Chemosphere 119 (2015) 978–986

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Comparing humic substance and protein compound effects on the bioaccumulation of perfluoroalkyl substances by Daphnia magna in water Xinghui Xia ⇑, Zhineng Dai, Andry Harinaina Rabearisoa, Pujun Zhao, Xiaoman Jiang School of Environment, Beijing Normal University, State Key Laboratory of Water Environment Simulation, Beijing 100875, China

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 PFAS partition coefficients between

HA–water were lower than between albumin–water.  The effects of HA and albumin on PFAS bioaccumulation in D. magna were comparable.  HA and albumin enhanced the bioaccumulation of all tested PFASs at a lower level.  HA and albumin decreased the bioaccumulation of all tested PFASs at a higher level.  DOM reduced the bioavailable concentrations and uptake rates of PFASs to D. magna.

a r t i c l e

i n f o

Article history: Received 26 July 2014 Received in revised form 5 September 2014 Accepted 8 September 2014 Available online 7 October 2014 Handling Editor: I. Cousins Keywords: Perfluoroalkyl substances (PFASs) Bioavailability Dissolved organic matter (DOM) Humic acid Sorption Daphnia magna

⇑ Corresponding author. Tel./fax: +86 10 58805314. E-mail address: [email protected] (X. Xia). http://dx.doi.org/10.1016/j.chemosphere.2014.09.034 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t The influence of humic substances and protein compounds on the bioaccumulation of six types of perfluoroalkyl substances (PFASs) in Daphnia magna was compared. The humic substances included humic acid (HA) and fulvic acid (FA), the protein compounds included chicken egg albumin (albumin) and peptone, and the PFASs included perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorononanoic acid (PFNA), perfluorodecanoic acid, perfluoroundecanoic acid, and perfluorododecanoic acid. Four concentrations (0, 1, 10, and 20 mg L1) of the four dissolved organic matter (DOM) types were investigated. At the 1 mg L1 level, HA and albumin enhanced all tested PFAS bioaccumulation, whereas FA and peptone only enhanced the bioaccumulation of shorter-chain PFASs (PFOS, PFOA, and PFNA). However, all four DOM types decreased all tested PFAS bioaccumulation at the 20 mg L1 level, and the decreasing ratios of bioaccumulation factors caused by FA, HA, albumin, and peptone were 1–49%, 23–77%, 17–58%, and 8–56%, respectively compared with those without DOM. This is because DOM not only reduced the bioavailable concentrations and uptake rates of PFASs but also lowered the elimination rates of PFASs in D. magna, and these opposite effects would change with different DOM types and concentrations. Although the partition coefficients (L kg1) of PFASs between HA and water (104.21–104.98) were much lower than those between albumin and water (104.92–105.86), their effects on PFAS bioaccumulation were comparable. This study suggests that although PFASs are a type of proteinophilic compounds, humic substances also have important effects on their bioavailability and bioaccumulation in aquatic organisms. Ó 2014 Elsevier Ltd. All rights reserved.

X. Xia et al. / Chemosphere 119 (2015) 978–986

1. Introduction Perfluoroalkyl substances (PFASs) are organofluorine compounds in which all of the hydrogens are replaced by fluorine on a carbon chain. These compounds are used in a multitude of consumer products because of their ability to repel water and oil, their heat resistance, and their chemical inertness (Schultz et al., 2003; Buck et al., 2011). Because the carbon–fluorine bond is one of the strongest bonds in organic chemistry, PFASs are persistent in the environment, and they are not degraded by any natural processes. Toxicological studies have demonstrated that some PFASs can cause peroxisomal proliferation, disturbances in fatty acid metabolism, and alterations in other important biochemical processes within organisms (Ankley et al., 2005; Giesy et al., 2010). PFASs are widely present in aquatic environments. Many PFAS types have been found in tap water (Skutlarek et al., 2006), groundwater (Eschauzier et al., 2013), rivers (Yeung et al., 2009; Zhao et al., 2014), lakes (Boulanger et al., 2004; Kannan et al., 2005), oceans (Taniyasu et al., 2004; Yamashita et al., 2008), and snowfall (Young et al., 2007); their concentrations generally ranged from pg to lg per liter for each compound (Skutlarek et al., 2006), and they even reached as high as mg per liter in some waters (Moody et al., 2002). Many investigators have found that PFASs could accumulate in aquatic organisms (Martin et al., 2003; Dai et al., 2013; Xia et al., 2013), and they might also be transferred to human beings through the food web (Houde et al., 2006). Therefore, it is necessary to understand the factors that affect the bioavailability and bioaccumulation of PFASs in aquatic environments. Dissolved organic matter (DOM), with concentrations ranging from 0 mg L1 to as much as 50 mg L1 dissolved organic carbon (Hofrichter and Steinbüchel, 2001), are known to significantly affect the bioavailability of hydrophobic organic compounds (HOCs) in aquatic environments (Haitzer et al., 1998; Xia et al., 2013). DOM are a heterogeneous mixture of aromatic and aliphatic organic compounds that can be divided into biochemically defined compounds and humic substances. The former includes proteins, carbohydrates, lipids, and others; the latter primarily consists of fulvic and humic acids (Thurman, 1985; Leenheer and Croué, 2003; Fu et al., 2007). Our previous study (Xia et al., 2013) found that the partition coefficients of PFASs between protein (bovine albumin from animals and soy peptone from plants) and water are very high, and they are comparable with those of the HOCs between lipid and water. At high concentrations (10 and 20 mg L1), these two protein types decreased the freely dissolved concentrations of PFASs and suppressed their bioaccumulation in Daphnia magna (D. magna) significantly. Although PFASs are considered as proteinophilic compounds, they have a highly hydrophobic perfluorocarbon chain and can associate with humic substances through hydrophobic interactions. Some studies have suggested that humic substances might bind strongly with PFASs (Chen et al., 2011; Xia et al., 2012). Therefore, it was hypothesized that humic substances, which are the most abundant DOM in aquatic environments, will also affect the bioavailability and bioaccumulation of PFASs in aquatic organisms, and their effects might be similar to those of protein compounds. Humic acid and fulvic acid are the most abundant components of humic substances and are widely believed to be representative of humic substances (Carter and Suffet, 1982; Mobed et al., 1996; Haitzer et al., 1998). Albumin is a protein type that is widely used in biological and environmental experiments as a model protein (Sabín et al., 2006; MacManus-Spencer et al., 2009; Bischel et al., 2010). Peptone encompasses various water-soluble protein derivatives created by the partial hydrolysis of proteins; peptone is ubiquitous in aquatic environments and widely used in biological and environmental experiments (Garcia et al., 2010; Banihashemi and

