Sorption and desorption of organic UV filters onto microplastics in single and multi-solute systems

Environmental Pollution 254 (2019) 113066

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Sorption and desorption of organic UV filters onto microplastics in single and multi-solute systems* Wai-Kit Ho a, Kelvin Sze-Yin Leung a, b, * a b

Department of Chemistry, Hong Kong Baptist University, Kowloon Tong, Hong Kong Special Administrative Region HKBU Institute of Research and Continuing Education, Shenzhen Virtual University Park, Shenzhen, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 February 2019 Received in revised form 3 June 2019 Accepted 15 August 2019 Available online 17 August 2019

Sorption studies of organic pollutants by microplastics (MPs) in single-solute systems are well established in the literature. However, actual aquatic environments always contain a mixture of contaminants. Prediction of the fate and biological effects of MPs-mediated chemical exposure requires a better understanding of sorption-desorption processes of multiple organic contaminants by MPs. In this study, the altered sorption and desorption behaviors of individual organic UV filters (BP-3 and 4-MBC) in the presence of cosolutes (BP-3, 4-MBC, EHMC and OC) on two types of MPs (LDPE and PS) were examined. In most cases, co-occurrence of other organic UV filters appeared to have an antagonistic effect on the sorption of primary solute, which was consistent with trends found in previous studies. Nevertheless, the sorption uptake of 4-MBC as primary solute on PS was enhanced in the presence of cosolute(s), arising presumably from solute multilayer formation caused by laterally attractive p-p interactions between adsorbed cosolute(s) and 4-MBC molecules. Such formation of multilayer sorption in multi-solute systems depends on the solute hydrophobicity and concentration as well as inherent sorptivity of MPs. Our further desorption experiments revealed that the bioaccessibility of primary solute was significantly elevated with cosolutes, even though competitive sorption was observed under the same experimental conditions. These findings supplement the current knowledge on sorption mechanisms and interactions of multiple organic contaminants on MPs, which are critical for a comprehensive environmental risk assessment of both MPs and hazardous anthropogenic contaminants in natural environments. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Organic UV filter Microplastic Multi-solute system Competitive interaction Synergistic interaction

1. Introduction The worldwide production of plastics has been reported to have reached 335 million tons in 2016 (PlasticsEurope, 2017), with production expected to be almost quadrupled by 2050 (MacArthur et al., 2016). Much of this plastic ends up in the sea, partly from direct deposit (e.g., by careless individuals) but primarily from inefficient waste management systems (Jambeck et al., 2015). Thus, given the expected increase in production, without improved waste management systems, plastic debris in the marine environment can be predicted to become a global environmental threat (Alimi et al., 2018). While the plastic itself causes problems, degradation of marine plastic debris into microplastics (MPs) under prolonged

* This paper has been recommended for acceptance by Maria Cristina Fossi. * Corresponding author. Department of Chemistry, Hong Kong Baptist University, Kowloon Tong, Hong Kong Special Administrative Region. E-mail address: [email protected] (K.S.-Y. Leung).

https://doi.org/10.1016/j.envpol.2019.113066 0269-7491/© 2019 Elsevier Ltd. All rights reserved.

exposure to solar radiation, in combination with mechanical abrasion, microbial activity and wave action, poses its own increasingly severe problems (Wright and Kelly, 2017). The term, MPs, is recently redefined as plastic particles of less than 1000 mm (Hartmann et al., 2019). The potential environmental risks of MPs are attracting more and more concern as evidence of their occurrence in various oceanic compartments, marine biota and aquatic products,
et al., together with toxicity, accumulates (Carbery et al., 2018; de Sa 2018; Rezania et al., 2018). One of the major concerns is that MPs exhibit strong affinities for hazardous persistent organic pollutants (POPs) in the aquatic environment because of their highly hydrophobic surface and large surface-to-volume ratio (Liu et al., 2016). The interactions of organic pollutants with MPs may change the environmental fate, behavior and bioavailability of the pollutants (Duis and Coors, 2016), as well as synergistic toxicity to biota (Chen et al., 2017; Jeong et al., 2018). In this regard, knowledge of sorption behavior of organic pollutants on MPs is essential for environmental risk assessment of both organic pollutants and MPs.

