Hepatotoxic microcystin removal using pumice embedded monolithic composite cryogel as an alternative water treatment method

Water Research 90 (2016) 337e343

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Hepatotoxic microcystin removal using pumice embedded monolithic composite cryogel as an alternative water treatment method Fatma Gurbuz a, *, S¸eyda Ceylan b, Mehmet Odabas¸ı b, Geoffrey A. Codd c, d a

Department of Environmental Engineering University of Aksaray, Aksaray 68200, Turkey Department of Chemistry, Faculty of Science, Aksaray University, Aksaray, Turkey c Biological and Environmental Sciences University of Stirling, Stirling FK9 4LA, UK d School of the Environment, Flinders University Adelaide, South Australia 5042, Australia b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 17 December 2015 Accepted 23 December 2015 Available online 29 December 2015

Microcystins are the most commonly encountered water-borne cyanotoxins which present short- and long-term risks to human health. Guidelines at international and national level, and legislation in some countries, have been introduced for the effective health risk management of these potent hepatotoxic, tumour-promoters. The stable cyclic structure of microcystins and their common production by cyanobacteria in waterbodies at times of high total dissolved organic carbon content presents challenges to drinking water treatment facilities, with conventional, advanced and novel strategies under evaluation. Here, we have studied the removal of microcystins using three different forms of pumice particles (PPs), which are embedded into macroporous cryogel columns. Macroporous composite cryogel columns (MCCs) are a new generation of separation media designed to face this challenging task. Three different MCCs were prepared by adding plain PPs, Cu2þ-attached PPs and Fe3þ-attached PPs to reaction media before the cryogelation step. Column studies showed that MCCs could be successfully used as an alternative water treatment method for successful microcystin removal. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Microcystin Pumice Cryogels IMAC Water treatment

1. Introduction Eutrophication, with consequent increases in cyanobacterial mass populations in water resources, is becoming a significant environmental threat throughout the world (Schindler, 1975; Smith et al., 1999). The exacerbating effects of climate change on cyanobacterial bloom formation, size and spread are additionally being recognized (Paerl and Paul, 2012). Microcystins (MCs) are the most commonly encountered, abundant and potent cyanotoxins and their risk management is also of increasing public interest since these toxins can occur in raw drinking water sources and in ineffectively-treated drinking waters (Chorus and Bartram, 1999; Codd et al., 2005). MCs are cyclic heptapeptides (Pearson et al., 2010; Metcalf and Codd, 2012). Of these, one of the most often identified, environmentally abundant and acutely toxic, is MC-LR (Fig. 1), which can be

* Corresponding author. E-mail addresses: [email protected], (F. Gurbuz). http://dx.doi.org/10.1016/j.watres.2015.12.042 0043-1354/© 2016 Elsevier Ltd. All rights reserved.

[email protected]

produced by species of several cyanobacteria, including Microcystis, Anabaena and Planktothrix, which are increasingly found in waterbodies as water blooms and scums due to eutrophication (Chorus and Bartram, 1999; Codd et al., 2005). The general structure of MC is: (D-Ala-L-X-D-erythro-ß-Methyl-DisoAsp-L-Y-Adda-isoGluN-methyldehydroAla), with X and Y representing the two variable amino acids and ADDA, shorthand for 3-amino-9-methoxy-2,6,8trimethyl-10-phenyldeca-4,6-dienoic-acid. So far, there have been over 90 MC variants identified (McElhiney and Lawton, 2005; Pearson et al., 2010; Metcalf and Codd, 2012). Out of all variants, microcystin-LR (MC-LR) and microcystin-RR (MC-RR) are the most commonly studied MCs (Meriluoto and Spoof, 2008). Moreover, a provisional safety guideline of 1.0 mg/L MC-LR in drinking water has set by the world Health Organization (Falconer, 1999). The stable cyclic structure of these toxins has presented many challenges to water treatment facilities where conventional processes have limited effect on the removal of MCs. Several strategies for the removal of MCs from water have been investigated. Chemical methods that produce immediate results include oxidation studies using ozone (Onstad et al., 2007; Sharma et al., 2012). However, caution should be taken when applying

