The effect of natural organic matter on the adsorption of microcystin-LR onto clay minerals

Colloids and Surfaces A 583 (2019) 123964

Contents lists available at ScienceDirect

Colloids and Surfaces A journal homepage: www.elsevier.com/locate/colsurfa

The effect of natural organic matter on the adsorption of microcystin-LR onto clay minerals Yen-Ling Liua, Harold W. Walkerb, John J. Lenharta, a b

T

⁎

Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH 43210, USA Department of Civil and Environmental Engineering, Worcester Polytechnic Institute, Worcester, MA 01609, USA

G R A P H I C A L A B S T R A C T

A R T I C LE I N FO

A B S T R A C T

Keywords: Microcystin Adsorption Desorption Clay Natural organic matter

In this study, we examined the extent and time-dependence in the adsorption and desorption of microcystin-LR (MCLR) to kaolinite, illite and montmorillonite as a function of pH, electrolyte cation and Suwanee River fulvic acid (SRFA) concentration. Clay suspensions were pre-loaded with SRFA at concentrations ranging from 0 to 25 mg/L SRFA in either Na- or Ca-enriched conditions at pH 5 or 7. Kaolinite adsorbed the highest amount of SRFA that resulted in a reduction in MCLR adsorption at pH 5, but little effect at pH 7. Illite adsorbed little SRFA and its presence altered MCLR adsorption in a manner that differed with pH and saturating cation. This result we take to indicate the formation of solution-phase MCLR-SRFA complexes that had complex interactions with illite. Montmorillonite adsorbed the most MCLR and did so more rapidly than did the other clays. It also adsorbed a moderate amount of SRFA, which enhanced MCLR adsorption to Na-montmorillonite, but not to Ca-montmorillonite. Desorption of MCLR varied for the systems, but was more evident at pH 7 than pH 5. Overall, the results demonstrate clay type and electrolyte cation were more important factors for MCLR adsorption than was the presence or concentration of SRFA.

1. Introduction The production of algal toxins during harmful algal blooms (HABs) is a concern because of the worldwide occurrence of HABs and the toxicity and persistence of the algal toxins produced therein [1].

⁎

Microcystins (MCs), one of the most common algal toxins produced by HABs, can adversely affect liver, kidney and reproductive function to those exposed via drinking or ingesting MC-contaminated water or food [2]. Exposure to MCs in a recreational setting (e.g., swimming) is also an issue and can result in skin irritation, allergic reactions and

Corresponding author. E-mail address: [email protected] (J.J. Lenhart).

https://doi.org/10.1016/j.colsurfa.2019.123964 Received 23 July 2019; Received in revised form 9 September 2019; Accepted 10 September 2019 Available online 19 September 2019 0927-7757/ © 2019 Elsevier B.V. All rights reserved.

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

can reduce MCLR adsorption by either enhancing electrostatic repulsion or via competing for sorption sites. However, since MCLR contains the hydrophobic ADDA group it is possible that surface-bound NOM can enhance MCLR interaction with the surface through hydrophobic bonding. Previous studies show differing trends in MCLR adsorption onto natural adsorbents in the presence of NOM [15,18]. For example, low concentrations of fulvic acid (< 2.5 mg/L) enhanced MCLR adsorption to iron oxide nanoparticles, but higher concentrations (> 2.5 mg/L) reduced adsorption. The authors indicate this reflects at low concentrations that adsorbed fulvic acid enhanced the hydrophobic attraction of the MCLR; however, at higher concentration fulvic acid competed with MCLR for adsorption sites. Wu et al. [15] observed the opposite trend in that competition occurred when the NOM content of a natural sediment was lower than 8% and enhanced adsorption when the NOM content exceeded 8%. Such differing results likely reflect heterogeneities in the natural sorbents in these studies and thus one way to more clearly identify how NOM influences on MCLR adsorption to natural mineral surfaces is to use isolated mineral phases that have well characterized properties. In this study, we examined how the presence of NOM on clay surfaces or in solution influence the sorption behavior of MCLR with the goal to better understand how NOM influences MCLR interactions with natural solids commonly present in soils and sediments. The objectives of this study were to determine 1) whether the presence and concentration of NOM affects the extent or rate of MCLR adsorption onto clays and 2) if adsorbed MCLR was released back to solution in response to changing water conditions. Experiments were conducted using the same kaolinite, illite and montmorillonite clays previously evaluated [17] at pH 5 or 7 and in 0.01 M NaNO3 or Ca(NO3)2. MCLR was chosen, because among the approximately 100 microcystin variants identified [22] it appears very frequently during HAB episodes [2] and as a result it is the focus of most studies (e.g., [7,11,14]). For our NOM source, we used Suwanee River Fulvic Acid (SRFA). Prior to the addition of MCLR, clays were pre-equilibrated with SRFA to mimic natural conditions where minerals would be coated with organic matter. Our results show the influence of SRFA and environmental factors, such as pH and cation electrolyte, on MCLR adsorption differ for the different clay minerals. For example, the presence of SRFA had little influence on MCLR adsorption to the Na-enriched kaolinite, yet it hindered adsorption to the Ca-enriched kaolinite. Kinetics differed as well, with montmorillonite reaching equilibrium with MCLR within one hour, while equilibration required 24 h or more for kaolinite and illite. Our results also show that more MCLR desorbed from the Ca-form of the clays at pH 7 and that the presence of SRFA only impacts MCLR desorption from illite. Overall, our results demonstrate that clay type and electrolyte cation were more important factors for MCLR adsorption than was the presence or concentration of NOM.

gastrointestinal illness [3]. One consequence of the presence of algal toxins is the promulgation of limits and guidance by regulatory bodies. In Ohio, for example, guidance levels for total MCs in drinking water for children under six and sensitive populations is 0.3 μg/L [4] and for recreational water a public health advisory will be triggered at 6 μg/L [5]. However, the concentration of MCs often exceeds hundreds of μg/L during the bloom season [2,6]. Thus, owing to the risks MCs pose to human health, it is important to understand the processes that dictate how MCs persist in aquatic systems. Adsorption is an important pathway for eliminating MCs from the environment. For example, MCs show significant adsorption onto sediments, with Morris et al. [7] demonstrating significant removal of microcystin-LR by a sediment sample dominated by the clay minerals kaolinite, montmorillonite and illite. In a similar manner, Miller et al. [8] observed clay-sized sediments adsorbed more microcystin than sediments dominated by other particle sizes. Understanding to what extent adsorption contributes to the removal of MCs from water [9–12] also requires knowledge of adsorption kinetics and whether MCs desorb. For example, if the kinetics of MC adsorption are rapid, significant amounts of toxin can adsorb to sediment during short-term contact situations, e.g., resuspension of sediments during storm events. If kinetics are slow, however, more extended contact time is required to effectively remove MCs from solution. It is also important to understand the potential risk associated with the release of adsorbed toxins back to aqueous phase if sorption is reversible. For example, systems that demonstrate low desorption [13] would act as a sink, while those that demonstrate high desorption [14] would act as a source. Unfortunately, details of what sorbent property leads to MC desorption is unknown as published results are often confounding (e.g., MC desorption from a high-clay sediment was more than that from a low-clay sediment [13,14]). Whether the organic content or clay properties results in the inconsistent desorption of MCLR from the two field sediments is unclear. The content of organic matter and clays are critical factors that influence the adsorption of MCLR by sediment and soil. Wu et al. [15], for example, observed MCLR adsorption to sediment with low organic matter content (< 8%) decreased with increasing NOM content. For high organic matter content sediments (> 8%), however, they observed the reverse [15]. This difference they attribute to competition at low NOM content and the interaction of MCLR with bound NOM at higher NOM content. Others report an increase in the adsorption of MCLR as the proportion of clay-sized soil and sediment particles within the sample increased [8,9,16]. For example, Mohamed et al. [9] used Freundlich isotherm parameter values to correlate MCLR sorption with both the organic matter and clay content of different sediment. However, the sorption behavior of MCLR in other studies show conflicting trends. For example, Miller et al. [8] compared sediments from five different sites and determined sediments with high clay content adsorbed greater amounts of cyanobacterial toxins. They did not observe a similar correlation for the soil organic matter. The inconsistent observations with these natural materials reflects their different compositions, which hinders ready comparison or interpretation of the results. One approach to reduce uncertainties associated with the adsorbent composition is to use well-characterized adsorbents. For example, our prior work with clay minerals [17], kaolinite (kGa-2), illite (iMt-2), Namontmorillonite (SWy-1) and Ca-montmorillonite (STx-1), demonstrate montmorillonite shows the greatest adsorption capacity for MCLR in organic matter-free environments and that the metal cation used to saturate the clay surface alters adsorption. The adsorption of natural organic matter (NOM) to an interface, particularly low-carbon mineral surfaces, can either decrease the sorption of organic compounds via competition for sites or increase it by increasing surface hydrophobicity [15,18,19]. The adsorption of negatively charged NOM molecules can also enhance or impart a negative charge of the underlying surface [20]. Because MCLR carries a net charge of negative one between pH 2–12 [21], surface-bound NOM