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Droste, 2014). Thus, humic acid (HA), fulvic acid (FA), chicken egg albumin (albumin), and peptone were studied in the present research as typical DOM types. The primary objective of this research was to study the effect of humic substances (HA and FA) on PFAS bioaccumulation in the water flea D. magna and compare their effects with those of protein compounds (albumin and peptone). The studied PFASs included perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorononanoic acid (PFNA), perfluorodecanoic acid (PFDA), perfluoroundecanoic acid (PFUnA), and perfluorododecanoic acid (PFDoA). The effects of the four DOM types were investigated by using concentrations ranging from 0 to 20 mg L1. The uptake and depuration kinetics of PFASs in the presence of different types and concentrations of DOM were studied, and the interactions between DOM and PFASs were examined to explore the effect mechanisms of DOM.

2. Materials and methods 2.1. Materials PFOS (98%) was purchased from Tokyo Chemical Industries (Tokyo, Japan). PFOA (96%), PFNA (97%), PFDA (98%), PFUnA (95%), and PFDoA (95%) were obtained from Acros Organics (New Jersey, US). The physicochemical parameters of the PFASs are described in Table S1 (Supplementary Information). A purity-corrected equimass stock solution containing these PFASs was prepared in a 80:20 (v/v) methanol/water solution at a concentration of 200 mg L1 for each PFAS. Chromatography grade methanol was purchased from J.T. Baker of Phillipsburg, NJ, USA. [1,2,3,4-13C4] Perfluorooctane sulfonate (MPFOS) (P99%) and [1,2,3,4-13C4] perfluorooctanoic acid (MPFOA) (P99%) were supplied by Wellington Laboratories (Guelph, Canada) for use as recovery indicators. Ammonium acetate (98%), methyl-tert-butyl ether (MTBE, 99.5%), and tetrabutylammonium hydrogen sulfate (TBA) were purchased from Sigma–Aldrich Chemical Co. (St. Louis, US), and they were used to extract PFASs from D. magna. HA, chicken egg albumin, and peptone were purchased from Sigma–Aldrich. FA (>95%) was purchased from He’nan Changsheng Co. Ltd. (He’nan, China), and it was ground into 100-mesh powder. Stock solutions of albumin, peptone, and FA were prepared in deionized water. To prepare HA solution, a given amount of HA was dissolved in approximately 5 mL of 0.1 M NaOH at first and then diluted with deionized water to 100 mg L1 HA; the pH was then adjusted to 7.0 with 1 M HCl. Anhydrous sodium hydrogen phosphate (Na2HPO4) and sodium dihydrogen phosphate monohydrate (NaH2PO4H2O) were purchased from Fisher Chemical (Fairlawn, NJ). A dialysis bag (Spectra Pro 6) with a molecular weight cutoff of 7000 Da was purchased from Sigma–Aldrich Chemical Co. (St. Louis, US). The C, H, and N contents of HA, FA, albumin, and peptone were determined with a CHN elemental analyzer (Thermo Finnigan, Germany), and the results are shown in Table S2; the other physicochemical parameters of the four DOM types are listed in Table S3. 2.2. Steady state and kinetic experiments of PFAS bioaccumulation D. magna individuals were cultured under the conditions described in the guidelines for chemical testing from the Organization for Economic Cooperation and Development (OECD, 2008). In brief, the D. magna were cultured in artificial freshwater (AFW) and maintained at 21 ± 0.5 °C under a 16:8 h (light:dark) photoperiod. Cultured daphnids were fed a Scenedesmus subspicatus suspension twice daily. The detailed culture procedure is shown in Supplementary Information.

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Bioaccumulation experiments were conducted in 500 mL polypropylene beakers. Each DOM type was prepared at concentrations of 1, 10, and 20 mg L1 in AFW. A total of 200 mL DOM solution was added to each beaker; 0.02 mL of PFAS solution (50 mg L1) was then added to each beaker at a nominal concentration of 5 lg L1 for each PFAS. Methanol was used as a carrier at 0.008% in the final test medium, and the preliminary experiments showed that it had no toxic effects on D. magna survival. The beakers were shaken at 95 rpm in darkness at 21 °C for 72 h before the exposure experiment to obtain a binding equilibrium state between DOM and PFASs. For the steady state bioaccumulation experiment, a total of 10 D. magna juveniles (6–24 h old) were added to each beaker, and they were cultured at 21 ± 0.5 °C under a 16:8 h (light:dark) photoperiod. At least 6 h before the exposure, the daphnids were transferred to clean AFW to empty their gut contents. The duration of the bioaccumulation test was 21 d; the exposure solution was renewed with fresh medium every 7 d and the D. magna were fed Scenedesmus subspicatus each day. The D. magna neonates were discarded daily. Previous studies indicated that the feeding and discarding of neonates would not affect PFAS accumulation in D. magna (Dai et al., 2013). Following the bioaccumulation period, the daphnids were transferred by pipettes from each beaker to a polystyrene culture dish and rinsed with AFW. The rinsed D. magna were dried with filter paper and then transferred by dental pick to a 10-mL plastic (polypropylene, PP) centrifuge tube, and their wet weights were obtained. The D. magna were then frozen and stored at 20 °C until extraction. A control group was set up to study PFAS accumulation in the absence of DOM, and a blank experiment without PFAS and DOM spiking was also conducted. Each experimental set was conducted in triplicate. The pH and hardness of experimental solutions were measured at the beginning and end of all tests, and the results indicated that their variations were 65%. After the steady state bioaccumulation experiments, more than 92% of the daphnids survived. The bioaccumulation factor (BAF) of PFASs in D. magna according to the steady state method was calculated by using the following equation:

BAF ¼

CB Cw

ð1Þ

where CB is the PFAS concentration in D. magna (lg kg1) at the end of the exposure, and Cw is the PFAS concentration in the water phase at the end of exposure (lg L1), which was considered to be equal to its initial concentration because the variation in the PFAS concentration was within 2% in the bioaccumulation experiments. Using HA and albumin as representatives for humic substances and protein compounds, respectively, the kinetic experiment was conducted to compare their effects on PFAS bioaccumulation. The procedure for the uptake phase of bioaccumulation was the same as that of the steady state experiment except that 60 D. magna were exposed in each beaker and 5 D. magna were sampled at 1, 3, 7, 11, and 24 h. The rest of the D. magna were then transferred to the same DOM solution without PFASs to start the depuration experiment, and 5 D. magna were sampled at 1, 3, 7, 11, and 24 h. The sampled daphnids were dried and weighed as explained above and then stored at 20 °C until further analysis. The kinetic parameters for uptake and elimination were obtained by fitting the uptake phase data with the following equation:

C b ¼ ku C w

  1  eke t ke

ð2Þ

where Cb is the PFAS concentration in D. magna (lg kg1) at time t (h); Cw is the PFAS concentration in the water phase (lg L1), which was considered to be equal to its initial concentration; ku is the uptake rate constant of PFASs from water (L kg1 h1) and ke is

the elimination rate constant of PFASs from D. magna (h1). The depuration rate constants (kd, h1) were obtained by fitting the depuration phase data with the following equation:

C b ¼ A  expðkd tÞ

ð3Þ

2.3. Dialysis bag experiments A dialysis bag experiment was conducted to investigate PFAS binding with HA and albumin. In brief, 20 mL of HA or albumin solution at a concentration of 10 mg L1 was added to the dialysis bags; the bags were then sealed and placed in 200 mL of deionized water inside 500 mL polypropylene beakers and shaken at 90 rpm in darkness for 72 h to remove the components with molecular weights lower than 7000 Da. The results showed that 4% of the HA and no substantial albumin could pass through the dialysis bag; this finding has been taken into account to calculate the partition coefficients of PFASs between HA and water. The pre-treated dialysis bags containing HA/albumin solution were placed in beakers with 200 mL of AFW, and they were opened and mixed with given amounts of PFAS solution with nominal PFAS concentrations of 5, 10, 20, and 50 lg L1 in the dialysis bags. The dialysis bags were then sealed and the beakers were shaken at 120 rpm in darkness at 21 °C for 7 d; a preliminary experiment showed that 7 d was long enough for the PFASs to reach equilibrium between the HA/albumin inside and water outside the dialysis bag. A control experiment was conducted with a dialysis bag but without HA/ albumin. Each treatment was performed with three replicates. After reaching equilibrium, water samples were collected from inside and outside the dialysis bags to determine the PFASs. The partition coefficients (Kp, L kg1) of PFASs between HA/albumin and water were calculated by using the following equation:

Kp ¼

Cs C free

ð4Þ

where Cfree (lg L1) is the freely dissolved concentration of each PFAS in the solution of PFASs and HA/albumin, and it was equal to the PFAS concentration outside the dialysis bag; CS (lg kg1) is the PFAS concentration bound to HA/albumin, which was calculated on the basis of the difference in PFAS concentrations between the inside and outside of the dialysis bag. 2.4. PFAS extraction and analysis The PFASs in D. magna and the water samples from the dialysis bag experiments were extracted by ion-pairing agent extraction method with some modification (Hansen et al., 2001; Taniyasu et al., 2003). In brief, 1 mL of the ion-pairing agent TBA (0.5 M, adjusted to pH 10), 2 mL of Na2CO3 (0.25 M), 2 mL of MTBE, and 100 lL (10 ng) each of MPFOA and MPFOS, the internal standards, were added to each PP centrifuge tube containing a 4.5 mL water sample or 10 D. magna. A detailed procedure can be found in Supplementary Information. PFASs were analyzed by liquid chromatography-tandem mass spectrometer (LC-MS/MS; Dionex Ultimate 3000 and Applied Biosystems API 3200) in electrospray negative ionization mode. In brief, a 10 lL sample aliquot was injected into a 4.6  150 mm Acclaim 120 C18 Column with 50 mM ammonium acetate and methanol as the mobile phase, at a flow rate of 1 mL min1. The detailed procedure was described by Xia et al. (2012). 2.5. Quality assurance and quality control (QA/QC) The limits of quantification (LOQs) were defined as the lowest PFAS concentrations that could be quantitatively determined at a