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Much research has been done examining the sorption of organic pollutants on MPs with various intrinsic (e.g., type of MPs, weathered MPs) and extrinsic properties (e.g., salinity, temperature, dissolved organic matter), and with different target compounds (e.g., DDT, PAHs, PCBs, antibiotics) in aqueous systems (Alimi et al., 2018; Li et al., 2018b; Wang et al., 2018). However, many of the studies have only examined single-solute systems whereas actual aquatic environments have mixtures of contaminants present. Prediction of the fate and biological effects of MPsmediated chemical exposure in natural environments requires a better understanding of sorption and desorption processes of multiple organic contaminants by MPs. The sorption behavior of hydrophobic organic contaminants (HOCs) in a multi-solute system can differ substantially from the behavior of those in a single-solute system according to several recent reports (Bakir et al., 2012; Wang and Wang, 2018; Wu et al., 2019). Specifically, competitive sorption and displacement of a primary solute on MPs would likely be observed in the presence of cosolute(s), thereby reducing its bioaccessibility and possibility of the overall toxicity of HOCs associated with MPs. Nevertheless, these studies have been limited to the characterization of competitive behavior of contaminants in multi-solute systems. None of these studies have elucidated fundamental principles of the competitive behavior of contaminants in multi-solute systems. Therefore, a full understanding of the factors and mechanisms controlling the simultaneous sorption of multiple organic contaminants on MPs has not yet been achieved. Apart from POPs, chemicals derived from personal care products (PCPs) are another important class of contaminants of emerging concern (CECs) due to their ubiquitous occurrence in various aquatic ecosystems and potential health and environmental risks (Ebele et al., 2017). As ingredients of these PCPs, organic UV filters have recently raised significant concerns due to their extensive consumption, persistent input and endocrine-disrupting potential (Brausch and Rand, 2011; Montes-Grajales et al., 2017). Organic UV filters are widely included in sunscreens and cosmetics to protect skin from damage upon UV radiation exposure (Ramos et al., 2015). They are also incorporated into a wide range of products including adhesives, packaging materials, plastics and rubber as sun blocking agents to retard or prevent UV degradation of polymeric materials, thus extending the lifetime of these products (Anderson and Castle, 2003; Gackowska et al., 2014; Rani et al., 2017). Polyethylene (PE) and polystyrene (PS), two of the most widely used plastics, are more susceptible to weathering by sunlight radiation than other plastics (Alimi et al., 2018). As far as we know, the study of sorption behavior of PCPs on MPs is rare. In this context, organic UV filters were selected as model compounds in this study for exploring the sorption behavior of multiple organic pollutants on MPs. The key objectives of this work were (i) to characterize the altered sorption behavior of organic UV filters on two types of MPs (LDPE and PS) in a multi-solute system as compared to that of a single-solute system; (ii) to elucidate the factors and mechanisms controlling synergistic sorption processes of primary solutes in different complex mixtures conditions; and (iii) to examine the change in bioaccessibility of organic UV filters adhered to MPs under simulated digestive fluid of marine biota in a multi-solute system.