2. Materials and methods 2.1. Materials 2.1.1. Adsorbents Kaolinite (kGa-2), illite (iMt-2), Na-montmorillonite (SWy-1) and Ca-montmorillonite (STx-1) were obtained from The Clay Minerals Society (West Lafayette, IN). Prior to use, the clays were washed and saturated with Na+ or Ca2+ following methods detailed by Liu et al. [17]. This procedure isolated particles nominally larger than 2 μm. The kGa-2 and iMt-2 samples were saturated with Na+ or Ca2+ producing Na-kaolinite, Ca-kaolinite, Na-illite and Ca-illite; SWy-1 was saturated by Na+ and STx-1 with Ca2+ forming Na-montmorillonite and Camontmorillonite, respectively. The clays were suspended in 0.01 M NaNO3 or 0.01 M Ca(NO3)2 and oven-dried overnight at the temperature of 75 °C before use. Details of the characteristics of the clays are presented by Liu et al. [17]. 2

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

montmorillonite systems, samples were collected at 1, 24 and 48 h.

2.1.2. Adsorbates MCLR was obtained from Cayman Chemical (Ann Arbor, MI) in a dissolved form as 1 mg/mL of ethanol. This stock was used as received and stored at −20 °C prior to use. SRFA was purchased in a dry form from the International Humic Substances Society. The SRFA stock solutions were made by dissolving 100 mg SRFA in 1 L solutions of 0.01 M NaNO3 or 0.01 M Ca(NO3)2, depending on the desired electrolyte conditions. These SRFA stock solutions were stored at 4 °C. The concentration of MCLR in solution was analyzed by high-performance liquid chromatography (HPLC) after Liu et al. [17] using a Hewlett-Packard 1110 HPLC equipped with a diode array detector (HPLC-DAD). Analyses used 80 μL sample injections and an Agilent Technologies Prep-C18 scalar column (4.6 × 150 mm, 5 μm particle size) with a 60:40 eluent ratio of 20 mM pH 3 phosphoric acid buffer and acetonitrile (HPLC grade, Fisher Scientific) at a flowrate of 1 mL/ min. Measurements utilized a wavelength of 238 nm and resulted in a detection limit of 50 μg/L MCLR. SRFA concentration in solution was measured via UV–vis spectroscopy (UV-4201PC, Shimadzu Corp.) at a wavelength of 220 nm. Standards for calibration were prepared in either 0.01 M NaNO3 or 0.01 M Ca(NO3)2.

2.2.4. Desorption of MCLR from Ca-clays Desorption of MCLR was studied using the Ca-form of the clays because Ca-clays demonstrated greater capacity for MCLR in the absence of NOM [17] and as a result we anticipated the desorption would be more readily observed. To facilitate comparison with the 48 h kinetic tests with the Na-clays, the 14 mL remaining after the conclusion of the 24 h equilibration were further equilibrated for another 24 h. After 48-h of total equilibration, the samples were centrifuged at 1500 g for 30 min and 1 mL of supernatant was removed to establish the time zero MCLR concentration for desorption. The remaining 6 mL of supernatant was discarded and 7 mL of 0.01 M Ca(NO3)2 at pH 5 or pH 7 was added and the samples were subsequently returned to the orbital shaker. The samples were agitated at 100 rpm at room temperature and sampled at 24, 48, 72, 96 and 120 h. At each sampling time, 1 mL samples were removed, centrifuged at 1500 g for 15 min and the supernatant was analyzed by HPLC. 2.2.5. Data analysis methods The adsorbed concentrations (mg/g) of SRFA and MCLR were calculated from the difference between the initial concentrations and the remaining concentrations in solution divided by the solid concentration. For the desorption experiments, the changing concentration of MCLR in solution was the difference between the measured concentration at each collection time and half of the concentration after the 48-h equilibration (time zero concentration), based upon the volume of sample that was decanted and replaced with electrolyte solution.

2.2. Methods 2.2.1. SRFA pre-loading of Na- and Ca-clays SRFA was mixed with clays prior to the addition of MCLR for 2 days. This entailed adding appropriate amounts of SRFA stock into 250 mL glass beakers which contained 1.5 g of the tested clay type suspended in 100 mL of 0.01 M NaNO3 or 0.01 M Ca(NO3)2 necessary to obtain the desired initial SRFA concentrations of 1, 10 or 25 mg/L. The sample pH was adjusted to pH 5 or 7 using 70% w/w HNO3 or 1 M NaOH. The samples were then placed on an orbital shaker at 100 rpm for a period of 48 h at room temperature. After equilibration, 15 mL of each mixture was removed and centrifuged at 1500 g for 30 min. The resulting supernatant was collected to measure the remaining SRFA concentration. The remainder of the mixtures were vigorously stirred to get a uniform ratio of solid and solution for use in the subsequent MCLR adsorption experiments.