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signal to noise ratio greater than 7, and the deviations were within ±20% from the theoretical values of the duplicate injection. The LOQs for the target chemicals in the LC-MS/MS ranged from 0.01 to 0.05 lg L1, and the corresponding detection limits for biological samples were 0.05–0.10 ng g1 wet weight. The correlation coefficients of the standard calibration curves were higher than 0.99, and the repeatability of these calibration curves was confirmed prior to each set of determinations. Recoveries for the target analytes in D. magna were between 81% and 95%, and the recoveries for MPFOS and MPFOA, the mass spectrometric isotope spiked to the D. magna samples, were between 90% and 95%. The recoveries of the target analytes and MPFOS in addition to the MPFOA from the water samples and DOM solutions ranged from 85% to 108%. A detailed procedure for quality assurance and quality control is shown in Supplementary Information. The sample concentrations were corrected according to the recovery indicators. PFASs were not detected in the D. magna samples of the blank bioaccumulation experiments without spiking with PFASs and DOM. In addition, each PFAS that accumulated in D. magna was less than 2% of the whole amount spiked to the system, indicating that PFAS bioaccumulation in the organisms did not significantly change the nominal concentrations of PFASs in the water system or break the PFAS equilibrium between DOM and water. The mass balance results of the dialysis bag experiments showed that the PFAS variations in the system were lower than 10%, and the control experiment results showed that the difference in PFAS concentrations between the inside and outside of the dialysis bag was less than 8% in the absence of DOM. 2.6. Data processes All statistical analyses were performed with SPSS 18.0 for windows (SPSS Inc., Chicago II., USA). An analysis of the variance (ANOVA, one factor) was performed to test differences between each two compared groups, and the difference was considered significant when the significance level was smaller than 0.05. The Pearson correlation coefficient was calculated and used to test the significance of correlation between each two variables. 3. Results and discussion 3.1. DOM Effects on the steady state bioaccumulation of PFASs in D. magna As shown in Fig. 1 and Table 1, in the absence of DOM, the body burden and BAF values of different PFAS types was ordered PFOA < PFNA < PFOS < PFDA < PFUnA < PFDoA, and the BAF values for carboxylate PFASs have a positive relation with their octanol/water partition coefficients (r = 0.980, p < 0.05). This relation was also found in other studies for rainbow trout (Martin et al., 2003), Chironomus plumosus larvae (Xia et al., 2012), and earthworms (Eisenia fetida) (Zhao et al., 2013). However, in the presence of the four DOM types, the order of the BAF values changed. For instance, the BAF value of PFNA was lower than that of PFOA in the presence of 20 mg L1 HA and the value of PFUnA was lower than that of PFDA in the presence of 20 mg L1 albumin (Table 1); the BAF of PFOS was even higher than those of PFUnA and PFDoA in the presence of fulvic acid, albumin, and peptone. This finding indicated that apart from the carbon chain length and functional groups of PFASs, the presence of DOM is also an important factor in PFAS bioaccumulation. For the HA and albumin effects, PFAS bioaccumulation was enhanced in the presence of 1 mg L1 HA/albumin but inhibited in the presence of 10 and 20 mg L1 HA/albumin (Fig. 1). According to the results shown in Table 1, when HA and albumin were at

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1 mg L1, the BAF values for the PFASs increased by 8-66% and 4–42%, respectively when compared with samples lacking DOM. By contrast, when the HA and albumin concentrations came to 10 mgL1, the BAF values of the PFASs decreased by 11–56% and 2–51% in comparison with the samples lacking DOM, and they decreased further when the HA and albumin concentrations reached 20 mg L1. Therefore, the effect of humic acid on PFAS bioaccumulation was similar to that of chicken egg albumin in the present research, and it was also consistent with the results obtained in the previous study that bovine albumin and soy peptone suppressed PFAS bioaccumulation at high concentrations (10 and 20 mg L1) but enhanced PFAS bioaccumulation at a low concentration (1 mg L1) (Xia et al., 2013). This finding suggests that although PFASs are a type of proteinophilic compounds, the effect of humic acid in water on their bioaccumulation in D. magna is similar to that of protein compounds. For the FA effect, the bioaccumulation of shorter-chain PFASs (PFOS, PFOA, and PFNA) in D. magna was enhanced when the FA concentrations were 1 and 10 mg L1 (Fig. 1), and the BAF values increased by 12–34% and 31–45%, respectively, in comparison with the control group (Table 1). However, the bioaccumulation of the shorter-chain PFASs was inhibited when the FA concentration reached 20 mg L1. The bioaccumulation of the longer-chain PFASs (PFDA, PFUnA, and PFDoA) was inhibited when FA was at 1, 10, and 20 mg L1, and their BAF values decreased with increasing FA concentrations. As shown in Fig. 1, the effect of peptone on PFAS bioaccumulation was similar to that of FA. According to the above results, the presence of the four DOM types at a higher concentration (20 mg L1) reduced the bioaccumulation of all tested PFASs. Furthermore, the reduction ratios of BAF values caused by FA (1–49%) and peptone (8–56%) were comparable, and the ratios caused by HA (23–77%) and albumin (17–58%) were also comparable. This evidence further demonstrates that the effect of humic substances in water on PFAS bioaccumulation in D. magna is similar to that of protein compounds. It is generally accepted that DOM leads to a decrease in the bioaccumulation of organic compounds (Leversee et al., 1983; McCarthy and Jimenez, 1985; Geyer et al., 1987; Barron, 1990; Leenheer and Croué, 2003). By contrast, the enhanced bioaccumulation of organic compounds caused by the presence of DOM with a concentration below 10 mg L1 has also been found in several studies (Leversee et al., 1983; Servos et al., 1989; Versteeg and Shorter, 1992; Haitzer et al., 1998). Thus, the effect of the four DOM types on the bioaccumulation of PFASs in the present research is in accordance with previous studies for other organic compounds. 3.2. DOM effects on the bioaccumulation kinetics of PFASs in D. magna 3.2.1. DOM effects on the uptake and depuration rates of PFASs The uptake and depuration kinetics of PFASs in D. magna were studied under different HA and albumin concentrations (Fig. S1). According to the fitted kinetic parameters shown in Table 2, in the absence of DOM, the uptake rate constant (ku) increased and the depuration rate constant (kd) decreased with the fluorocarbon chain length of PFASs, which led to the BAF value increasing with the fluorocarbon chain length of the PFASs. The ku values of the control group (DOM-free) were significantly higher than those of the HA and albumin groups (p < 0.05), and they decreased significantly with increasing HA and albumin concentrations (p < 0.05). Similar to the ku value, the kd values in the control group were also significantly higher than those of the HA and albumin groups (p < 0.05), and the depuration ratios of the former (61-81%) were higher than the ratios of the latter (34–76%) after depuration for 24 h (Table S4). In addition, the depuration ratio decreased with increased fluorocarbon chain length of PFASs in the presence of

