sorption results for 1,2-dichlorobenzene and phenanthrene (Figure 2) were similar, reaching equilibrium in 12-24 h, while the benzene uptake reached equilibrium within the first hour. A 24 h equilibration time for plant sorption experiments is consistent with that of previous work (23, 24). Recovery from blanks was, on average, 96%. Background reactors did not show any radioactivity above that of normal background radiation. Mass balances, where the solute concentrations in the plant and water phases were analyzed, showed recoveries greater than 94%. A series of sorption isotherms for the above three compounds onto the roots and shoots of annual rye are approximately linear over the range of concentrations studied (Figure 3 and Table 2). In Figure 3, each data point represents a single experiment, with the open circles indicating tests for a single solute while closed circles represent tests in the presence of unlabeled 1,2-dichlorobenzene (at equilibrium water concentrations of 56 and 35 mg/L for the benzene and phenanthrene experiments, respectively). Sorption of 1,2-dichlorobenzene was tested for a variety of plant materials (Table 2). The resulting partition coefficients (the slope of the best-fit line relating plant concentration to water concentration) were plotted as a function of the lipid content (dry basis) (Figure 4). The uncertainty in the sorption data is expressed as the standard error in the slope (Table 2 and Figure 4), as determined through the IsoFit analysis, based on 10-26 data points for each solute/plant combination.
Discussion Analysis of the data indicates that lipid-water partitioning is the predominant uptake mechanism of these three aromatic compounds. This finding is supported by several experimental results. The first observation that supports lipid-water partitioning is the linearity and magnitude of the sorption of the three solutes to annual rye (Figure 3) and other plants for the range of concentrations studied. The uptake of benzene by annual rye roots was extremely weak, and we were unable to obtain meaningful equilibrium data for this system. The remaining eight pollutant/plant combinations (Table 2) were fitted to linear, Langmuir, and Freundlich isotherms and compared on the basis of rootmean-squared error. A Langmuir isotherm was the best fit for the sorption of phenanthrene to annual rye roots, while a linear isotherm provided the best fit for the other seven sets of data. The absence of competitive effects is further evidence that uptake is occurring by partition. The sorption data for benzene to annual rye shoots with and without 1,2-dichlorobenzene present were analyzed with multiple regression analysis using a dummy variable (39). This analysis indicates that single and binary solute benzene sorption isotherms are not statistically different (p ) 0.25). Single and binary solute phenanthrene sorption isotherms to annual rye shoots are also not statistically different (p ) 0.10).
FIGURE 3. Sorption of (a) benzene, (b) 1,2-dichlorobenzene, and (c) phenanthrene to roots and shoots of annual rye. Each data point represents results from a single batch reactor. Two additional observations indicate lipid-water partitioning as the primary uptake mechanism. There is a positive correlation between the lipid contents of the plants and the plant-water partition coefficients for 1,2-dichlorobenzene (Figure 4). Finally, the partition coefficients for annual rye shoots increased inversely with the solute aqueous solubility (Table 2). In summary, the uptake magnitude, linear and noncompetitive sorption, and the relation between sorption and solute solubility and lipid content are strong evidence that lipid-water partitioning is the primary uptake mechanism for these compounds by nonliving plants. Given the importance of lipid-water partitioning in the uptake of organic solutes by plants, it is useful to calculate the value of lipid-water partition coefficients on the basis of the experimental sorption data collected in this study. The lipid-water partition coefficient, Klip, was calculated for each solute/plant combination using the following relation from Chiou et al. (13), simplified for dried plant samples:
Cpt/Cw ) fchKch + flipKlip
(1)
In eq 1, Cpt is the concentration of pollutant in the plant (mg of pollutant/kg of plant) and Cw is the concentration of pollutant in water (mg of pollutant/kg of water). The ratio VOL. 39, NO. 21, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Reference Values for the Octanol-Water Partition Coefficient and Solubility (Source Shown in Parentheses), Experimental Values (with Standard Errors from IsoFit for Cpt/Cw Values) and Goodness of Fit (R2) for the Plant-Water Partition Coefficient (Cpt/Cw) of Each Pollutant/Plant System, and the Calculated Value of the Lipid-Water Partition Coefficient [log(Klip)] for Each System compd
log(Kow)
log(Sw)
benzene 1,2-DCB
2.13 (37) 3.38 (37)
3.25 (27) 2.19 (28)
phenanthrene
4.46 (38)
0.773a (29)
a
plant
part
Cpt/Cw
R2
log(Klip)
annual rye annual rye annual rye tall fescue red fescue spinach annual rye annual rye
shoots shoots roots shoots shoots shoots shoots roots
22.5 ( 2.1 259 ( 5 105 ( 1 261 ( 4 257 ( 5 208 ( 8 4601 ( 105 1988 ( 27
0.89 0.99 0.71 0.99 0.98 0.93 0.97 0.99
2.44 3.51 3.67 3.53 3.58 3.59 4.76 4.96
The log(Sw) value for phenanthrene is that of the supercooled liquid.