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Fig. 1. Structure of microcystin, MC-LR, X ¼ L-Leucine (L) ve Z ¼ L-Arginine (R) R1 ve R2, H or CH3 (Gurbuz, 2014).

these methods due to their adverse effects on other organisms and the expedited extracellular release of MCs (Chorus and Bartram, 1999). Other methods including UV photolysis (Pelaez et al., 2012; He et al., 2012), also in the presence of TiO2 (Lawton et al., 1999), show potential as reliable treatment methods when used under appropriate conditions. Advanced oxidation processes such as pre-ozonation and photo-irradiation using UV, have been successful but they may not be cost-effective due to high maintenance costs for example if only used seasonally during cyanobacterial bloom events. Adsorption studies, using for example activated carbon (Pendleton et al., 2001; Huang et al., 2007), pumice (Gurbuz and Codd, 2008) and graphene oxide (Zhao et al., 2011; Pavagadhi et al., 2013) have shown high potential for removing MCs. Due to the special molecular structure of MCs, with seven carbonyl groups and two or more free carboxyl groups, they show a great potential affinity toward metals. Xu et al. (2006) have successfully enriched peptides using immobilized Feþ3 ions on magnetic microspheres and iron oxide (maghemite) nanoparticles have been examined for MC-LR removal from water (Lee and Walker, 2011). Likewise, the Fenton and modified Fenton-like oxidation reactions have also received attention as a feasible and promising alternative for MC degradation (Bandala et al., 2004; Antoniou et al., 2010). All of these studies have shown that the adsorption kinetics differed with changing pH, with maximum sorption at low pH and decreasing sorption as pH was increased. Changes in hydrophobicity of MC-LR as a function of pH may also contribute to the pH-dependent adsorption behaviour. Immobilized metal affinity chromatography (IMAC) a partitioning technique to increase the selectivity and adsorption capacity by using some transition metal ions (Cu2þ, Ni2þ, Fe2þ etc.) as affinity ligands, was first formulated and introduced by Porath et al. (1975). IMAC offers some advantages including easy preparation, high adsorption capacity and stability (Ceylan and Odabas¸ı, 2014). In IMAC, affinity separation is based on interaction between metal ions and accessible amino acids such as mainly histidine and to a lesser extent tryptophan, cysteine, aspartate, glutamate, etc. on biological molecules (Yip and Hutchens, 1994). Cryogels are alternative column materials for separation media, and have some advantages including large pores, short diffusion paths, low pressure drop and very short residence time during both the adsorption and elution periods when compared with other conventional materials (Daniak et al., 2004; Derazshamshir et al.,

2002; Ceylan and Odabas¸ı, 2013,2014) However, cryogels have low adsorption capacity because of the low surface area of the supermacropores within the matrix. In order to amend the binding capacity of supermacroporous cryogels, particle-embedding methods were introduced to separation media (Erzengin et al., 2011). Recently, several natural materials plant biomass, powdered activated carbon, clay minerals and fungi have been introduced to separation media as potential adsorbents (Newcombe et al., 2003,). Pumice particles used in this study as embedded materials have several advantages including such as low cost, high surface area for high adsorption capacity, chemical reactivity, hydrophilicity and lack of toxicity when compared to other natural materials and commercial synthetic sorbents (Gurbuz and Codd, 2008). The aim of this research was to design and evaluate pumice particle-embedded macroporous composite cryogel columns, thereby combining some advantages of cryogels (i.e., short diffusion path, low pressure drop, very short residence, etc.) with pumice particles (i.e., high surface area for high adsorption capacity, chemical reactivity, etc.) to remove dissolved MCs from water with high efficiency, in an environmentally-friendly, economical and reproducible manner. 2. Methods and materials 2.1. Materials Hydroxyethyl methacrylate (HEMA) was obtained from Fluka A.G. (Buchs, Switzerland), distilled under reduced pressure in the presence of hydroquinone inhibitor, and stored at 4  C until use. N,N’-methylene-bis-acrylamide (MBAAm) and ammonium persulphate (APS) were supplied by Sigma (St. Louis, MO, USA). All other chemicals were of reagent grade and were purchased from Merck AG (Darmstadt, Germany). Pumice was obtained from the Pumice Research Centre, Suleyman Demirel University, (Isparta, Turkey). N,N,N0 ,N0 -tetramethylethylenediamine (TEMED) was obtained from Fluka A.G. (Buchs, Switzerland). Water used in the experiments was purified using a Barnstead (Dubuque, IA, USA) ROpure LP® reverse osmosis unit with a high-flow cellulose acetate membrane (Barnstead D2731), followed by a Barnstead D3804 NANOpure® organic/ colloid removal and ion-exchange packed bed system. Empty cartridge columns, 3 cm long, 0.6 mm internal diameter were used, in which composite cryogel, which were packed with