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3500

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Fig. 1. Effects of DOM concentrations on the bioaccumulation of PFASs by D. magna (significant difference exists between the groups with different letters (a, b, c, and d) (P < 0.05) and no significant difference between the groups with at least one same letter (P > 0.05)).

Table 1 BAF values (L kg1, mean ± SD) based on the nominal concentrations of PFASs (5 lg L1) under the effect of different concentrations and types of DOM (mean ± standard deviation, n = 3).

Control 1 mg L1 HA 10 mg L1 HA 20 mg L1 HA 1 mg L1 Albumin 10 mg L1 Albumin 20 mg L1 Albumin 1 mg L1 FA 10 mg L1 FA 20 mg L1 FA 1 mg L1 Peptone 10 mg L1 Peptone 20 mg L1 Peptone

PFOS

PFOA

PFNA

PFDA

PFUnA

PFDoA

296 ± 36 392 ± 61 196 ± 26 145 ± 23 419 ± 91 289 ± 75 214 ± 42 396 ± 35 428 ± 13 320 ± 21 428 ± 10 415 ± 71 235 ± 31

136 ± 24 226 ± 33 121 ± 29 105 ± 69 166 ± 22 128 ± 34 113 ± 46 168 ± 41 190 ± 49 98 ± 42 110 ± 39 80 ± 34 60 ± 10

197 ± 24 214 ± 35 144 ± 24 70 ± 17 210 ± 62 159 ± 35 117 ± 56 221 ± 43 259 ± 27 175 ± 18 212 ± 45 204 ± 21 180 ± 33

310 ± 31 414 ± 63 136 ± 19 71 ± 24 396 ± 87 235 ± 68 227 ± 16 287 ± 42 265 ± 41 219 ± 31 261 ± 25 250 ± 44 188 ± 35

446 ± 43 562 ± 74 260 ± 38 169 ± 38 567 ± 47 252 ± 45 213 ± 13 288 ± 15 266 ± 38 231 ± 27 316 ± 64 281 ± 4 260 ± 51

558 ± 30 848 ± 28 317 ± 39 245 ± 84 578 ± 40 274 ± 13 232 ± 10 341 ± 51 296 ± 50 286 ± 41 408 ± 38 435 ± 92 371 ± 81

HA/albumin (Table S4), suggesting that the longer fluorocarbon chain PFASs are harder to eliminate from D. magna than the shorter ones; this is because the longer ones are more hydrophobic. 3.2.2. The effect mechanism of DOM on the bioaccumulation kinetics of PFASs To analyze the DOM effect mechanism on the bioaccumulation kinetics of PFASs, the binding of PFAS to both HA and albumin have been studied. As shown in Fig. 2, PFAS binding to both HA and albumin followed the Freundlich isotherm, suggesting that it is not a linear partitioning process but an adsorption-like process. According to the results shown in Table 3, when the initial PFAS concentration was 5 lg L1 and the HA/albumin was 10 mg L1, the partition coefficients of PFASs between HA and water (log KHA, L kg1) ranged from 4.21 to 4.98, and the coefficients between

albumin and water (log KALB, L kg1) ranged from 4.92 to 5.86; the albumin–water results were significantly higher than the HA–water ones (p < 0.05). The organic carbon normalized partition coefficient of PFUnA between HA and water (log Kow = 5.76, log Koc = 5.04 L kg1) obtained in the present research was comparable to that (log Koc = 5.30) of 8:2 fluorotelomer alcohol (one type of PFAS) with a similar log Kow (5.58) (Liu and Lee, 2005). However, the log KHA values for the PFASs were lower than those of other polycyclic aromatic hydrocarbons with similar log Kow values. For instance, the PFNA value (log Kow = 4.84, log KHA = 4.37) was lower than that of phenanthrene (log Kow = 4.46, log KHA = 4.68); PFDA (log Kow = 5.30, log KHA = 4.76) had a lower value than that of pyrene (log Kow = 5.30, log KHA = 5.18) (Kukkonen and Pellinen, 1994); and PFUnA (log Kow = 5.76, log Koc = 5.04) had a lower value than that of chrysene (log Kow = 5.61, log Koc = 5.80) (Gourlay et al.,

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Table 2 The uptake and depuration rate constants of PFASs in Daphnia magna under the effect of different concentrations of HA and Albumin. (The error is the 95% confidence interval obtained from the regression.) PFOS

