Uptake of perfluorooctane sulfonate (PFOS) by wheat (Triticum aestivum L.) plant

Chemosphere 91 (2013) 139–144

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Uptake of perfluorooctane sulfonate (PFOS) by wheat (Triticum aestivum L.) plant Hongxia Zhao ⇑, Yue Guan, Guolong Zhang, Zhou Zhang, Feng Tan, Xie Quan, Jingwen Chen Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Environmental Science and Technology, Dalian University of Technology, Linggong Road 2, Dalian 116024, China

h i g h l i g h t s " We study uptake kinetics of PFOS by wheat (Triticum aestivum L.) seedlings. " We examine the effect of environmental factors on PFOS uptake. " Increasing salinity, temperature and concentration will increase PFOS uptake. " The maximum PFOS uptake is found at pH = 6 with pH increasing from 4 to 10.

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Article history: Received 9 October 2011 Received in revised form 12 October 2012 Accepted 13 November 2012 Available online 11 December 2012 Keywords: Perfluorooctane sulfonate (PFOS) Plant uptake Wheat (Triticum aestivum L.) Environmental factors

a b s t r a c t Perfluorooctane sulfonate (PFOS) is a highly persistent organic pollutant which has raised many concerns in recent years. Research focusing on plant uptake of PFOS is very necessary when considering its risk of transfer from soil into food chain. In this work, the uptake of PFOS by wheat (Triticum aestivum L.) which is the most main food crop in northern China, was studied. To predict the kinetic uptake limit, the partition-dominated equilibrium sorption of PFOS by roots of wheat was determined. The uptake of PFOS from water at a fixed concentration (1 lg mL1) increased with exposure time in approach to steady states and the observed uptake was lower than its limit, due presumably to the PFOS dissipation in wheat. The influences of the environmental factors on plant uptake of PFOS were investigated. The concentrations of PFOS measured in the plant compartments increased with increasing salinity (0.03– 7.25 psu), temperature (20–30 °C) and concentration (0.1–100 mg L1) at the ranges tested, whereas the maximum uptake of PFOS was found at pH = 6 with increasing pH from 4 to 10. In addition, in all of the cases, the average levels of PFOS detected in the roots were higher than those in the shoots. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction Perfluorooctane sulfonate (PFOS) is a manmade persistent organic contaminant used for decades in industry worldwide due to its high degree of chemical stability (Kissa et al., 2001; Magali et al., 2006). When released in the environment, PFOS can enter soil, water and atmosphere and bioaccumulate in the food chains. At present, PFOS has been found in a wide range of environmental and biological samples including soils, sediments, snow, water, birds, edible marine organisms, marine mammals and human beings (Hoff et al., 2005; Olsen et al., 2005; Haukås et al., 2007; Higgins et al., 2007; Kelly et al., 2009; Delinsky et al., 2010; Schecter et al., 2010; Kirsten et al., 2011; Sarah et al., 2012). The chronic toxicity studies show that PFOS can increase liver triglyceride and cholesterol levels, decrease serum cholesterol, cause hypolipide-

⇑ Corresponding author. Tel./fax: +86 411 84707965. E-mail address: [email protected] (H. Zhao). 0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.11.036

mia, and reduce food consumption in cynomolgus monkeys (Butenhoff et al., 2002, 2009; Lau et al., 2007). Additionally, PFOS is also found to result in development toxicity, hepatotoxicity, immunotoxicity or neurotoxicity in mammals (Butenhoff et al., 2009; Qazi et al., 2010; Ribes et al., 2010; Bogdanska et al., 2011). Owing to its ubiquity in the environment and these potential adverse effects on organism, PFOS has raised growing concerns in recent years. It is well known that plant uptake is an important step for the transfer of toxic contaminants into the terrestrial food chain/web (Travis and Arms, 1988; Jones et al., 1991; Dowdy and McKone, 1997; Thomas et al., 1999), which may pose great threats to ecological and human health. The degree of organic contaminant uptake is usually affected by the physico-chemical properties such as octanol–water partitioning coefficients (Kow). Highly lipophilic contaminants with Kow > 3 log unit have a high tendency to be absorbed by plant roots from water. Good log–log linear relationships have been established between the root concentration factors (RCFs) and log Kow and are commonly used to estimate the equilibrium distribution of organic contaminants in water-plant systems