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metal-attached pumice particulates. Columns were initially saturated with deionised water. The pH in all adsorption trials was maintained at 6.5 to 7.0. 2.2. Preparation of pumice particles (PPs) Natural pumice particles were pre-treated to remove extractable materials that can affect surface area of particles (and hence adsorption rate and capacity). To achieve this, particles were exposed to alkali (3.0 M NaOH) and acid (3.0 M HCl) solutions, and a heating process (130  C for 5 h) to remove organic pollutants from the pores and surface of the particles to enlarge the surface area. The pre-treated PPs were then washed with deionised water and dried overnight at 180  C. PPs of about 2 mm in diameter were obtained by sedimentation, and kept in desiccators until used (Jones et al., 1986). 2.3. Preparation of Cu2þ and Fe3þ-attached pumice particles (Cu2þAPPs and Fe3þ-APPs) Two different pumice samples of 1.0 g were treated with Cu(NO3)2 and Fe(NO3)3 solutions (100 mg/L, pH 5.0 solutions adjusted with 0.1 M HCl and 0.1 M NaOH) separately at room temperature for 2 h. The initial and final concentrations of 2 different ions solutions were determined with a graphite furnace atomic absorption spectrometer. The experiments were performed in triplicate. The Cu2þ and Fe3þ concentrations in the initial and final solutions were used to calculate the amount of Cu2þ and Fe3þ ions attached to the surface of the PPs (Ünlü et al., 2011). 2þ

3þ

2.4. Preparation of Cu - APPs and Fe monolithic composite cryogels

- APPs embedded

Supermacroporous monolithic composite cryogels embedded with Cu2þ-APPs and Fe3þ-APPs were prepared as follows: Monomers (100 mg N,N0 -methylene-bis-acrylamide and 0.6 mL hydroxyethyl methacrylate) were dissolved in deionized water (9 mL). After degassing the mixture under vacuum for 5 min to eliminate soluble oxygen, the mixture was divided to two aliquots in plastic syringes (5 mL, i.d. 0.8 cm) to prepare two different composite columns and previously-prepared 15-g Cu2þ-APPs and Fe3þ-APPs were added to plastic syringes. The composite cryogels were produced by free radical polymerization. After adding APS (100 mL, 10% (w/v) to the syringes, the mixtures were cooled in an ice bath for 2e3 min. Then, TEMED (20 mL) was added to the mixtures, and the contents were rotated for 1 min. Finally, the polymerization mixtures in the syringes were frozen at 12  C for 24 h and then thawed at room temperature. For the removal of unconverted monomers and initiator, washing solutions (diluted HCl solution and water-ethanol mixture) were recirculated through the columns, until the composite cryogel columns were clean. The purity of the composite cryogels was followed by observing the change of optical densities of the samples taken from the liquid phase in the recirculation system. After washing, the composite cryogels were stored in buffer containing 0.02% sodium azide at 4  C until use. An illustration of cryogel embedded with Me2þ,3þAPPs for MC removal is given in Fig. 2. 2.5. Characterization of pumice and monolithic composite cryogel The chemical composition of the pumice was determined by XRF. Pore structure and morphology of the monolithic cryogel were studied by scanning electron microscopy (SEM).