3. Results and discussion 3.1. Interactions of SRFA with clay minerals 3.1.1. SRFA adsorption onto kaolinite SRFA adsorption to kaolinite was higher at pH 5 than pH 7 and exhibited little dependence on the saturating cation (Fig. 1a and b). The maximum adsorption observed of ca. 1.5 mg/g was for the Ca-kaolinite system at pH 5 with an initial SRFA concentration of 25 mg/L. This decreased to about 1.1 mg/g for the same Ca-kaolinite system at pH 7. For the Na-kaolinite systems with the same SRFA concentrations, adsorption values of 1.4 mg/g and 1.3 mg/g were measured for pH 5 and 7, respectively. These values were similar to that reported by Schroth and Sposito [23] for the adsorption of SRFA to kGa-2 kaolinite without a specific saturating cation at pH 5 and 7. The concentration of SRFA remaining in solution after adsorption was below detection for all of the systems with an initial SRFA concentration of 1 mg/L. For the remaining systems, concentrations ranged from 1.67 to 7.90 mg/L, except for the Na-kaolinite system with an initial concentration of 10 mg/L of SRFA at pH 5, where no SRFA was detected in solution. It should be noted for these systems with remaining SRFA that the residual solutionphase SRFA concentration exceeded the initial MCLR concentration used in the subsequent adsorption experiments. This indicates that both surface-bound and solution-phase SRFA might influence the adsorption of MCLR to kaolinite. Based on previous results [19,23,24], the favorable and pH-dependent adsorption of SRFA to kaolinite likely reflects ligand exchange interactions between the SRFA acidic functional groups and the Al-sites on the alumina sheet or edge sites of kaolinite. The consequence of such interactions suggest the formed surface complex between SRFA and kaolinite should be strong and irreversible [25]. The bound SRFA may also occupy the available binding sites on the kaolinite surface or provide for extra hydrophobic interactions with MCLR. Since the higher molecular weight and more aromatic fulvic acid fractions are likely to be adsorbed to kaolinite [24,26], it was expected that the lower molecular weight and less aromatic fulvic acid components remained in solution. Thus, the remaining solution-phase SRFA could have higher

2.2.2. Adsorption of MCLR to Ca- and Na-clays MCLR adsorption was studied with the SRFA pre-loaded clays by transferring 15 mL aliquots from the SRFA-clay mixtures to 15 mL glass centrifugal tubes. Into each tube was added 15 μL of the stock MCLR solution (1 mg/mL) to obtain the initial 1 mg/L MCLR concentration. This concentration was chosen to facilitate ready measurement of solution phase MCLR at the conclusion of the adsorption tests. Samples for each pre-loaded SRFA level, i.e. 1, 10 or 25 mg/L, were prepared in triplicate. Blanks, without clay or SRFA, were prepared in a similar manner to assess MCLR removal to the tube surfaces. Each tube was wrapped in aluminum foil and shaken at 100 rpm on an orbital shaker at room temperature. After shaking for 24 h, the samples were centrifuged at 1500 g for 15 min. Samples of the supernatant were transferred to 1 mL HPLC amber glass vials for MCLR concentration measurement by HPLC. 2.2.3. Kinetics of MCLR adsorption to Na-clays The kinetics of MCLR sorption to SRFA pre-loaded Na-clays was evaluated over a period of 48 h in 0.01 M NaNO3 at pH 5 and 7. The Naclays were chosen for these experiments as previous results in the absence of NOM indicate lower affinity of MCLR for clays in this form [17], hence we anticipated the kinetics would be slower and more tractable to study. The experimental procedures were similar to those previously described (see Section 2.2.2), with the exception that 1 mL samples were removed at designated times to quantify MCLR concentration. For the Na-kaolinite and Na-illite systems, samples were collected at 1, 2, 4, 10, 24 and 48 h of mixing. For the Na3

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Fig. 1. Adsorption of SRFA as a function of the initial preload concentration and pH to (a) Na-kaolinite, (b) Ca-kaolinite, (c) Na-illite, (d) Ca-illite, (e) Na-montmorillonite and (f) Ca-montmorillonite. The left-side axis is the solution-phase SRFA concentration remaining in solution. The right-side axis is the adsorbed concentration of SRFA. The clay concentration was 15 g/L.

Ca2+ on the illite surface reduces the magnitude of the negative surface charge [32], producing perhaps the observed increase in SRFA adsorption. The decrease in SRFA adsorption with increasing pH could also reflect changing electrostatic interactions as both the negative charge of fulvic acid as well as that for the exposed edge sites increase in magnitude with increasing pH [25,30]. With so little adsorption occurring, the bulk of the SRFA added remained in solution and thus it was anticipated for the illite systems that solution-phase SRFA would impact MCLR interactions more than the surface-bound SRFA.

polarity and lower aromaticity than the SRFA bound to the kaolinite, resulting in greater affinity to polar organics [19,27]. 3.1.2. SRFA adsorption onto illite Except for the Ca-enriched systems with 10 or 25 mg/L initial SRFA, little SRFA adsorbed onto illite over our studied conditions (Fig. 1c and d). Even in the Ca-enriched systems adsorption was low, with only about 10% of the initial SRFA adsorbing. This adsorption was slightly higher at pH 5 than at pH 7. These results were similar to those of Staunton and Roubaud [28] that show negligible adsorption of a soil fulvic acid onto illite saturated with a monovalent cation, and those of Slavek and Pickering [29] and Du et al. [30] that show reductions in the adsorption of fulvic acid to illite as pH increased. According to Du et al. [30], fulvic acids primarily bind to exposed Al-sites, instead of Si-sites, on aluminosilicate clay surfaces. Since 2:1 clays like illite primarily expose Si-sites, the amount of fulvic acid adsorbed would be expected to be lower than to kaolinite, which as a 1:1 clay exposes both Al-sites and Si-sites. In addition, the limited amount of edge sites on illite and its negatively charged basal surface could further hinder illite adsorption of fulvic acid [31]. Replacing Na+ with

3.1.3. SRFA adsorption onto montmorillonite The adsorption of SRFA to montmorillonite was greater than that to illite, but less than that to kaolinite, and depended upon both the saturating cation and solution pH (Fig. 1e and f). Higher SRFA adsorption on montmorillonite occurred in the Ca-enriched systems that was reduced one to three times in systems with Na+. Evans and Russell [33] report similar results for the adsorption of a soil fulvic acid onto bentonite at pH 4 in Ca-enriched systems being 2.2 times that in Na-enriched systems. Increasing the pH from 5 to 7 decreased SRFA adsorption to montmorillonite by about 2 times in all systems, except for 4

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Fig. 2. Adsorption of MCLR as a function of the pre-loaded SRFA concentration and pH to (a) Na-kaolinite, (b) Ca-kaolinite, (c) Na-illite, (d) Ca-illite, (e) Namontmorillonite and (f) Ca-montmorillonite. The initial MCLR concentration was 1 mg/L and the clay concentration was 15 g/L.

(Fig. 2). However, other trends in adsorption reflected the unique properties of the respective systems. For example, montmorillonite exhibited a decrease in MCLR adsorption with increasing pH whereas kaolinite generally produced an increase in adsorption with increasing pH. The influence of the cation was similarly dependent on the particular clay mineral, with illite exhibiting greater MCLR adsorption for the Ca-enriched systems while adsorption of MCLR to kaolinite was similar for both Na-enriched and Ca-enriched systems. Because of this, trends observed will be discussed for each clay separately. The adsorption of MCLR to kaolinite exhibited more variation with respect to pH and SRFA loading for the Ca-enriched systems than the Na-enriched systems (Fig. 2a and b). In the presence of SRFA, for instance, the adsorption of MCLR to Ca-kaolinite nearly doubled with increasing pH whereas for the Na-kaolinite only that system with 10 mg/L initial SRFA exhibited a significant pH dependence. In a similar fashion, the preloaded SRFA influenced MCLR adsorption more for the Ca-enriched systems than the Na-enriched systems, particularly at pH 5, where MCLR adsorption decreased from ca. 35 μg/g in the absence of SRFA to 4 μg/g in the presence of 25 mg/L SRFA (Fig. 2b). At pH 7, however, the influence of the SRFA was not significant (based on p-values are above 0.05) except for the Ca-kaolinite system with 25 mg/