4-methylbenzylidene camphor (4-MBC), ethylhexyl methoxy cinnamate (EHMC), and octocrylene (OC). They were obtained either from Alfa Aesae (UK) or Sigma-Aldrich (USA) with a minimum purity of 99%. Structure and physicochemical properties of these organic UV filters are listed in Table S1. BP-3-d5, 3-benzylidene camphor (3-BC) and EHMC-d15, used as internal standards for liquid-liquid extraction, were supplied by CDN Isotope (Canada), MP Biomedical (USA) and Sigma-Aldrich, respectively. Sodium taurocholate was purchased from Acros Organics (USA). Solvents, including acetonitrile, ethyl acetate, methanol and n-heptane, were HPLC grade or above and were obtained from Duksan Pure Chemicals (South Korea). Individual stock solutions of the four organic UV filters were prepared in methanol and stored in the dark at 4
C. Artificial seawater was prepared according to standard procedures of ASTM D1141 in ultrapure water (ASTM, 2013); 200 mg/L of NaN3 was added to inhibit microbial activity. The initial pH of artificial seawater after adjustment with 0.1 M NaOH was 8.2. Microscopic particles of low-density polyethylene (LDPE) and polystyrene (PS) were purchased from Goodfellow Cambridge Ltd. (UK). The particle sizes of LDPE and PS were 300 mm and 250 mm, respectively. Both types of MPs were washed three times with methanol to remove any existing chemical contamination and airdried before use. Details of the characterization of MPs are provided in the Supporting Information (SI). 2.2. Experimental design 2.2.1. Single-solute sorption experiments All batch experiments were performed using glass centrifuge tubes with PTFE-line screw caps as the reactor system. Each tube was filled with 25 mL of artificial seawater, to which 10 mg of MPs was added. The aqueous phase of each reactor was spiked with 50 mL of methanol solution containing a predesignated quantity of organic UV filter. Initial concentration range for each solute in the single-solute sorption experiment was 20e200 mg/L. The relative volume of methanol in the aqueous solution was the same for all the samples and kept below 0.2% (v/v) to minimize cosolvent effects (Pinal et al., 1990). The tubes were capped and equilibrated on an orbital shaker (150 rpm) in the dark at 20 ± 2
C for 48 h as preliminary experiments had showed that sorption equilibrium was established within 36 h (Figs. S2e3). Upon equilibrium, samples were passed through 0.45 mm Whatman GF/C glass fiber filters to separate the aqueous solution and plastic particles. For more information regarding chemical analysis, quality assurance and quality control refer to the SI. 2.2.2. Multi-solute sorption experiments Procedures of multi-solute sorption experiments were the same as those of single-solute sorption experiments except for the content of spiking solvent. Different stock solutions containing fixed concentration of primary solute (20 mg/L) with varying levels of cosolute(s) concentration (0e200 mg/L) were prepared and spiked into each reactor simultaneously. Various combinations of primary solute and cosolute(s) in different test mediums were designed to improve mechanistic understanding of altered sorption properties caused by complex mixtures. The specific conditions of each experiment are summarized in Table 1 for easy reference.

2. Materials and methods 2.1. Materials and chemicals Organic UV filters in the present study were selected according their ubiquitous environmental occurrence and high ecological risk (Sang and Leung, 2016). Four were chosen: benzophone-3 (BP-3),

2.2.3. Preliminary desorption experiments Desorption experiments were conducted in simulated digestive fluid of marine biota following the method of Teuten et al. (2007) with modifications. In detail, organic UV filters were sorbed to MPs as described previously for multi-solute systems (Set 1e4), but a higher initial concentration of primary solute (100 mg/L) was used

W.-K. Ho, K.S.-Y. Leung / Environmental Pollution 254 (2019) 113066 Table 1 Conditions of different setups in multi-solute sorption experiments. Setup

Sorbent

Primary Solutea

Cosolute(s)b

pH

I. Characterization of the sorption behavior of organic UV filters in multisolute systems 1 LDPE BP-3 4-MBC þ EHMC þ OC 8.2 2 PS BP-3 4-MBC þ EHMC þ OC 8.2 3 LDPE 4-MBC BP-3 þ EHMC þ OC 8.2 4 PS 4-MBC BP-3 þ EHMC þ OC 8.2 II. Elucidation of the fundamental mechanisms of synergistic sorption in complex mixtures conditions 5 PS 4-MBC BP-3 8.2 6 PS 4-MBC EHMC 8.2 7 PS 4-MBC OC 8.2 8 PS BP-3 4-MBC þ EHMC þ OC 4.0 a

The initial concentration of primary solute in solute mixtures was fixed at 20 mg/

L. b The initial concentration of individual cosolute in solute mixtures was identical, with each ranged from 0 to 200 mg/L.

to make the difference caused by cosolute effects more noticeable. Then, 25 mL of simulated digestive fluid (15.5 mM sodium taurocholate in seawater) was added to an amber vial containing 10 mg of the collected MPs particles. The vial was sealed and shaken continuously in the dark at 20
C for 3 h to simulate the digestive system of marine biota (Bakir et al., 2016, 2014; Teuten et al., 2007). 2.3. Instrumental analysis Quantification of organic UV filters in each phase was achieved with an Acquity Ultra Performance Liquid Chromatography system hyphenated to a Xevo-TQ triple quadrupole mass spectrometer (UPLC-MS/MS) (Waters, USA). Further details of chromatographic separation and MS instrument conditions are described in SI. 2.4. Statistical analysis All experiments were repeated in triplicate. Data were compared by one-way analysis of variance (ANOVA) and Tukey's honestly significant difference (Tukey's HSD) post hoc test using SPSS version 22.0 (SPSS Inc., Chicago). For all statistical tests, p values < 0.05 were regarded as statistically significant differences among experimental groups. Sorption isotherms of organic UV filters by MPs were generated by both the linear and Freundlich models. (1). Linear model: qe ¼ Kd Ce (2). Freundlich model: log qe ¼ log KF þ nF log Ce where qe (mg/kg) is the sorbed concentration of solute at equilibrium; Ce (mg/L) is the residual aqueous concentration of solute at equilibrium; Kd (L/kg) is the sorption equilibrium partition coefficient at a specified condition; KF (L/kg) is the Freundlich isotherm coefficient and nF is the Freundlich exponent, which is often applied as an indicator of isotherm nonlinearity (proportional to the departure of nF from 1). 3. Results and discussion 3.1. Single-solute sorption experiments Sorption experiments were firstly examined in single-solute isotherms to provide a basic understanding of main mechanisms governing sorption of organic UV filters by MPs. The sorption parameters derived from the linear and Freundlich models are listed in Table 2. All the individual sorption isotherms were adequately