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2.6. Microcystin extraction Cultures of Microcystis PCC 7806, which produces MCs, were grown under a continuous light regime (fluorescent white light, irradiance on growth flask surfaces, about 25 mEm2 s1.)at 20e24  C, in BG11 medium with nitrate and sparged with filtered air at 800e1500 mL min1. Cells were harvested by centrifuging and lyophilized. MCs were extracted from batches of 30 mg lyophilized cells suspended in MilliQ water (18.2 MU cm1), and disrupted by ultrasonication for 5 min with cooling in ice. After three subsequent freezeethaw cycles, the supernatant containing MCs was collected by centrifuging at 10,000  g for 10 min. 2.7. Analytical methods MCs were quantified by high-performance liquid chromatography with photodiode array detection (HPLC-PDA, Shimadzu) using a Symmetry column (C18 Waters, 3.9 mm internal diameter 150 mm, 5 mm particle size), maintained at 40  C, with a mobile phase of acetonitrile þ 0.1% trifluoroacetic acid (TFA)/MilliQ water þ 0.1% TFA, using a linear gradient from 25% to 75%. The flow rate was 1 mL min1. The UV detector was set to 238 nm. The detection limit for MC-LR was 5 ng on column (25 mL injection volume). For a 25 mL injection this equated to 200 ng per ml of sample. MC variants were quantified for those for which reference MCs were obtained, namely: MCeRR, eYR, eLR, eLA, eLY, eLW, and eLF (Alexis Corporation, Germany).

  y ¼ 27307x  1749:1 R2 ¼ 99:8

(1)

The column was initially saturated with deionised water. The amount of toxin (l mg) removed from solution per gram of pumice at each toxin concentration was determined by difference and plotted against the concentration (l mg mL1) of toxin at equilibrium using the following modified equation (Eq (2); Zhou et al., 1998).

Ceq ¼ ðC0  Ct ÞxV=m

(2)

Where Ceq is the amount of toxin adsorbed to pumice (l mg mg1), C0 (l mg mL1) is the initial concentration and Ct (l mg mL1) is the remaining concentration of toxin in solution at equilibrium. V (mL) is the volume of the solution; m, is the mass of pumice. 3. Results and discussion 3.1. Characterization of test materials The chemical composition of pumice is shown in Table 1. The SEM images of the internal structures of PPs embedded monolithic composite cryogels are shown in Fig. 3A,B,C. The composite cryogels had a labyrinth-like structure of continuous interconnected pores (10e50 mm in diameter) with thin polymer walls that facilitate high liquid velocity. The possible reason for these structures may be the orientation of water crystals and monomer molecules by pumice particles. PPs are visible in Fig. 3B, C. PPs were distributed uniformly into the cryogel network offering a high surface area for MCs loading-capacity. 3.2. Microcystin analysis MC variants were quantified for those for which reference MCs were obtained, namely: MCeRR, eYR, -LR, eLA, -LY, -LW, and eLF (Fig. 4A) The crude extract of Microcystis PCC 7806 contained MCRR, MC-LR, MC-LY variants (Fig. 4B) which are common forms of this cyanotoxin group in freshwater lakes (Chorus and Bartram,

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Fig. 2. Illustration of cryogel embedded with Me2þ,3þ-APPs for MCs.