that with Ca-montmorillonite and 1 mg/L of initial SRFA. This reflects in systems with 1 mg/L SRFA that trends associated with the cation and pH were not significant as SRFA adsorption was nearly complete for all the samples, except for the Na-montmorillonite system at pH 7. Overall, little SRFA adsorbed in the Na-enriched systems except for that with 25 mg/L SRFA, where SRFA adsorption was 0.18 mg/g at pH 7 and 0.38 at pH 5. This was consistent with Staunton et al. [28] observing limited adsorption of soil fulvic acid to Na-montmorillonite at neutral pH. Unlike the other clay systems, we observed a notable enhancement in the dispersion of Na-montmorillonite in the presence of SRFA, regardless of its loading concentration. This was consistent with reports that increasing NOM concentration within a certain range, about 0–40 mg/L, increases the dispersion of Na-montmorillonite [34,35]. Little effect of NOM on the dispersion of Ca-montmorillonite suspension was observed in our study, which was in agreement with the results of Tarchitzky et al. [35].

3.2. Adsorption of MCLR onto clays Regardless of the presence of SRFA, the adsorption of MCLR was generally greater to montmorillonite than it was to illite or kaolinite 5

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Na-illite at pH 5 decreased in systems with 10 or 25 mg/L of SRFA (Fig. 2c). The reduction in the adsorption of MCLR to Na-illite at pH 5 with 10 and 25 mg/L pre-loaded SRFA could reflect 1) the SRFA in solution had stronger interactions with the MCLR-SRFA complexes than did the Naillite surface, and/or 2) the formation of complexes was reduced when the SRFA concentration increased. According to Delle Site [37], the association of hydrophobic organics to humic substances is reduced when the concentration of humic substances increases because an increase in humic-humic interactions at these higher concentrations reduces available binding sites for hydrophobic organic compounds. Furthermore, humic substances form submicellar aggregates at elevated concentrations [38] that correspondingly increase the apparent water solubility of hydrophobic organics [39]. Although the organics in these studies were more hydrophobic than MCLR, the potential for similar interactions to occur with SRFA were possible and could have influenced MCLR interactions with Na-illite. Trends in MCLR adsorption to illite in the Ca-enriched conditions (Fig. 2d) differed from those observed in the Na-enriched systems (Fig. 2c). At pH 5, the adsorption of MCLR to Ca-illite in the system with 1 mg/L pre-loaded SRFA was about 60% lower than in the SRFA-free system. With increasing pre-loaded SRFA concentration, however, the MCLR adsorption increased and was similar to that measured in the absence of SRFA (Fig. 2d). This trend in MCLR adsorption to Ca-illite at pH 5 is opposite to that observed in the Na-enriched conditions at the same pH. Similar to the Na-enriched conditions, limited SRFA adsorbed to the Ca-illite surface (Fig. 1d) and thus MCLR presumably only interacted with solution-phase SRFA as opposed to the adsorbed SRFA. Therefore, the opposite trend of MCLR adsorption between Na-illite and Ca-illite indicates the cation altered interactions between MCLR, SRFA and illite. The reduction in MCLR adsorption to Ca-illite with 1 mg/L pre-loaded SRFA indicates at low SRFA concentration that MCLR affinity to SRFA exceeded MCLR affinity to the Ca-illite surface. With increasing preloading of SRFA, MCLR adsorption increased to nearly match that measured in the absence of SRFA (Fig. 2d). As previously noted this could suggest interactions between the SRFA molecules increased and as a result hindered interactions between MCLR and SRFA. MCLR adsorption to illite in the Ca-enriched conditions at pH 7 increased with increasing SRFA loading (Fig. 2d). Thus, unlike in the Na-enriched systems at this pH, solution-phase SRFA had a significant influence on MCLR adsorption in Ca-enriched systems and produced enhanced MCLR adsorption. Similar to Ca-enriched conditions at pH 5, MCLR could interact with solution-phase SRFA producing a SRFAMCLR complex that enhanced MCLR adsorption at neutral pH. This could reflect the tendency for humic molecules to interact to a greater extent at lower pH [40] thereby resulting in less humic-humic interactions at pH 7 than at pH 5. Because of this, solution-phase SRFA was better able to interact with MCLR even though the SRFA concentration increased. Differences in pH were also manifest in the adsorption of MCLR in the presence of SRFA being higher at pH 7 than that at pH 5. This suggests the affinity of MCLR-SRFA complexes to the Ca-illite surface increases with increasing pH. It was previously observed in the absence of SRFA that cation bridging between MCLR and illite under Ca-enriched conditions could increase with increasing pH [17]. Therefore, it seems reasonable that Ca2+ coordination with the MCLRSRFA complex could have increased at higher pH and that this coordination impacted MCLR adsorption. The adsorption of MCLR to montmorillonite did not exhibit marked changes with SRFA pre-loading concentration (Fig. 2e and f). This was despite the fact that the resulting solution-phase SRFA differed significantly for the different pre-loading conditions (Fig. 1e and f), indicating MCLR adsorption to montmorillonite was not strongly influenced by the presence of SRFA. In the Na-enriched system, the remaining solution-phase SRFA concentration ranged from trace levels to 20 mg/L at pH 5 and from 1 mg/L to 22.3 mg/L at pH 7. However, in the presence of these different concentrations of SRFA, the MCLR