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fitted with the Freundlich model with R2 values > 0.98. Sorption isotherms of organic UV filters studied here by LDPE were highly linear with nF values close to 1, suggesting the sorption processes on LDPE are dominated by partitioning mechanism (Hüffer and Hofmann, 2016; Velzeboer et al., 2014). Due to its aliphatic nature with no specific functional groups, LDPE was only able to interact with the organic UV filters by means of relatively weak van-der-Waals forces rather than other mechanisms (e.g. pp interaction, hydrogen bonding) (Guo et al., 2012). Different from LDPE, PS exhibited nonlinear sorption behaviors for all tested compounds with nF values of 0.79e0.91. Negative departures from linearity indicate that sorption processes on PS are governed by both linear partitioning and nonlinear adsorption (i.e., surface adsorption and pore-filling) mechanisms (Hüffer and Hofmann, 2016; Teuten et al., 2009). The nonlinear adsorption processes for PS could be attributed to the high-energy adsorption sites provided by external surfaces and internal nanopores. Unlike LDPE, PS possessed heterogeneous components include benzene rings and methylene chains, resulting in surface heterogeneity. The dissimilar sorption affinity among specific sorption sites on external surfaces of PS could lead to sorption isotherm nonlinearity (Xing, 2001). Besides, PS contains substantial closed internal nanopores that can serve as additional adsorption sites, because of its rigidity. The high affinity sorption sites provided by these internal nanovoid spaces could be the major reason for nonlinear sorption behaviors in PS (Pignatello and Xing, 1996; Teuten et al., 2009). Apparently, the nF est values of the targeted compounds onto PS followed the order of OC z EHMC > 4-MBC > BP-3, which followed the reverse order of their molecular size. This correlation implies that the porefilling mechanism is sorbate-size-dependent, as some of internal nanovoids might be inaccessible to larger sorbates (Ran et al., 2004). Hence, the difference between values of nF and nF est (especially for 4-MBC) is possibly due to incomplete solid phase extraction; that is, a portion of adsorbed solute could be trapped in these highly adsorptive internal nanopores of PS, resulting in underestimation of qe , and subsequently the nF values (Liu et al., 2018). The sorption behaviors of organic UV filters with regard to MPs can also be described using partition coefficients (logKd ). The log Kd of studied pollutants sorbed onto different types of MPs were clearly positively correlated with their octanol-water partition coefficients (logKow ), which is in accordance with earlier studies (Rodrigues et al., 2019; Wang et al., 2018). The trend indicates that hydrophobic interactions are the principal driving forces for partition-adsorption processes (Velzeboer et al., 2014). Experimental resultsdi.e., the logKd values of organic UV filters sorbed onto LDPE were apparently higher than those of PSdalso suggest that rubbery polymer has higher sorption affinity toward organic UV filters. This difference, compared to a lower sorption affinity for HOCs in PS, could be explained by differences in the degree of crosslinking and crystallinity of the two polymers. Due to the presence of benzene rings in the polymeric skeleton, the polymer segments of PS present greater cohesive forces and are more condensed (i.e., having fewer amorphous sorption domains) (Guo et al., 2012; Teuten et al., 2009). Such structures lead to a reduced mobility of PS chain segments and lower free volume in the polymer matrix of PS, thereby restricting the partitioning of solutes into PS (Pascall et al., 2005). Therefore, due to its more condensed structure with substantial internal nanopores, sorption on PS would be masked by surface adsorption and pore-filling instead of partitioning (Guo et al., 2012; Rodrigues et al., 2019).