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(Briggs et al., 1982, 1983; Burken and Schnoor, 1998; Turgut, 2005). However, Kow is not an appropriate parameter for PFOS due to its intrinsic amphiphilic nature (Hites et al., 2006). Furthermore, accurate value for Kow of PFOS is still not available. Therefore, it is necessary to use laboratory studies involving plant exposure models to assess plant uptake of PFOS. To the best of our knowledge, little information is hitherto available on plant uptake of PFOS except for a recent report that PFOS entered plants from contaminated soils by a concentrationdependent manner (Stahl et al., 2009; Lechner and Knapp, 2011). There is still a lack of experimental data to elucidate rate of plant uptake and the effect of environmental factor on plant uptake of PFOS. Thus, the objectives of this study were to examine (1) the equilibrium sorption of PFOS from water into roots of wheat seedlings; (2) the kinetic uptake of PFOS by roots and shoots of wheat seedlings; and (3) the effect of pH, salinity, temperature and concentration on PFOS uptake in wheat seedlings.

2.4. Plant uptake kinetics Plant uptake from water was conducted under the lighting conditions described above. An apparatus was setup based on previous studies with minor modification (Li et al., 2002, 2005) (see Fig. 1), As shown in Fig. 1, a pump continuously transferred the fresh solution from a reservoir to the grid at a flow of 1 mL min1; A group of 50 seedlings were allowed to grow through the 2.2 cm holes on the polymethyl pentene cover. The grid contained the half-strength Hoagland solution, with roots below the cover and immersed in the solution. The setting not only maintained a constant solute concentration in the grid solution, but also prevented the direct loss of aqueous phase solute to the air and thus minimized foliar uptake from the ambient air. The solute concentrations in the Hoagland solution were constantly monitored throughout the experimental periods. Plant samples were taken in triplicate for solute analysis. 2.5. Sample extraction and analysis

2. Materials and methods 2.1. Materials PFOS (>98% purity) was purchased from Fluka (Steinheim, Switzerland). The stock solutions of testing chemicals were prepared in the deionized water from a Milli-Q water purification system (Millipore, Milford, MA) using polymethyl pentene containers. All reagents used in this study were analytical grade. The variety of tested wheat (Triticum aestivum L.) was Liaoning Spring No. 10, which wheat seeds were obtained from the Liaoning Dongya Seed Co., in Shenyang, China.

2.2. Plant culture and treatment Wheat seeds were sterilized with 5% sodium hypochlorite solution for 10 min and then thoroughly washed with distilled water. After the wheat seeds were germinated on wet filter paper for 7 d, the seedlings were transferred to 1 L glass beakers containing half-strength Hoagland’s solution (Lin and Xing, 2008) for further growth. The seedlings grew in the laboratory at temperature 25 ± 0.2 °C. Light was supplied by sets of 40-W fluorescent tubes. The lighting period was set at 16 h d1. When their roots reached 12 ± 1 cm, and leaves grew 9 ± 1 cm, these seedlings were used for further uptake experiments.

2.3. Sorption experiment Sorption of PFOS by roots of fresh wheat seedlings from water was measured using the batch equilibration technique at 25 ± 1 °C. A series of organic solute solutions with a range of initial concentrations were prepared using a half-strength Hoagland solution as the matrix. The chopped fresh roots (1–2 mm in size) were weighed into glass centrifuge tubes; the initial solutions were added. Tubes were then put in a shaker at 185 G for 8 h according to the kinetic study. The mass of plant used was approximately 0.4 g (fresh weight), which was chosen to allow between 25% and 75% of the added solute to be sorbed at equilibrium. The initial solute concentrations were 0.1, 0.2, 1, 2, 5, 10, 20 mg L1. Following the equilibration and subsequent 30 min sedimentation of plant material, the supernatant from each tube was analyzed for solute. The amount sorbed by the plant roots was calculated from the difference between the initial and final concentrations of the solute. The loss of solute from process other than sorption was found negligible.