L SRFA which exhibited a decrease in MCLR adsorption of ca. 65% (Fig. 2b). MCLR adsorption to Na-kaolinite systems was similar across all systems, with only the system at pH 5 and 10 mg/L exhibiting a significant deviation with an adsorbed concentration ca. 50% lower than the other systems. The adsorption of MCLR to illite exhibited trends that varied with SRFA pre-loading, saturating cation and pH (Fig. 2c and d). Under Naenriched conditions at pH 5, the SRFA pre-loading initially increased MCLR adsorption compared to system without SRFA and then with increasing SRFA pre-loading the MCLR adsorption decreased (Fig. 2c). At pH 7, MCLR adsorption in the Na-illite systems exhibited a gradual increase in adsorption with increasing pre-loading of SRFA, however, the trend was not statistically significant (p-values comparing the effect of SRFA on MCLR adsorption all exceeded 0.05). Trends in the adsorption of MCLR for the systems with Ca2+ were different to those with Na+. At pH 5, MCLR adsorption decreased by a factor of 2 for the 1 mg/L SRFA preloading. With increasing SRFA, MCLR adsorption increased and was similar to that measured in the absence of SRFA (Fig. 2d). At pH 7, MCLR adsorption increased with increasing SRFA preloading from 13 μg/g with no SRFA to 47 μg/g with 25 mg/L of preloaded SRFA. Overall, the adsorption to Ca-illite exceeded that to Naillite. MCLR adsorption to Ca-montmorillonite was nearly constant across all systems at ca. 40–50 μg/g whereas that to Na-montmorillonite exhibited significant dependence on SRFA pre-loading and pH. For example, the addition of SRFA into the systems resulted in a significant increase in MCLR adsorption to Na-montmorillonite at both pH 5 and 7. The preloaded SRFA concentration did not significantly influence MCLR adsorption to Na-montmorillonite, however, as the results at 1, 10 and 25 mg/L pre-loaded SRFA were not statistically different (p-values > 0.05). The adsorption of MCLR to Na-montmorillonite decreased with increasing pH, with that at pH 5 being about twice that at pH 7 (Fig. 2e). 3.2.1. Influence of solution-phase SRFA on MCLR adsorption As previously noted and evident in Fig. 1, the concentration of SRFA remaining in solution after the pre-loading experiments was higher than the MCLR concentration in all systems except those where the preloading concentration of SRFA was 1 mg/L. In the case of the kaolinite systems where SRFA adsorption was extensive it appears that the remaining solution-phase SRFA had little influence on the MCLR adsorption. This was evident in MCLR adsorption to kaolinite being higher at pH 7 than at pH 5 (Fig. 2a and b) despite the remaining SRFA concentration in solution being higher at pH 7 than at pH 5 (Fig. 1a and b). This negative correlation implies for this system that the solution-phase SRFA either enhanced MCLR adsorption to kaolinite or had limited influence on it. In the case of the illite system, the adsorption of SRFA was minimal and consequently the majority of the added SRFA stayed in solution (Fig. 1c and d). Unlike the kaolinite system, it appears in this case that this solution-phase SRFA may have influenced interactions with MCLR and illite. For example, the adsorption of MCLR to Na-illite at pH 5 decreased with increasing pre-loaded SRFA and since so little SRFA adsorbed in these systems this reflects systems with increasing amounts of solution-phase SRFA. The decrease in adsorption with this increasing solution-phase SRFA suggests interactions between SRFA and MCLR inhibited MCLR adsorption. At pH 7, however, SRFA pre-loading had little effect on MCLR adsorption and thus these potential interactions between MCLR and solution-phase SRFA were more important at pH 5 than at pH 7. This pH dependence suggests interactions between SRFA and MCLR might reflect hydrophobic interactions since the hydrophobic nature of both MCLR and SRFA decrease when increasing pH as the molecules ionize [21,36]. The increase in MCLR adsorption to Naillite at pH 5 for 1 mg/L preloaded SRFA indicates such a MCLR-SRFA complex had a higher affinity to the surface than did MCLR itself. However, this increase in affinity was limited as MCLR adsorption onto 6

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Fig. 3. The adsorption of MCLR as a function of time and fulvic acid concentration [FA] onto Na-kaolinite at (a) pH5 and (b) at pH7; Na-illite at (c) pH5 and (d) pH7; and Na-montmorillonite at (e) pH5 and (f) pH7. The initial MCLR concentration was 1 mg/L and the clay concentration was 15 g/L.

adsorption remained at 60 μg/g at pH 5 and 30 μg/g at pH 7. Similar negligible difference in MCLR adsorption to Ca-montmorillonite was observed for the SRFA pre-loadings at both pH values (Fig. 2f). Overall, this indicates that MCLR interactions to montmorillonite were stronger than interactions between MCLR and SRFA.

kaolinite systems may reflect that kaolinite saturated with Na+ has a more negative surface charge than when saturated with Ca2+ [42]. This would increase electrostatic repulsion between MCLR and the kaolinite surface, which could inhibit ligand exchange reactions [25]. The adsorption of SRFA to illite was negligible in the Na-enriched systems and as a result surface-bound SRFA was only capable of influencing interactions of MCLR to Ca-illite. At pH 5, the influence of surface-bound SRFA on the adsorption of MCLR to Ca-illite was limited to the decrease observed in the system with 1 mg/L preloaded SRFA (Fig. 2d). The adsorption of SRFA to Ca-illite was lower at pH 7 than at pH 5 and this reduction in surface-bound SRFA correlated with an increase in MCLR adsorption with increasing SRFA pre-loading (Fig. 2d). Overall, these results suggest surface-bound SRFA had little influence on MCLR adsorption to illite. Thus, the influence of SRFA on MCLR interacting with illite was likely due to the interactions with solutionphase SRFA, rather than surface-bound SRFA. MCLR adsorption to montmorillonite in the presence of SRFA was only enhanced under Na-enriched conditions (Fig. 2e and f). This enhancement did not vary with pre-loading SRFA concentration and since

3.2.2. Influence of surface-bound SRFA on MCLR adsorption As previously noted, the adsorption of SRFA varied for the clays and was most extensive for the kaolinite systems (Fig. 1). For Ca-kaolinite, the presence of surface-bound SRFA correlated with a reduction in MCLR adsorption, particularly at pH 5 (Fig. 2a and b). SRFA adsorbed more at pH 5 than pH 7 and thus it appears that competition for binding sites between SRFA and MCLR on Ca-kaolinite occurred more at pH 5 than at pH 7. For the Na-kaolinite system, however, MCLR adsorption varied little with pH or the amount of surface-bound SRFA. Due to the importance of ligand exchange on SRFA adsorption to kaolinite [41], the reduction in MCLR adsorption to Ca-kaolinite suggests MCLR competes against SRFA for similar sites on kaolinite available to form ligand exchange reactions. The lack of a significant effect for the Na7

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

adsorption for the Na-kaolinite system at pH 5 and possibly the Na-illite system at pH 7. Under these two conditions, MCLR adsorption onto clays continued over the 48-h time period studied when there was no pre-loaded SRFA, but was nearly steady for systems with SRFA beyond 24 h. This change in the MCLR adsorption over time could be attributed to the dispersion of clays in the different systems, since the adsorption of natural organic matter on clays can enhance its dispersion [44]. This occurs when adsorbed NOM prevents clay aggregation from occurring between the positively charged edges and negatively charged faces of clay by adding negatively charged functional groups, e.g. carboxyl groups, on edge sites [44]. While not explicitly observed, it was possible the clays stayed more dispersed in the presence of SRFA, resulting in more rapid adsorption of MCLR in systems with preloaded SRFA. Fluctuations in MCLR adsorption at pH 7, particularly for Na-kaolinite and Na-illite, suggests the presence of weak adsorption interactions. Grutzmacher et al. [16] observed fluctuations in the adsorption of MCRR to slow sand filter materials, where values for the relative concentration (C/Co) increased from 0.3 after mixing for 6 h to 0.6 after 24 h. However, no literature demonstrates unstable adsorption of MCLR over time at neutral pH, as most studies indicate it reached equilibrium in a few hours [18]. The unstable adsorption not only suggests the bonding between MCLR and clays in the Na-enriched environment at neutral pH was weak but also implies that the adsorbed MCLR could be released back to the aqueous phase more readily under these conditions.

the adsorption of SRFA increased with pre-loading concentration (Fig. 1e), the lack of dependence in MCLR adsorption with surfacebound SRFA suggests MCLR primarily interacted with the clay. This suggests the Na-montmorillonite surface had greater affinity for MCLR than surface-bound SRFA. Under these conditions, the dispersion of the clay was observed to be enhanced in the presence of SRFA. This could have increased the availability of reactive surface area, which is a factor influencing MCLR adsorption [15]. There was no significant difference in MCLR adsorption to Camontmorillonite when changing solution pH or pre-loaded SRFA (Fig. 2f). Ca-montmorillonite adsorbed more SRFA than Na-montmorillonite, and adsorption decreased with an increase in pH from 5 to 7 (Fig. 1f). Since little enhancement of MCLR adsorption on Ca-montmorillonite occurred in the presence of SRFA and since there was little adsorbed SRFA on Ca-montmorillonite at pH 7, it was likely that the surface-bound SRFA and solution-phase SRFA had limited effect on MCLR adsorption in this system. The maximum MCLR adsorption in this study occurred in the montmorillonite systems (approximately 50–60 μg/g) and it represented 50–60% of the added MCLR. This compares well to similar surface coverage values reported for clays and clay-sized particle fractions of sediments [13,15], but is about an order of magnitude lower than that reported for MCLR adsorption to iron oxide particles [18]. This suggests the capacity of silicate clays to adsorb MCLR might be lower than that for metal oxides, which might reflect limitations in available binding sites.