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Table 2 Sorption parameters derived from the linear and Freundlich models for individual sorption of organic UV filters onto LDPE and PS. Compound

Linear model LDPE log Kd (L/kg)

BP-3 4-MBC EHMC OC

2.52 4.15 5.52 5.40

± ± ± ±

Freundlich model PS

0.01 0.05 0.03 0.06

LDPE

log Kd (L/kg) 2.19 2.82 5.07 5.14

± ± ± ±

0.03 0.05 0.04 0.05

PS

log KF (L/kg) 2.47 4.11 5.51 5.43

± ± ± ±

0.03 0.09 0.04 0.05

nF

nF

1.02 1.03 1.00 1.01

0.97 1.00 0.98 1.00

est:

a

R2

log KF (L/kg)

0.998 0.994 0.991 0.988

2.68 3.04 5.12 5.21

± ± ± ±

0.09 0.05 0.02 0.02

nF

nF

0.79 0.91 0.86 0.86

0.79 0.81 0.84 0.84

est:

a

R2 0.997 0.998 0.990 0.997

a nF est: values were calculated from mass balance equation [qe est: ¼ (Ci e Ce )V/m], where Ci ¼ initial aqueous solute concentration; Ce ¼ residual aqueous solute concentration at equilibrium; V ¼ volume of solution; m ¼ initial mass of MPs (n ¼ 3, mean ± SD).

3.2. Characterization of sorption behavior of organic UV filters in a multi-solute system Possible competitive or synergistic effects on sorption behavior of primary solute were first studied in a multi-solute system. The behavior of a given solute in multi-solute systems is more realistic and representative of actual environmental conditions. BP-3 and 4MBC were employed as model primary solutes in the following studies. The influences of cosolute on logKd of two primary solutes by both MPs are illustrated in Fig. 1. Sorption of primary solute (either BP-3 or 4-MBC) onto LDPE was slightly suppressed by adding three other organic UV filters as cosolutes; the success of this strategy is shown by the decrease in logKd of the primary solute (Fig. 1). The competitive sorption between primary solute and cosolute(s) is always emphasized in the literature, in which overlapping of sorption sites has been published as the major mechanism of competitive sorption processes (Bakir et al., 2012; Wang and Wang, 2018; Wu et al., 2019). The effects of cosolutes on sorption of BP-3 by PS were more pronounced compared to LDPE, as the relative impact of competitive sorption onto PS was 3.3 times higher than that onto LDPE (Setup 1 and 2 in Table S5). The more pronounced displacement could be explained by the surface and structural heterogeneity of PS. The surface heterogeneity of PS is arisen from the incorporation of benzene rings into polymeric skeleton, resulting in heterogeneous energy distribution of surface sorption sites. Due to the aromatic structure of organic UV filters, they would be more preferentially sorbed to benzene rings of PS through pp interaction (Jonker and Koelmans, 2002). This leads to a stronger

Fig. 1. Effects of cosolute on the uptake of primary solute (BP-3 and 4-MBC) by LDPE and PS in multi-solute systems. The relative log Kd is defined as the log Kd of individual primary solute over the log Kd of primary solute with cosolute (n ¼ 3, mean ± SD).