The analytical procedure for the plant sample was similar to that described elsewhere with minor modifications (Pan et al., 2008; Shi et al., 2010). In brief, 0.1 g (fresh weight) of the homogenized total sample was put into a 10-mL polypropylene tube, then 1 mL of 170 g L1 tetrabutyl ammonium hydrogen sulfate solution and 2 mL of 26.5 g L1 sodium carbonate buffer were added for extraction. After thorough mixing, 4 mL of methyl-tert-butyl ether (MTBE) was added, and the mixture was shaken for 20 min. The organic and aqueous layers were separated by centrifugation (12 000g), and an exact volume of MTBE (3 mL) was transferred from the solution. The aqueous mixture was rinsed with MTBE and separated twice. The solvent was allowed to evaporate under nitrogen at about 50 °C before being reconstituted in 1.5 mL of methanol. The sample was vortexed for 30 s and passed through a 0.2 lm nylon mesh filter into an autosampler glass vial. Analyte separation was performed using an Agilent 1100 HPLC system (Agilent Technologies, Palo Alto, CA). Two ll of extract was injected onto a 2.1  100 mm (3.5 lm) Agilent Eclipse Plus C18 column (Agilent Technologies, Palo Alto, CA) with a 10 mM ammonium acetate/acetonitrile mobile phase starting at 40% acetonitrile at a flow rate of 0.3 mL min1, to 90% acetonitrile at 11 min before reverting to original conditions at 13 min. Column temperature was maintained at 40 °C. For quantitative determination, the HPLC system was interfaced to an Agilent 6410 Triple Quadrupole mass spectrometer (Agilent Technologies, Santa Clara, CA) operated with electrospray ionization (ESI) in negative mode. The gas temperature and ion spray voltage were maintained at 350 °C and 4000 V. Ions were monitored with a multiple reaction monitoring (MRM) mode, and the parameters for parent and product ions were 499, 99 and 80, and collision energies were 50 and 60 eV respectively. 2.6. Statistical analysis Statistical analysis was performed using the SPSS (version 13.0, SPSS Inc., 2004). A probability value p < 0.05 was thought as statistically significant. The statistical comparison of means between the different plant roots and leaves was done by a one-way analysis of covariance (ANCOVA). Means were expressed with their standard error (SE). All experiments were repeated three times. 3. Results and discussion 3.1. Sorption of PFOS by wheat roots Concentrations of PFOS detected in water (the half-strength Hoagland solution in this study) and plant samples are listed in

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(A) Experimental apparatus

(B) Profile

Fig. 1. The setup for kinetics study.

the supporting information (Table S1). Sorption of PFOS by roots of wheat seedlings from water is presented in Fig. S1, in which the sorbed amount by plant roots on fresh weight basis (mg kg1) was plotted against the equilibrium concentration (mg L1). The sorption isotherm was highly linear over the range of concentrations with correlation coefficient square greater than 0.99, indicating the predominant role of partition in sorption (Chiou et al., 1979, 1982, 2001). Based on the above result, the sorption model Qeq = CwKpw (Qeq is the concentration of solute in plant at the equilibrium concentration (Cw) and Kpw represents the plant-water partition coefficient) can be used to describe the PFOS root sorption and the corresponding relationship was obtained below:

Because of the linear characteristic of sorption isotherms, the plant-water partition coefficient of PFOS for root was acquired from the slopes of the corresponding sorption isotherm with Kpw = 4.18. 3.2. Uptake kinetics of PFOS by wheat The PFOS uptake by wheat seedlings as a function of exposure time was monitored using a continuous flow in which the solute concentration in water was kept constant. Such experimental apparatus was setup based on the previous studies (Li et al., 2002, 2005) with minor adjustment. This setup allowed one to observe the progression of the plant uptake toward a plateau by avoiding the complication caused by a change in solute concentration in water with time. In this system, the limiting solute uptake to a plant part at a fixed aqueous concentration can be equated theoretically with the determined sorption isotherm (Eq. (1)).With the defined uptake limits, the kinetic approach to the limits can be assessed in terms of the quasi-equilibrium factor (a) developed by Chiou et al. (2001).

Q t ¼ aQ eq

A

ð1Þ

ð2Þ

where Qt represents the uptake at the time of sampling. a is equal to the ratio of the kinetic uptake to the equilibrium limit and thus describes the actual approach to the limit. The condition that a = 1 denotes the state of uptake equilibrium. The data on PFOS uptakes by roots and shoots of wheat seedlings and calculated a values using sorption model are presented in Fig. 2. The PFOS uptake by wheat seedlings increased with exposure time. The root and shoot uptakes reached an apparent uptake plateau within 72 h. The concentrations of PFOS in roots were at least

Uptake dry weight (ug/kg)

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3.5 times higher than those in shoots. This difference was statistically confirmed by one-way analysis of covariance at p 6 0.05. In addition, Fig. 2 also implies that PFOS uptake did not exceed its limits defined by the sorption model and the calculated a lower than 1. Actually, most of the uptakes are lower than the limits. The exact reason for this was unclear. The dissipation process within plants was a possible reason (Burken and Schnoor, 1997; Trapp and Karlson, 2001). Previous studies have shown that some processes including foliar volatilization, solute metabolism in

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Time (h) Fig. 2. Uptake concentrations of (A) PFOS in roots and shoots of wheat seedlings as a function of exposure time, as well as their corresponding quasi-equilibrium factors (B) calculated from the sorption model.

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plants, formation of bound residues and plant-growth-induced dilution can effectively reduce the levels of foreign solutes in plants (Simonich and Hites, 1995; Burken and Schnoor, 1997; Newman et al., 1997; Bhadra et al., 1999a,b). 3.3. pH effect on PFOS uptake in wheat The uptake of ionizable compounds is very complicated and can be affected by many factors such as hydrophobicity, pKa and substrate pH (Briggs et al., 1987; Trapp, 2000). Here the effect of pH on PFOS uptake by wheat was investigated, as shown in Fig. 3. At a solution concentration of 1 mg L1, the PFOS uptake by roots and its subsequent translocation to shoots increased as the pH of the solution increased from 4 to 6, then decreased with pH increasing to 10. It has been well known that the plant uptake and translocation for weak ionizable organic compounds decrease with the increasing the pH value, which could be accounted for by the ion-trap mechanism assuming that entry of the chemicals occurs largely by passive diffusion of the undissociated form of the acids, with passage of the anions across the cell membranes being very slow (Trapp, 2000; Trapp et al., 2010). The different influence of pH on them may be due to the fact that PFOS is a strong acid, and based on the calculated pKa value of 3.3 (Brooke et al., 2004), PFOS should be present completely in the ionized form on the pH range tested, thus like the other electrolytes, facilitated diffusion and active transfer may be main mechanisms for PFOS uptake. The maximum uptake of PFOS was found at pH = 6. This may be caused by plant growth. It is well known that pH can directly affect nutrient availability, and the best pH range for wheat growing is between 5.8 and 6.5. Thus, at the tested pH range, wheat thrived best in the solution of pH = 6, which may also facilitate the uptake of PFOS by wheat seedlings. On the whole the roots contained a higher concentration of PFOS than the shoots. The concentrations of PFOS were of the one order of magnitude in the roots than that in the shoots. This difference was also statistically confirmed by one-factorial analysis of covariance with repeated measures at p 6 0.05. 3.4. Concentration effect on PFOS uptake in wheat