3.4. Desorption of MCLR from Ca-clays 3.3. Kinetics of MCLR adsorption to Na-clays The desorption of MCLR from the Ca-clays was minimal and demonstrates that, except for the SRFA-free Ca-illite system at pH 5, MCLR adsorption to Ca-clays was more stable at pH 5 than at pH 7 (Fig. 4). This was consistent with MCLR adsorption over time exhibiting more variation at pH 7 than pH 5 (Fig. 3). The results also demonstrate that SRFA pre-loading had a more significant influence on MCLR desorption in the Ca-illite systems (Fig. 4c and d) as well as the Ca-montmorillonite system at pH 7 (Fig. 4f). In some systems, the results also demonstrate continued adsorption, particularly for the Ca-kaolinite systems where MCLR adsorption persisted at both pH values after the initiation of the desorption experiments when half the solution was replaced by MCLR-free electrolyte solution (Fig. 4a and b). At pH 5, for example, MCLR adsorption increased by approximately 15 μg/g during the 120-h desorption experimental timeframe in the absence of SRFA. In the presence of SRFA, MCLR adsorption increased 20 μg/g for the 1 and 10 mg/L SRFA pre-loaded systems and 10 μg/g for the 25 mg/L SRFA pre-loaded system. Most of the observed increase occurred in the first 24 h of the desorption experiments. For systems at pH 7, MCLR adsorption also continued after the initiation of the desorption conditions, regardless of SRFA presence and concentration. The time required for MCLR adsorption to achieve equilibrium with Ca-kaolinite was much longer than that for Na-kaolinite (Fig. 3a and b) and indicates the electrolyte cation alters interactions between MCLR and kaolinite. This, and the lack of desorption was consistent with the importance of ligand exchange interactions for the adsorption of MCLR [17] and NOM to kaolinite [41]. The trends in MCLR interactions with Ca-illite during the desorption phase of the experiments reflected the pre-loaded SRFA and displays different trends at the two tested solution pH values. At pH 5, MCLR desorption was evident in the SRFA-free solution but not in the SRFApreloaded systems (Fig. 4c). At pH 7, MCLR desorption was only evident for the system with 25 mg/L of pre-loaded SRFA (Fig. 4d). For the SRFA-free and 1 mg/L SRFA pre-loading no change in MCLR adsorption was observed. In the case of the 10 mg/L SRFA system, MCLR adsorption increased during the first 24 h of the desorption experiment, stabilized for about three days, and then desorbed for the final 2 days. The observed differences in the influence of pre-loaded SRFA on MCLR desorption emphasized its presence in solution or on the surface had

The dependence in MCLR adsorption onto Na-kaolinite, Na-illite and Na-montmorillonite as a function of time with and without preloaded SRFA was evaluated over 48 h (Fig. 3), which was 24 h beyond the equilibration time used to evaluate MCLR adsorption (Fig. 2). In most cases the trends established at 24 h persisted, but in select cases (e.g., Na-illite at pH 7) differences were observed. This establishes 24 h was sufficient time for most of the Na-enriched systems to achieve equilibrium. This was consistent with previous studies showing MCLR adsorption to sediments only required a few hours [13,15]. Overall, montmorillonite achieved equilibrium more quickly than the other two clays as MCLR adsorption plateaued at the first sampling time of 1 h. Equilibration to Na-illite was achieved between the 10 and 24 h sampling times, whereas adsorption to Na-kaolinite equilibrated by about 24 h. The time-dependence in MCLR adsorption depended upon the SRFA preloading for some but not all systems. For example, MCLR adsorption to Na-kaolinite at pH 5 was more rapid in the presence of SRFA (Fig. 3a). At pH 7, however, MCLR adsorption to Na-kaolinite fluctuated, with no obvious trend with SRFA loading (Fig. 3b). Similarly, MCLR adsorption to Na-illite with time showed little dependence on SRFA (Fig. 3c and d). At pH 5, MCLR adsorption reached equilibrium in the first 10 h and, regardless of the concentration of SRFA in the system, remained stable for the remainder of the 48 h. At pH 7, MCLR adsorption fluctuated over the first 10 h and, except for the system without SRFA, stabilized after 24 h. In the Na-montmorillonite systems, the separation of particles from solution necessary to measure the dissolved concentration of MCLR was hindered because of the highly dispersed clay suspension, and hence we only collected samples at 1, 3, 24 and 48 h. The results show MCLR adsorption to Na-montmorillonite reached equilibrium in one hour, regardless of the solution pH and SRFA preloading, and was stable without significant fluctuation during the remainder of the experiment (Fig. 3e and f). This rapid and stable reaction suggests MCLR bound to the Na-montmorillonite surface via chemical interactions [25], such as those reported for the adsorption of aspartic acid to montmorillonite, which reached equilibrium in 2 h [43]. The pre-loaded SRFA influenced the time-dependence of MCLR 8

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Fig. 4. Adsorbed concentration of MCLR as a function of time and fulvic acid concentration [FA] during the desorption trails for (a) Ca-kaolinite at pH5, (b) Cakaolinite at pH7, (c) Ca-illite at pH5, (d) Ca-illite at pH7, (e) Ca-montmorillonite at pH5 and (f) Ca-montmorillonite at pH7.

Trends in MCLR desorption from Ca-montmorillonite differed for systems at pH 5 and pH 7 (Fig. 4e and f). At pH 5, there was little effect of pre-loaded SRFA on MCLR desorption over the 5-day study, with about 20% desorption occurring toward the later stages of the experiment for all systems with SRFA. The system without SRFA did not produce MCLR desorption. At pH 7, more significant MCLR desorption occurred that varied by the pre-loaded SRFA concentration. In the absence of SRFA, the adsorbed MCLR fluctuated during the 5-day experiment and showed a nominal amount of desorption. This fluctuation, on the other hand, did not occur when SRFA was present in the system, regardless of the preloading concentration. Unlike the Ca-illite systems, increasing the pre-loaded SRFA concentration for Ca-montmorillonite inhibited the desorption of MCLR as the ratio of desorbed MCLR decreased from 46% to less than 17% when increasing the concentration of pre-loaded SRFA from 1 to 25 mg/L. Desorption of MCLR from Ca-montmorillonite did not exhibit a consistent dependence on SRFA concentration. This may reflect that the STx-1 interlayer spacing expands to accommodate solutes [45,46]. Such expansion could allow for MCLR to form interlayer binding with Ca-

different impacts on MCLR interactions with Ca-illite at pH 5 and 7. Although little SRFA adsorbed to Ca-illite at pH 5 (Fig. 1d), the results for the desorption experiments (Fig. 4c) suggest at this pH that it strengthened MCLR interactions with the Ca-illite surface. This we base on the lack of MCLR desorption observed in the pH 5 Ca-illite system with SRFA, coupled with desorption observed in the corresponding SRFA-free system. At pH 7, desorption of MCLR occurred in the systems with 10 and 25 mg/L SRFA and to some extent the system with 1 mg/L SRFA as well (Fig. 4d). Under these conditions the adsorption of MCLR increased with SRFA preloading (Fig. 2d), which we attributed to the potential for a SRFA-MCLR complex to interact with the Ca-illite surface. The affinity of SRFA for the Ca-illite surface was lower at pH 7 than pH 5 (Fig. 1d) and upon initiating the desorption experiments it was possible that SRFA desorption occurred. This SRFA desorption could have also resulted in the observed MCLR desorption at the higher SRFA preloading conditions. At 1 mg/L SRFA preloading and pH 7, little SRFA was adsorbed and thus its influence on MCLR desorption was negligible. Thus, the limited adsorption of SRFA to illite appears to affect the potential for MCLR to desorb.