competition for specific sorption sites on external surfaces of PS. In terms of structural heterogeneity, PS contained substantial internal nanopores with high sorption affinity as previously mentioned. The isotherm linearity of a solute increases (nF more close to 1) in the presence of cosolute(s) (Table S6), which indicates pore competitions among different sorbates onto PS (Bakir et al., 2012; Teuten et al., 2009). Hence, pore competition could be another important mechanism causing more pronounced competitive sorption onto PS. Nevertheless, the sorption of 4-MBC onto PS was significantly enhanced by the presence of cosolutes, as illustrated by the increase in logKd of primary solute (Setup 4 in Fig. 1). The result indicates that cosolutes have a synergistic, rather than a competitive, effect on the sorption of primary solute. There appear to be no other reports of enhanced sorption of primary solute onto MPs induced by the presence of cosolutes in the system. However, synergistic sorption of organic compounds in complex mixtures was observed in experiments utilizing other carbon-based materials as sorbents (Brusseau, 1991; Jin et al., 2014; Yang et al., 2010, 2006). Among these studies, synergistic sorption processes were mainly caused by the formation of solute multilayers on sorbent surface. Briefly, these studies proposed that the solute-coated sorbent surfaces could serve as additional sorption sites for other solutes, with a lower potential energy as compared with uncoated sorbent surface. In this regard, the surface adsorption of primary solute in multisolute systems was contributed by both sorbent surface and solute-coated sorbent surface. Based on the results discussed above, the enhanced sorption of 4-MBC onto PS in multi-solute systems presumably arises from laterally attractive interactions between adsorbed cosolutes (BP-3, EHMC and OC) and 4-MBC molecules. Two possible types of attachment of cosolute molecules to PS could occur, either through (i) pp interactions with aromatic rings or (ii) hydrophobic interactions with hydrophobic alkyl chains. Considering the molecular structure of organic UV filters studied here, aromatic rings and alkenyl groups of these compounds should be responsible for the increased sorption capacity of primary solute because these structures create the possibility of forming favorable pp interactions with surrounding primary solute molecules (Jonker and Koelmans, 2002). Hence, displacement of primary solute in the former mechanism could be diminished due to formation of solute multilayers in a multi-solute system. Meanwhile, sorption of primary solute could be enhanced in the latter mechanism as cosolutes might complementarily occupy different sorption sites (Zhang et al., 2012). The observed synergistic sorption indicates that the enhanced surface adsorption of primary solute resulting from solute-solute interaction could override the suppressed uptake of primary solute caused by competition for sorption sites and nanopores.

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3.3. Elucidation of the synergistic sorption mechanisms in complex mixtures Previous results show that multi-solute systems can exhibit distinctly different sorption behaviors, as both competitive and synergistic effects of the cosolutes on the sorption of primary solute have been observed. Because current understanding of the balance between these two opposite effects is limited, it deserves further study. We therefore performed sorption experiments with different complex mixtures to improve mechanistic understanding of factors controlling the sorption of multiple organic contaminants on MPs. Experimental results of various combinations of primary solute and cosolute(s) at different test mediums are presented in Figs. 2 and 3. 3.3.1. Change in initial concentration of cosolute The relative impact of cosolute(s) on the sorption of primary solute was directly linked to initial aqueous concentration of cosolute(s) and type of MPs, as illustrated in the results of this study (e.g., Fig. 2). The dissimilar response in cosolute effect between two types of MPs (Setup 3 and 4) indicates difference in the significance of solute multilayers for two polymers, which could be explained by differences in their dominant sorption mechanisms. Compared with LDPE, PS shows a much higher relative contribution of surface adsorption than partitioning due to its aforementioned more condensed structure. In this regard, a stronger competition of sorption sites and nanopores in higher cosolute concentration could still be compensated for by the formation of solute multilayers on sorbent surface of PS, but this could not happen for LDPE. 3.3.2. Change in hydrophobicity of cosolute The degree of synergistic sorption of primary solute could be expressed as a function of cosolute hydrophobicity (Fig. 2), which is determined by the mass and nature of the cosolute attached to a sorbent surface. With the increase in hydrophobicity of cosolute, more solute-coated sorbent surfaces are formed due to enhanced hydrophobic interactions with PS, together with stronger attractive forces for the formation of solute multilayers. The larger cooperative effects on 4-MBC sorption observed (þ23.29%, Table S5) in the multi-solute system (using BP-3, EHMC and OC as cosolutes) could be also explained by the greater number of solute-coated sorbent surfaces available for multilayer sorption. Nevertheless, there appear to be hydrophobicity cutoff effects in the formation of solute multilayers, as the relative impact of synergistic sorption of 4-MBC with EHMC (logKow : 5.80) was 1.3 times

Fig. 3. Change in log Kd of primary solute (BP-3 and 4-MBC) with different values of hydrophobicity onto PS in binary-solute systems (n ¼ 3, mean ± SD).