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3.5. Temperature effect on PFOS uptake in wheat Temperature is an important parameter affecting plant growth, which may indirectly influence plant uptake to chemicals. Fig. 5 shows the impact of temperature on PFOS uptake by wheat seedlings. It is well known that the chemical concentrations in plants usually increased with increasing temperature in most cases (Ekvall and Greger, 2003; Fritioff et al., 2005). This was also found to be significant in wheat seedlings for PFOS. As shown in Fig. 5, the PFOS concentrations in the plant compartments increased directly with temperature increasing from 20 to 30 °C at a solution concentration of 1 mg L1. Linear regression analysis showed that this increase in concentration and temperature was statistically significant at p 6 0.05, with correlation coefficient square greater than 0.985. Concentrations of PFOS were of the same order of magnitude in both the roots and the shoots, but the average level detected in the roots was 3.84 times higher than that in the shoots. This difference was also statistically confirmed by one-way analysis of covariance at p 6 0.05. 3.6. Salinity effect on PFOS uptake in wheat The changes in salinity affect the physicochemical properties of chemicals as well as the physiology of organisms, consequently leading to changes in contaminant uptake and toxicity (Dyer et al., 1989; Hall and Anderson, 1995). Fig. 6 shows the effect of salinity on PFOS uptake by wheat seedlings. For the roots and shoots, the concentration of PFOS was significantly higher in wheat seedlings exposed to NaCl than those in the control. At a solution concentration of 1 mg L1, the PFOS uptake by wheat seedlings increased by 3.5-fold as salinity increased from 0.03 to 7.25 psu (practical salinity unit, psu). The linear relationships were found between this increase in salinity for PFOS and in both plant compartments with correlation coefficient square higher than 0.93 (see Fig. 6B). The concentrations of PFOS in roots were at least 4.5 times higher than those in shoots. This difference was statistically confirmed by one-way analysis of covariance at p 6 0.05.

Concentration in wheat seedling (ug/kg)

Concentration in wheat seedling (mg/kg)

Fig. 4 shows the effect of concentration on the PFOS uptake by wheat seedlings. Comparison of the PFOS content of roots and shoots shows that the concentration was higher in roots than in shoots (as much as three times higher at a solution concentration of 1 mg L1). These differences between the levels in the plant

compartments were statistically verified at p 6 0.05 by one-way analysis of covariance. The concentration of PFOS measured in the plant compartments increased directly with increasing PFOS concentration in the solution (from 0.1 to 100 mg L1). Good log– log linear relationships were obtained between this increase in concentration for PFOS and in both plant compartments, which were statistically significant at p 6 0.05 (see Fig. 4B). This result was consistent with a previous study (Stahl et al., 2009).

6

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pH Fig. 3. Effect of pH on PFOS uptake by wheat seedlings.

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Concentration in water (mg/L) Fig. 4. Effect of concentration on PFOS uptake by wheat seedlings.

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Salinity (psu) Fig. 6. Effect of salinity on PFOS uptake by wheat seedlings.

4. Environmental relevance This study demonstrated the ability of plant to take up PFOS from solution under the test conditions selected. Furthermore, the plant uptake of PFOS may be significantly influenced by the environmental factors (temperature, contaminant concentrations, salinity and pH value). It is possible that PFOS is stored by plant and then accumulated through the food chain which could pose potential risks to species consuming plant parts, including humans. Acknowledgements The authors acknowledge the financial supports from the Natural Science Foundations of China (Nos. 20907005 and 20907004) and the Fundamental Research Funds for the Central Universities. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.chemosphere. 2012.11.036. References Bhadra, R., Spanggord, R.J., Wayment, D.G., Hughes, J.B., Shanks, J., 1999a. Characterization of oxidation products of TNT metabolism in aquatic phytoremediation systems of Myriophyllum aquaticum. Environ. Sci. Technol. 33, 3354–3361.

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