PFOA

PFNA

8.03 ± 0.83 7.19 ± 0.74 4.13 ± 0.19 3.30 ± 0.16 4.49 ± 0.47 3.60 ± 0.23 1.38 ± 0.16

Depuration rate constant, kd (h1) Control 0.061 ± 0.001 1 mg L1 HA 0.045 ± 0.005 1 10 mg L HA 0.045 ± 0.001 0.040 ± 0.004 20 mg L1 HA 1 mg L1 Albumin 0.044 ± 0.008 10 mg L1 Albumin 0.036 ± 0.002 20 mg L1 Albumin 0.033 ± 0.005

0.067 ± 0.007 0.038 ± 0.002 0.041 ± 0.003 0.033 ± 0.001 0.053 ± 0.002 0.039 ± 0.006 0.025 ± 0.005

PFASs bound to albumin (mg kg-1)

Uptake rate constant, ku (L kg1 h1) Control 10.70 ± 1.16 1 mg L1 HA 9.04 ± 1.43 1 7.25 ± 0.39 10 mg L HA 20 mg L1 HA 5.87 ± 0.22 1 mg L1 Albumin 4.73 ± 0.45 10 mg L1 Albumin 3.86 ± 0.44 20 mg L1 Albumin 2.55 ± 0.34

y = 779.3x 0.778 y = 373.5x 0.692 R² = 0.998 R² = 0.995

Albumi

3000 2500

PFDoA PFOS

PFDA

PFUnA

PFDoA

8.47 ± 0.72 6.70 ± 0.81 6.00 ± 0.80 4.60 ± 0.60 2.40 ± 1.16 1.85 ± 0.18 0.96 ± 0.25

14.89 ± 1.29 10.80 ± 1.47 9.93 ± 1.22 8.11 ± 1.59 7.17 ± 1.44 5.75 ± 0.72 4.21 ± 0.27

31.25 ± 2.53 28.39 ± 2.55 24.53 ± 1.53 23.03 ± 3.2 12.77 ± 1.48 11.23 ± 4.02 7.63 ± 1.59

45.08 ± 2.51 37.32 ± 1.20 27.06 ± 3.17 22.59 ± 3.08 23.01 ± 2.35 21.00 ± 2.57 16.06 ± 2.11

0.056 ± 0.002 0.036 ± 0.002 0.037 ± 0.002 0.037 ± 0.006 0.047 ± 0.001 0.039 ± 0.001 0.036 ± 0.004

0.062 ± 0.002 0.042 ± 0.003 0.043 ± 0.006 0.042 ± 0.004 0.047 ± 0.006 0.037 ± 0.002 0.034 ± 0.005

0.044 ± 0.005 0.037 ± 0.007 0.036 ± 0.006 0.035 ± 0.005 0.033 ± 0.008 0.025 ± 0.005 0.024 ± 0.006

0.035 ± 0.005 0.025 ± 0.003 0.023 ± 0.004 0.023 ± 0.003 0.026 ± 0.005 0.020 ± 0.005 0.019 ± 0.004

PFDA PFOA

PFUnA PFNA

y = 280.4x 0.660 R² = 0.995

2000

206.3x 0.631

y= R² = 0.999

1500

y = 159.7x 0.601 R² = 0.996

1000 y = 104.1x 0.555 R² = 0.996

500 0 0

5

10

15

20

25

30

PFASs bound to humic acid (mg kg-1)

PFASs

Humic acid

1600

y = 276.6x 0.670 R² = 0.977

PFDoA

PFUnA

PFDA

PFOS

PFNA

PFOA

y = 138.1x 0.594 R² = 0.990

1200

800

y = 86.61x 0.539 R² = 0.999 y = 69.03x 0.514 R² = 0.999 y = 56.89x 0.496 R² = 0.996

400 y = 46.81x 0.476 R² = 0.998

0 0

35

10

Freely dissolved PFAS concentration (µg L-1)

20

30

40

50

60

Freely dissolved PFAS concentration (µg L-1)

Fig. 2. Sorption isotherms of PFASs to albumin and humic acid with the concentration of 10 mg L1 (mean ± standard deviation, n = 3).

Table 3 Freundlich isotherms of PFASs and their partition coefficients between albumin/HA (10 mg L1) and water when with the initial PFAS concentration of 5 lg L1 (mean ± standard deviation, n = 3).

Freundlich isotherms Freundlich isotherms Partition coefficients, Partition coefficients,

for albumin (Q, mg kg1; c, lg L1) for HA (Q, mg kg1; c, lg L1) log KALB (albumin, L kg1) log KHA (HA, L kg1)

PFOS

PFOA

PFNA

PFDA

PFUnA

PFDoA

Q = 206.3c0.631 Q = 69.03c0.514 5.29 ± 0.03 4.61 ± 0.02

Q = 104.1c0.555 Q = 46.81c0.476 4.92 ± 0.01 4.21 ± 0.03

Q = 159.7c0.601 Q = 56.89c0.496 5.19 ± 0.02 4.37 ± 0.02

Q = 280.4c0.660 Q = 86.61c0.539 5.61 ± 0.01 4.76 ± 0.01

Q = 373.5c0.692 Q = 138.1c0.594 5.76 ± 0.01 4.79 ± 0.02

Q = 779.3c0.778 Q = 276.6c0.670 5.86 ± 0.02 4.98 ± 0.03

2003). This finding suggested that the binding capacity of PFASs to humic substances was lower than that of other hydrophobic compounds, which is explained by the relatively higher solubility of PFASs in addition to the hydrophobic and oleophobic characteristics of their fluorocarbon chain. The partition coefficients of PFASs between HA/albumin and water were used to calculate the freely dissolved concentrations of PFASs in the exposure system with the following equations:

C total ¼ C free þ C free K p C p

ð5Þ

C total 1 þ K pCp

ð6Þ

C free ¼

where Ctotal (lg L1) and Cfree (lg L1) are the total and freely dissolved PFAS concentration in the system under the equilibrium status, respectively; Kp (L kg1) is the protein/water partition coefficient; and Cp (kg L1) is the protein concentration in the system. The calculated results of the freely dissolved PFAS concentrations are shown in Fig. 3. Many investigators found that the

bioaccumulation factor could be satisfactorily predicted from the freely dissolved chemical concentrations in the presence of DOM (Kukkonen and Oikari, 1991; Yang et al., 2007; Chen et al., 2010; Gouliarmou et al., 2012). For decreased organic compound bioaccumulation caused by the presence of DOM, the most accepted mechanism is a lack of bioavailability of DOM-bound chemicals (McCarthy and Jimenez, 1985; Akkanen and Kukkonen, 2003). However, in the present research, we found that the BAFfreely values based on the freely dissolved PFAS concentrations were elevated in the presence of 1 and 10 mg L1 albumin and in the presence of 1 mg L1 HA (Table S5). Furthermore, although the partition coefficients of PFASs between albumin and water were much higher than those between HA and water, the body burden of most PFASs was higher in the presence of 10 and 20 mg L1 albumin relative to HA (Fig. 4). This finding suggests that, apart from the uptake rates of PFASs in D. magna that depend on their freely dissolved concentrations, the depuration rates of PFASs will also be affected by the presence of both humic substances and protein compounds in water. This conclusion is consistent with the results reported by Al-Reasi

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Freely dissolved PFAS concentrations (µg L-1)

7.00 6.00

Control

1 mg/L HA

10 mg/L HA

20 mg/L HA

1 mg/L Albumin

10 mg/L Albumin

20 mg/L Albumin

5.00 4.00 3.00 2.00 1.00 0.00 PFOS

PFOA

PFNA

PFDA

PFUnA

PFDoA

Different kinds of PFASs

Body burden (ng/g wet weight)

Fig. 3. Freely dissolved concentrations of PFASs in the exposure systems with different concentrations of humic acid (HA)/albumin.

5000 4500 4000 3500 3000 2500 2000 1500 1000 500 0

Control

1 mg/L Albumin

1 mg/L Peptone

1 mg/L fulvic acid

1 mg/L humic acid

a

a ab ab

ab a

aa a

b

b

b

a ab a a aa a b b b

PFOS

PFOA

PFNA

bb

b

c c

b

c

c

PFDA

PFUnA

PFDoA

Body burden (ng/g wet weight)

Different kinds of PFASs 3500 3000

Control

10 mg/L Albumin

10 mg/L Peptone

10 mg/L fulvic acid

a

2500 2000 b

bc

ab

b

a

a

a a

c

1000

ababab

500 PFOS

a

a

a

1500

0

10 mg/L humic acid

bbc b c

PFNA

b

b

b

b

PFOA

bb b b

aa

PFDA

PFUnA

PFDoA

Body burden (ng/g wet weight)

Different kinds of PFASs

3.3. Comparing the effects of the four DOM types on PFAS bioaccumulation

3500 3000

Control

20 mg/L Albumin

20 mg/L humic acid

20 mg/L Peptone

20 mg/L fulvic acid

a

a

2500

b

2000 a

1500 1000

c

500 0

a

a b

b

a a a ab ab b

PFOS

PFOA

ab ab

b

bc b

b b bb

b

c

PFNA

PFDA

bc c

bc

PFUnA

et al. (2013b) that the ammonia and urea excretion rates from D. magna were reduced by three natural DOMs and one commercial humic acid (Aldrich). On the basis of the above results, it can be deduced that during the uptake phase, both humic substances and protein compounds can bind with PFASs and then reduce the freely dissolved concentrations of PFASs, and this reduction leads to a decreased ku. The correlation analysis showed that there was a significant positive correlation between the freely dissolved concentration and ku for each PFAS (r > 0.83, n = 7, p < 0.05). In the meantime, because some studies have shown that humic substances can be absorbed by aquatic organisms (Roditi et al., 2000; Matsuo et al., 2006), HA, FA, peptone, and albumin might also be absorbed by D. magna in the present study, and they could bind with PFASs in the inner body of D. magna. Because of their large molecular size and hydrophobicity, the DOM-bound PFASs were harder to eliminate from the organism than the freely dissolved PFASs, leading to a decreased depuration rate in the presence of DOM. However, more research should be conducted to obtain direct evidence for this mechanism. Based on this inference, it is possible to provide a reasonable explanation for the effects of HA and albumin concentrations on PFAS bioaccumulation. D. magna ingested the freely dissolved PFASs and eliminated them at a regular rate in the absence of DOM. At a lower HA/albumin concentration (1 mg L1 in this experiment), HA/albumin and PFAS binding in the water phase reduced the freely dissolved concentrations of PFASs and led to a decrease in the uptake rate (ku). However, the HA/albumin and PFAS binding in the inner body of D. magna would also decrease the elimination/depuration rates (kd) of PFASs, and the decrease of kd prevailed over that of ku. Thus, the BAF value increased under the lower HA/albumin concentration. With the increased HA concentration, the ku was further decreased. However, the HA quantity in the inner body of D. magna might not increase with the HA concentration in the exposure solution because it might reach a maximum capacity in D. magna when the HA was at 1 mg L1. As a result, the kd value stayed nearly constant when the HA concentration increased from 1 to 20 mg L1 (Table 2). Because the ku value decreased while the kd almost remained constant, the BAF value decreased at a relatively higher HA concentration. For albumin, as shown in Table 2, although both the ku and kd values were further decreased with the increased albumin concentration, the decrease of ku might prevail over that of kd, leading to a reduction in the BAF value at a relatively higher albumin concentration. Similar to HA and albumin, FA and peptone affected the bioaccumulation of PFASs by influencing the depuration rates of PFASs in D. magna in addition to their freely dissolved concentrations and uptake rates.

c

PFDoA

Different kinds of PFASs Fig. 4. Comparison of the effects of different types of DOM on the bioaccumulation of PFASs (Significant difference exists between the groups with different letters (a, b, c, and d) (P < 0.05) and no significant difference between the groups with at least one same letter (P > 0.05)).