9

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

Acknowledgments

montmorillonite as seen for aspartic acid [43]. Desorption of MCLR from Ca-montmorillonite at pH 7, however, decreased when the preloaded SRFA increased, suggesting MCLR interacted with surface-bound SRFA. This suggests that surface-bound SRFA enhanced the bonding of MCLR to Ca-montmorillonite and inhibited desorption. This was consistent with infrared results for the adsorption of enrofloxacin, a fluoroquinolone antibacterial agent, on montmorillonite [47] showing the presence of NOM on montmorillonite surface changed the nature of the interactions [47]. These included electrostatic interactions and hydrogen bonding between the positively charged amine groups on enrofloxacin and deprotonated carboxyl groups on surface-bound NOM as well as via carbonyl and carboxyl groups on enrofloxacin and the carboxylic and phenolic moieties of SRFA [47]. Hence, by extension the MCLR functional groups might also have electrostatic interactions and hydrogen bonding with the surface-bound SRFA in the Ca-montmorillonite system. Overall, these results demonstrate the need for more detailed, specific analyses of whether and to what extent MCLR complexes organic matter and how these complexes influence interfacial processes.

We gratefully acknowledge the support of the U.S. National Oceanic and Atmospheric Administration through its Ohio Sea Grant College Program for primary funding of this research. References [1] X.X. He, Y.L. Liu, A. Conklin, J. Westrick, L.K. Weavers, D.D. Dionysiou, J.J. Lenhart, P.J. Mouser, D. Szlag, H.W. Walker, Toxic cyanobacteria and drinking water: impacts, detection, and treatment, Harmful Algae 54 (2016) 174–193. [2] USEPA, Drinking Water Health Advisory for the Cyanobacterial Microcystin Toxins, United States Environmental Protection Agency Office of Water, Washington DC, 2015. [3] USEPA, Health Effects Support Document for the Cyanobacterial Toxin Microcystins, United States Environmental Protection Agency Office of Water, Washington DC, 2015. [4] OhioEPA, Public Water System Harmful Algal Bloom Response Strategy, Ohio Environmental Protection Agency Division of Drinking and Ground Waters, Columbus, OH, 2019. [5] J.R. Kasich, M. Taylor, C.W. Butler, J. Zehringer, R. Hodges, State of Ohio 2016 Harmful Algal Bloom Response Strategy For Recreational Waters, (2016). [6] WHO, Cyanobacterial Toxins: Microcystin-LR in Drinking-water. Background Document for Preparation of WHO Guidelines for Drinking-water Quality, World Health Organization, Geneva, 2003. [7] R.J. Morris, D.E. Williams, H.A. Luu, C.F.B. Holmes, R.J. Andersen, S.E. Calvert, The adsorption of microcystin-LR by natural clay particles, Toxicon 38 (2) (2000) 303–308. [8] M.J. Miller, M.M. Critchley, J. Hutson, H.J. Fallowfield, The adsorption of cyanobacterial hepatotoxins from water onto soil during batch experiments, Water Res. 35 (6) (2001) 1461–1468. [9] Z.A. Mohamed, H.M. El-Sharouny, W.S. Ali, Microcystin concentrations in the Nile river sediments and removal of microcystin-LR by sediments during batch experiments, Arch. Environ. Contam. Toxicol. 52 (4) (2007) 489–495. [10] M. Thirumavalavan, Y.L. Hu, J.F. Lee, Effects of humic acid and suspended soils on adsorption and photo-degradation of microcystin-LR onto samples from Taiwan reservoirs and rivers, J. Hazard. Mater. 217 (2012) 323–329. [11] W.J. Huang, B.L. Cheng, Y.L. Cheng, Adsorption of microcystin-LR by three types of activated carbon, J. Hazard. Mater. 141 (1) (2007) 115–122. [12] G. Newcombe, D. Cook, S. Brooke, L. Ho, N. Slyman, Treatment options for microcystin toxins: similarities and differences between variants, Environ. Technol. 24 (3) (2003) 299–308. [13] E. Maghsoudi, M. Prevost, S.V. Duy, S. Sauve, S. Dorner, Adsorption characteristics of multiple microcystins and cylindrospermopsin on sediment: implications for toxin monitoring and drinking water treatment, Toxicon 103 (2015) 48–54. [14] M.J. Miller, J. Hutson, H.J. Fallowfield, The adsorption of cyanobacterial hepatoxins as a function of soil properties, J. Water Health 3 (4) (2005) 339–347. [15] X.Q. Wu, B.D. Xiao, R.H. Li, C.B. Wang, J.T. Huang, Z. Wang, Mechanisms and factors affecting sorption of microcystins onto natural sediments, Environ. Sci. Technol. 45 (7) (2011) 2641–2647. [16] G. Grutzmacher, G. Wessel, S. Klitzke, I. Chorus, Microcystin elimination during sediment contact, Environ. Sci. Technol. 44 (2) (2010) 657–662. [17] Y.L. Liu, H.W. Walker, J.J. Lenhart, Adsorption of microcystin-LR onto kaolinite, illite and montmorillonite, Chemosphere 220 (2019) 696–705. [18] J. Lee, H.W. Walker, Adsorption of microcystin-LR onto iron oxide nanoparticles, Coll. Surf. A-Physicochem. Eng. Asp. 373 (1–3) (2011) 94–100. [19] E.M. Murphy, J.M. Zachara, S.C. Smith, Influence of mineral-bound humic substances on the sorption of hydrophobic organic compounds, Environ. Sci. Technol. 24 (1990) 1507–1516. [20] R. Kretzschmar, D. Hesterberg, H. Sticher, Effects of adsorbed humic acid on surface charge and flocculation of kaolite, Soul Sci. Soc. Am. J. 61 (1997) 101–108. [21] P.G.J. de Maagd, A.J. Hendriks, W. Seinen, D. Sijm, pH-dependent hydrophobicity of the cyanobacteria toxin microcystin-LR, Water Res. 33 (3) (1999) 677–680. [22] T. Niedermeyer, Microcystin Congeners Described in the Literature, (2014). [23] B.K. Schroth, G. Sposito, Effect of landfill leachate organic acids on trace metal adsorption by kaolinite, Environ. Sci. Technol. 32 (1998) 1404–1408. [24] M. Meier, K. Namjesnik-Dejanovic, P.A. Maurice, Y.-P. Chin, G.R. Aiken, Fractionation of aquatic natural organic matter upon sorption to goethite and kaolinite, Chem. Geol. 157 (1999) 275–284. [25] G. Sposito, The Chemistry of Soils, Oxford University Press, New York, 1989. [26] K. Namjesnik-Dejanovic, P.A. Maurice, G.R. Aiken, S. Cabaniss, Y.P. Chin, M.J. Pullin, Adsorption and fractionation of a muck fulvic acid on kaolinite and goethite at pH 3.7, 6, and 8, Soil Sci. 165 (7) (2000) 545–559. [27] F. DePaolis, J. Kukkonen, Binding of organic pollutants to humic and fulvic acids: influence of pH and the structure of humic material, Chemosphere 34 (8) (1997) 1693–1704. [28] S. Staunton, M. Roubaud, Adsorption of Cs-137 on montmorillonite and illite: effect of charge compensating cation, ionic strength, concentration of Cs, K and fulvic acid, Clay Clay Min. 45 (2) (1997) 251–260. [29] J. Slavek, W.F. Pickering, The effect of pH on the retention of Cu, Pb, Cd and Zn by clay-fulvic acid mixtures, Water Air Soil Pollut. 16 (2) (1981) 209–221. [30] Q. Du, Z.X. Sun, W. Forsling, H.X. Tang, Complexations in illite-fulvic acid-Cu2+ systems, Water Res. 33 (3) (1999) 693–706.