that with OC (log Kow : 6.88) (Setup 6 and 7 in Table S5). In this case, steric hindrance effects of adsorbed cosolute molecules (i.e., molecular size of OC > EHMC) should also be considered in multilayer sorption, especially for these highly hydrophobic organic compounds (log Kow > 5e6) (Jin et al., 1994). The possibility of favorable pp stacking between the aromatic compounds and sorbent surfaces could be suppressed in larger molecules as they are less likely to come close to the sorption surface (Jonker and Koelmans, 2002). 3.3.3. Change in hydrophobicity of primary solute Hydrophobicity of primary solute could also be a major parameter determining the sorption behavior of primary solute in the multi-solute system. The hydrophobicity of primary solute examined in the present study followed the order of 4-MBC (log Kow : 4.95) > BP-3pH 4.0 (log Dow : 3.62) > BP-3pH 8.2 (log Dow : 2.67), which was in accordance with the change in log Kd of these systems (Fig. 3, Table S5). The balance between these two opposite sorption effects could be elucidated more clearly using ionizable BP-3 as model primary solute. The diminished suppression of BP-3 onto PS in a multi-solute system at acidic pH can be interpreted from three aspects. First, the electrostatic repulsion among BP-3 molecules (pka 7.07) and surface of PS (point of zero charge: 4.7 ±0.2) could be pronounced in artificial seawater (pH 8.2) as both were negatively charged (Zhang et al., 2018). Hence, the electrostatic repulsion caused by similarity in charge would be minimized at acidic pH as BP-3 molecules would be mainly presented in neutral form. Second, neutral BP-3 molecules could have stronger competition advantages for sorption sites as indicated by their higher log Kow , thus reducing the possibility of displacement by other cosolute molecules. Third, cooperative interactions among more hydrophobic neutral BP-3 molecules and solute-coated sorbent surface would be more favored due to stronger hydrophobic interactions. Therefore, differences between two opposite effects could be much narrower for the sorption of BP-3 in a multi-solute system at acidic pH as shown by the decreased relative impact of competitive sorption from 7.08% to 1.51% after pH adjustment (Table S5). 3.4. Bioaccessibility of organic UV filters on MPs in simulated digestive fluid

Fig. 2. Effects of cosolute on the uptake of primary solute (4-MBC) by PS in binary- and multi-solute systems (n ¼ 3, mean ± SD).

To mimic the effects of cosolute on MP-mediated chemical exposure caused by MPs ingestion by marine biota, simulated

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digestive fluid was used as a desorption medium. The desorption time was restricted to 3 h, primarily due to limited digestive time in marine biota (Lee et al., 2019; Mohamed Nor and Koelmans, 2019). Generally, variations in primary solute desorption from MPs in a multi-solute system could be predicted from the trends observed in the previous parts of this study. That is, we expected to find that the bioaccessibility of primary solute would be suppressed by the competitive sorption and displacement among multiple organic compounds on MPs. Instead, the cosolute effects showed a distinctly different response between sorption (downward trend, Fig. 4a) and desorption behavior (upward trend, Fig. 4b) of multisolute systems on PS using BP-3 as primary solute. Differences in bioaccessibility of sorbed cosolutes between two types of MPs might provide some information to interpret this discrepancy. It could be noticed that the bioaccessibility of organic UV filters in LDPE was much larger than that of PS (Table S7), even though the qe values of EHMC and OC in LDPE and PS were quite close to each other (Table S8). The presence of substantial internal nanopores in glassy PS should account for the underestimated amount of sorbed solutes. Ran et al. (2004) examined the sorption and desorption behaviors of HOCs in glassy sediment. The results suggested that desorption hysteresis of HOCs was observed due to slow pore diffusion and entrapment of sorbed molecules within narrow pores. Hence, the fraction of organic pollutants sorbed on the external surface of PS and into the polymer matrix would be more mobile, and thus bioaccessible, than those trapped in the