As shown in Fig. 4, the effect of HA and albumin with larger molecular sizes was different from that of fulvic acid and peptone with smaller molecular sizes. At the 1 mg L1 concentration, HA and albumin enhanced the bioaccumulation of all tested PFASs, whereas FA and peptone only enhanced the bioaccumulation of shorter-chain PFASs, and they inhibited the bioaccumulation of longer-chain PFASs (PFDA, PFUnA, and PFDoA). When the concentration came to 10 mg L1, HA and albumin decreased the bioaccumulation of all tested PFASs; however, FA and peptone still enhanced the bioaccumulation of shorter-chain PFASs except for the effect of peptone on PFOA. When the concentration reached 20 mg L1, all four DOM types decreased the bioaccumulation of all tested PFASs, but the decreasing ratios were different between the HA/albumin and fulvic acid/peptone groups.

X. Xia et al. / Chemosphere 119 (2015) 978–986

Furthermore, although the partition coefficients of PFASs between albumin and water were significantly higher than the partition coefficients between humic acid and water, their effects on PFAS bioaccumulation in D. magna were comparable (Fig. 4). This finding is due to the fact that the relatively higher value of log KALB led to a lower freely dissolved PFAS concentration in albumin solution than in the HA solution, resulting in a lower uptake rate constant (ku); this trend is demonstrated by the results shown in Table 2. However, because the absorption of albumin to D. magna might be greater than that of HA at a higher DOM concentration (10 and 20 mg L1), the kd values of PFASs in the presence of albumin were lower than those in the presence of HA. In addition, as shown in Table S5, the BAFfreely values of PFASs based on their freely dissolved concentrations in the presence of albumin were much higher than those in the presence of HA; this finding suggested that albumin will exert a stronger influence on the depuration rates of PFASs than HA. Therefore, these effects on the uptake and depuration rate constants of PFASs resulted in a comparable net effect between humic acid and protein. In addition, although the composition and origin of peptone and fulvic acid were different, their effects on PFAS bioaccumulation in D. magna were similar. This similarity suggests that although PFASs are a type of proteinophilic compounds, similar to protein compounds, the humic substances will also have a significant effect on PFAS bioavailability and bioaccumulation in aquatic organisms. Furthermore, although humic acid and fulvic acid belong to humic substances, their effects on PFAS bioaccumulation were significantly different, and this was also true for albumin and peptone. Therefore, all DOM types should be accounted for when studying the bioavailability and bioaccumulation of PFASs in aquatic environments. Many direct interactions of DOM with aquatic organisms have been demonstrated; DOM molecules may accumulate on biological surfaces, influence membrane permeability, and affect basic physiological functions (Campbell et al., 1997; Glover et al., 2005; Galvez et al., 2008; Al-Reasi et al., 2013a). For instance, recently published evidence demonstrates that DOM affects Na+ transport, diffusive permeability, and the electrical properties of the gills of fish and crustaceans in a manner that will promote Na+ homeostasis; these actions could thereby protect against metal toxicity by physiological mechanisms (Wood et al., 2011). Although these investigations were focused on DOM’s effect on metal toxicity and bioaccumulation, it is possible that its effects on the physiology of aquatic organisms might also affect the bioaccumulation of PFASs and other HOCs.

4. Conclusions The influence of humic substances and protein compounds on the bioaccumulation of six types of PFASs in D. magna was compared in the present study, and the main conclusions were drawn as follows. The DOM effect on PFAS bioaccumulation depended on the concentrations of DOM. At a lower level (1 mg L1), HA and albumin enhanced the bioaccumulation of all tested PFASs, whereas FA and peptone only enhanced the bioaccumulation of shorter-chain PFASs (PFOS, PFOA, and PFNA). However, all four DOM types decreased the bioaccumulation of all tested PFASs at a higher level (20 mg L1). This is due to the fact that DOM not only reduced the bioavailable concentrations and uptake rates of PFASs but also lowered the elimination rates of PFASs in D. magna, and these opposite effects would change with different DOM types and concentrations. Although the partition coefficients of PFASs between humic acid and water were much lower than those between albumin and water, their effects on PFAS bioaccumulation in D. magna were comparable. These findings suggest that although

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PFASs are a type of proteinophilic compounds, humic substances also have important effects on their bioavailability and bioaccumulation in aquatic organisms. Therefore, all DOM types should be considered when studying the bioavailability and bioaccumulation of PFASs in aquatic environments. The results obtained in the present research also suggest that, apart from the reduced bioavailability of PFASs caused by DOM, the DOM effect on the physiology of aquatic organisms might also affect PFAS bioaccumulation in D. magna. Further work should address the effect of DOM on the physiology and biochemistry of organisms, and the effects of these actions on the bioaccumulation of PFASs and other organic pollutants by organisms.

Acknowledgements This study was supported by the National Science Foundation for Distinguished Young Scholars (No. 51325902), the National Science Foundation for Innovative Research Group (No. 51121003), and the National Science Foundation of China (No. 51279010).

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