4. Conclusion In this study, we evaluated the adsorption of MCLR to kaolinite, illite and montmorillonite in response to environmental factors, including SRFA presence, preloaded SRFA concentration, pH and electrolyte cation. SRFA had a different degree of adsorption to the clay minerals and as a result, its presence in solution or surface influenced MCLR adsorption in a manner unique to each clay. In systems with illite, for example, the results suggest solution-phase SRFA could form a complex with MCLR or increased the clay dispersion. The formation of an MCLR-SRFA complex enhanced MCLR adsorption to Ca-illite at pH 7 while inhibiting its adsorption at pH 5. The presence of SRFA enhanced MCLR adsorption to Na-montmorillonite and MCLR equilibrium time to Na-kaolinite, perhaps reflecting increased particle dispersion. Depending upon the system, surface-bound SRFA competed for sorption sites with MCLR or enhanced MCLR adsorption. Kaolinite adsorbed the most SRFA and at pH 5 the adsorption of MCLR was reduced with increasing SRFA preloading. Illite adsorbed little SRFA, however, the small amount of surface-bound SRFA on Ca-illite at pH 5 enhanced MCLR adsorption. The time-dependence in MCLR adsorption differed based on clay type in that it reached equilibrium in one hour for montmorillonite yet kept adsorbing to kaolinite over the entire 48-h experiment. Strong bonding between MCLR and kaolinite results in the majority of toxin remaining bound to the clays. For illite and montmorillonite desorption was observed, particularly at pH 7. This research demonstrates that MCLR interactions with clay in the presence of natural organic matter depend more upon the properties of the clay than on the presence of organic matter. This was consistent with results for natural soils and sediments [8,9,16] and provides guidance to better understand the fate of microcystins in natural systems. The results further demonstrate under the conditions of our study that MCLR desorption was limited, suggesting sediments and soils will act more as a sink for toxins than as a source. The potential formation of a complex involving MCLR and SRFA was also evident and such complexes merit additional study (e.g., [48]) as the potential for dissolved organic matter to complex cyanotoxins thereby influencing their fate remains relatively unknown.

Declaration of Competing Interest 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.

10

Colloids and Surfaces A 583 (2019) 123964

Y.-L. Liu, et al.

[31] B. Gu, J. Schmitt, Z. Chen, L. Liang, J.F. McCarthy, Adsorption and desorption of natural organic matter on iron oxide: mechanisms and models, Environ. Sci. Technol. 28 (1994) 38–46. [32] J.B. Liu, Y.S. Hwang, J.J. Lenhart, Heteroaggregation of bare silver nanoparticles with clay minerals, Environ.-Sci. Nano 2 (5) (2015) 528–540. [33] L.T. Evans, E.W. Russell, The adsorption of humic and fulvic acids by clays, J. Soil Sci. 10 (1) (1959) 119–132. [34] S.A. Visser, M. Caillier, Observations on the dispersion and aggregation of clays by humic substances. 1. Dispersive effects of humic acids, Geoderma 42 (3–4) (1988) 331–337. [35] J. Tarchitzky, Y. Chen, A. Banin, Humic substances and pH effects on sodiummontmorillonite and calcium-montmorillonite flocculation and dispersion, Soil Sci. Soc. Am. J. 57 (2) (1993) 367–372. [36] M. Schnitzer, S.U. Khan, Humic Substances in the Environment, Marcel Dekker, Inc., New York, 1972. [37] A. Delle Site, Factors affecting sorption of organic compounds in natural sorbent/ water systems and sorption coefficients for selected pollutants. A review, J. Phys. Chem. Ref. Data 30 (1) (2001) 187–439. [38] M. Drastik, A. Ctvrtnickova, O. Zmeskal, J. Kucerik, Aggregation of Humic an Fulvic Acids in Diluted Solutions, World Scientific and Engineering Acad and Soc, Athens, 2009. [39] D.E. Kile, C.T. Chiou, Water solubility enhancements of DDT and trichlorobenzene by some surfactants below and above the critical micelle concentration, Environ. Sci. Technol. 23 (7) (1989) 832–838. [40] M. Terashima, M. Fukushima, S. Tanaka, Influence of pH on the surface activity of

[41]

[42]

[43] [44] [45]

[46] [47]

[48]

11

humic acid: micelle-like aggregate formation and interfacial adsorption, Colloid Surf. A-Physicochem. Eng. Asp. 247 (1–3) (2004) 77–83. M. Meier, K. Namjesnik-Dejanovic, P.A. Maurice, Y.P. Chin, G.R. Aiken, Fractionation of aquatic natural organic matter upon sorption to goethite and kaolinite, Chem. Geol. 157 (3–4) (1999) 275–284. M. Chorom, P. Rengasamy, Dispersion and zeta potential of pure clays as related to net particle charge under varying pH, electrolyte concentration and cation type, Eur. J. Soil Sci. 46 (4) (1995) 657–665. A. Naidja, P.M. Huang, Aspartic acid interaction with Ca-montmorillonite: adsorption, desorption and thermal stability, Appl. Clay Sci. 9 (4) (1994) 265–281. P.B. Durgin, J.G. Chaney, Dispersion of kaolinite by dissolved organic matter from douglas-fir roots, Can. J. Soil Sci. 64 (3) (1984) 445–455. L. Mercier, C. Detellier, Intercalation of tetraalkylammonium cations into smectites and its application to internal surface-area measurements, Clay Clay Min. 42 (1) (1994) 71–76. G.Y. Sheng, C.T. Johnston, B.J. Teppen, S.A. Boyd, Adsorption of dinitrophenol herbicides from water by montmorillonites, Clay Clay Min. 50 (1) (2002) 25–34. W. Yan, J.F. Zhang, C.Y. Jing, Adsorption of Enrofloxacin on montmorillonite: twodimensional correlation ATR/FTIR spectroscopy study, J. Colloid Interface Sci. 390 (2013) 196–203. S. Hernandez-Ruiz, L. Abrell, S. Wickramasekara, B. Chefetz, J. Chorover, Quantifying PPCP interaction with dissolved organic matter in aqueous solution: combined use of fluorescence quenching and tandem mass spectrometry, Water Res. 46 (4) (2012) 943–954.