internal nanopores. Based upon the above discussion, the reverse trend of the cosolute effects on the fate of BP-3 in PS should be due to difference in implication of pore-filling mechanism between sorption and desorption processes. The cosolutes not only enhanced the surface adsorption of BP-3 molecules through multilayer sorption, but also excluded them from less mobile glassy polymeric sorption domains (i.e., internal nanopores) in PS. This observation further confirms the occurrence of solute-solute interaction among multiple organic contaminants on the surface of MPs. Apart from the increased bioaccessibility of primary solute, the formation of solute multilayers caused by lateral interactions between different solutes in a multi-solute system should also be considered in terms of toxicity. Li et al. (2018a) discovered that the bioaccumulation of multiple organic UV filters (BP-3, EHMC and OC) in marine biota was significantly elevated as compared to their individual constituents. Potentially, the overall toxicity to the ecosystem might be elevated by toxicologically synergistic effect resulted from solute-solute interaction. Therefore, the synergistic sorption of environmental contaminants on MPs could result in more serious adverse effects to marine biota than that predicted by the competitive sorption model. Current limited understanding on sorption mechanisms and interactions of multiple organic pollutants on MPs may result in a large underestimation regarding the health and environmental hazards of both organic pollutants and MPs. 4. Conclusions Results of this study showed that distinctly different sorption behaviors could be exhibited in multi-solute systems, as both competitive and synergistic sorption behaviors have been observed. The relative contribution of the two opposite effects is controlled by the hydrophobicity and molar ratio of both solutes, together with inherent sorptivity of MPs. The synergistic sorption behavior in solute mixtures should not be overlooked as it does not only mean increased bioaccessibility of sorbed HOCs on MPs, but also the formation of solute multilayers between different HOCs in multi-solute systems. As a matter of fact, the concentration of HOCs adhered to environmental sampled MPs can be several orders of magnitude higher than those in natural sediments and ambient seawater (Mato et al., 2001; Wright et al., 2013). Owing to their strong sorption capacity, it is possible that MPs could be the platform, facilitating the formation of solute multilayers with potential joint toxicity in actual aquatic environments. In this regard, the synergistic sorption behavior of multiple organic contaminants on MPs could result in more serious adverse effects to marine biota than that predicted by the competitive sorption model. Proper understanding of altered sorption and desorption behaviors of organic contaminants in multi-solute systems is critical for accurately assessing the hazard enforced by MPs-mediated chemical exposure as the environmental fate, bioaccessibility and toxicity of HOCs associated with MPs could be strongly affected by the cooccurrence of multiple organic contaminants in natural environments. Declaration of interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Fig. 4. Effects of cosolute on the (a). sorption and (b). desorption behaviors of primary solute (BP-3 and 4-MBC) caused by LDPE and PS in multi-solute systems (n ¼ 3, mean ± SD).

Acknowledgements K. S. eY. Leung is grateful for funding support from the Inter-

W.-K. Ho, K.S.-Y. Leung / Environmental Pollution 254 (2019) 113066

institutional Collaborative Research Scheme (RC-ICRS/16-17/02B), Inter-disciplinary Research Matching Scheme (RC-IRMS/16-17/01A) and State Key Laboratory of Environmental and Biological Analysis (SKLP-1617-P03), Hong Kong Baptist University. Kelvin S. eY. Leung acknowledges the Science, Technology and Innovation Commission of Shenzhen (JCYJ20170817173243420) for funding support. W. -K. Ho is supported by a postgraduate studentship offered by the University Grants Committee. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.envpol.2019.113066. References Alimi, O.S., Farner Budarz, J., Hernandez, L.M., Tufenkji, N., 2018. Microplastics and nanoplastics in aquatic environments: aggregation, deposition, and enhanced contaminant transport. Environ. Sci. Technol. 52, 1704e1724. Anderson, W.A.C., Castle, L., 2003. Benzophenone in cartonboard packaging materials and the factors that influence its migration into food. Food Addit. Contam. 20, 607e618. ASTM, 2013. ASTM D1141-98(2013), Standard Practice for the Preparation of Substitute Ocean Water. ASTM International, West Conshohocken, PA (2013). https://doi.org/10.1520/D1141-98R13. Bakir, A., O'Connor, I.A., Rowland, S.J., Hendriks, A.J., Thompson, R.C., 2016. Relative importance of microplastics as a pathway for the transfer of hydrophobic organic chemicals to marine life. Environ. Pollut. 219, 56e65. Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Enhanced desorption of persistent organic pollutants from microplastics under simulated physiological conditions. Environ. Pollut. 185, 16e23. Bakir, A., Rowland, S.J., Thompson, R.C., 2012. Competitive sorption of persistent organic pollutants onto microplastics in the marine environment. Mar. Pollut. Bull. 64, 2782e2789. Brausch, J.M., Rand, G.M., 2011. A review of personal care products in the aquatic environment: environmental concentrations and toxicity. Chemosphere 82, 1518e1532. Brusseau, M.L., 1991. Cooperative sorption of organic chemicals in systems composed of low organic carbon aquifer materials. Environ. Sci. Technol. 25, 1747e1752. Carbery, M., O'Connor, W., Palanisami, T., 2018. Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environ. Int. 115, 400e409. Chen, Q., Yin, D., Jia, Y., Schiwy, S., Legradi, J., Yang, S., Hollert, H., 2017. Enhanced uptake of BPA in the presence of nanoplastics can lead to neurotoxic effects in adult zebrafish. Sci. Total Environ. 609, 1312e1321.
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