FIGURE 4. Plant-water partition coefficients (slopes of sorption isotherms) for 1,2-dichlorobenzene to various plants plotted as a function of lipid content (dry basis). Cpt/Cw is equivalent to the slope of the corresponding sorption isotherm (Table 2). The lipid fraction, flip, was measured (Table 1), with the carbohydrate fraction, fch, constituting the remainder of the dried plant material. The values of the carbohydrate-water partition coefficient, Kch, used in eq 1 were assumed to be 1, 2, and 3 for benzene, 1,2-dichlorobenzene, and phenanthrene, respectively, on the basis of the guidelines set forth in Chiou et al. (13). The Kch values are approximations based on data for cellulose, but the effect of these estimations is small for hydrophobic solutes, as demonstrated by the following equation:
% pollutant stored in lipids ) flipKlip/(fchKch + flipKlip) × 100 (2) Using the plant composition data and partition coefficients described above (Tables 1 and 2), it can be shown that, even though lipids make up a small fraction of the plant mass (2.2-7.9%), they can account for 95.9% (benzene) to 99.9% (phenanthrene) of the solute storage capacity of the dry plant. The lipid-water partition coefficients calculated using the measured lipid contents and the slopes of the sorption isotherms are, on average, approximately twice as large as the corresponding octanol-water partition coefficients. The lipid-water partition coefficients and octanol-water partition coefficients exhibit similar relations to solute solubility (Figure 5). On the basis of the data for 1,2-dichlorobenzene and phenanthrene, the root lipids may be more hydrophobic than the shoot lipids. The results of this study suggest that the lipid materials in these plants are, on average, more hydrophobic than octanol. Prior work by Chiou et al. (40) supports this observation. Chiou et al. (40) used triolein as a model lipid and experimentally quantified triolein-water partition coefficients, Ktw, for benzene and 1,2-dichlorobenzene (Table 3). The triolein-water partition coefficient for phenanthrene, 8372
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FIGURE 5. Relation between the experimentally derived values for the lipid-water partition coefficients and the water solubilities of benzene, 1,2-dichlorobenzene, and phenanthrene. Literature values were used for the octanol-water partition coefficients and solubilities (Table 2).
TABLE 3. Literature Values of Octanol-Water and Triolein-Water Partition Coefficients and Averages of Measured Values of the Lipid-Water Partition Coefficientsa compd
log(Kow)
log(Ktw)
log(Klip)
benzene 1,2- dichlorobenzene phenanthrene
2.13 (37) 3.38 (37) 4.46 (38)
2.25 (40) 3.51 (40) 4.84b (40)
2.44 3.58 4.86
a References for literature values are shown in parentheses. b The triolein-water partition coefficient for phenanthrene was estimated on the basis of the regression equation of log(Ktw) and log(Sw) (40).
reported in Table 3, was estimated using the regression equation of log(Ktw) and log(Sw) (40). The Klip values show relatively good agreement with the Ktw values, suggesting that triolein-water partition coefficients provide better estimates of lipid-water partitioning than Kow values. Although performed with dried plants, this study also has implications for uptake of solutes by living plants. As described in the Introduction, solute uptake by living plants is more complicated than the uptake by nonliving plants. In living plants, solutes must pass through the Casparian strip before entering the vascular system and may be metabolized, sequestered, or released to the atmosphere. However, it is likely that the equilibrium distribution of solute in living plants is at least partially controlled by partitioning that occurs between the transpiration stream and the lipid reservoirs of the plant. Indeed, several plant uptake models (13, 41, 42) use the Kow to estimate equilibrium uptake of pollutants by plants. It seems reasonable to use the Kow as a first approximation. However, for the aromatic hydrocarbons in
this study, it may be more accurate to use the lipid-water partition coefficient (or, alternatively, the triolein-water partition coefficient). The lipid-water partition coefficients derived herein may not be applicable to plants that differ significantly from those used in this study as there may be differences between the nature of the lipids from one plant type to the next. Further testing is required to determine the variability of the lipid behavior with plant type. Additionally, long-term uptake experiments are needed to determine the relation between the equilibrium sorption to nonliving plants and the equilibrium uptake of a solute through the roots of a living plant.
Acknowledgments Support for this research was provided by the Department of Education and the U.S. Geological Survey. We thank J. Buckels and T. Wenk for assistance in the early stages of this investigation. The use of trade, brand, or product names in this paper is for identification purposes only and does not imply endorsement by the U.S. Government.
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Received for review March 14, 2005. Revised manuscript received July 11, 2005. Accepted August 25, 2005. ES0504946 VOL. 39, NO. 21, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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