Table 1 Chemical composition of pumice (Gurbuz and Codd, 2008). Chemical constituent

% Content

SiO2 Al2O3 Fe2O3 TiO2 MgO Na2O K2O CaO MnO

70.0e71.4 12.7e13.3 1.3e1.5 0.1e0.2 0.3e0.6 3.2e3.5 4.0e4.3 0.8e1.2 0.1

1999). The concentrations of MC-RR (27 mg l1), MC-LR (127 mg l1) and MC-LY (36 mg l1) were applied to the columns, greatly exceeded that of the provisional Guideline Value of the World Health Organization for MC-LR in drinking water of 1 mg l1 (Falconer et al., 1999). According to Pearson (1968), while the hard metal ions (e.g. Fe3þ, Ca2þ, Al3þ) prefer oxygen for coordination with biomolecules, the borderline metal ions (e.g., Cu2þ, Ni2þ, Zn2þ, Co2þ) coordinate to

nitrogen, oxygen, and sulphur. In this study, we used Cu2þ and Fe3þ ions for MC adsorption., MC-LY and MC-LR have an Arginine and a Tyrosine residue at variable position Y(4) region respectively, and also, because of Aspartate and Glutamate at positions 3 and 6 respectively, we can say that Fe3þ attached pumice particles embedded composite monolithic cryogels has a greater affinity for both MC-LY and MC-LR containing more groups with oxygen ions.

3.3. Effect of adsorbents MC removal efficiency was tested on Cu minus pumice; Fe3þ minus pumice; pumice minus metals and Fe3þ plus pumice (10 mg) attached cryogel and found that Fe attachment resulted in a high adsorption of MC-LR (5.4 mg/g). However, Fe3þ- Pumice showed better adsorption, which was 7.2 mg/g MC-LR, (Fig. 5). A 100% adsorption of MC-RR and MC-LY was achieved, via either Fe3þ or pumicee Fe3þ. MC-LR adsorption remained at 50e65% due to the high concentration of this toxin loaded onto the columns and possible due to other compounds in the Microcystis cell extracts competing with MCLR for binding sites.

Fig. 3. A,B,C. SEM images of the internal structures of PPs embedded monolithic.

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Fig. 4. A, HPLC chromatogram of MC standards. B, HPLC chromatograms of Microcystin before (ex1) and after (ex2) adsorption by cryogel-pumice (10 mg) -Feþ3.

According to Evanko and Dzombak (1998), hydrophobic interactions can be important mechanisms in the sorption of aromatic organic acids, such as humic substances, onto iron oxide surfaces. Hydrophobic interactions may also play a minor role in MC adsorption onto iron oxide nanoparticles since MC-LR contains an aromatic ring in the ADDA residue and seven peptides exhibiting hydrophobic properties in aqueous media (Pendleton et al., 2001).

It is already established that due to its charge, MC-LR is readily removed at lower pH (Miller et al., 2001; Lawton et al., 1999; Gurbuz and Codd, 2008; Lee and Walker, 2011), However the pH in the blooming eutrophic waterbodies were between 7 and 9 and acidification, of the water for example pH 3 to 5 was not carried out but maintained, to reduce operational requirements, at pH 6 to 7. Takenaka et al. (1995) have pointed out that FeO3 would degrade MC-LR in extreme acid conditions, at around pH 2. Anipsitakis and Dionysiou (2004) found similar results. Fe þ3 in acidified conditions generates Fe (OH) 2 and the latter would generate hydroxyl radicals, which can then act as oxidant degrading MC-LR. This was evidenced by the fact that at high pH over 7, most of toxin can be eluted from microgel-Fe(III) (Dai et al., 2012). Here, in this study MC was adsorbed and removed Fe3þ ions with pumice attached to the cryogel under neutral conditions. 3.4. Effect of adsorbent dosage

Fig. 5. Microcystin adsorption via different substances attached to cryogel

The effect of adsorbent doses including 10, 20 30 and 40 mg of Fe3þ- pumice-attached cryogels, were investigated using 50 mL

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trial volumes of Microcystis PCC 7806 extract, containing 27 mg/l MC-RR, 127 mg/L MC-LR, and 36 mg/L MC-LY. Higher Fe3þ pumice concentrations (i.e.,higher solideliquid ratios) resulted in greater removal of MCs probably due to the increased surface area available for adsorption (Fig. 6). Nevertheless, the most efficient removal was obtained with 20 mg Fe3þ-pumice. Although MCs adsorption were increased by increasing the dose of 30, 40 mg the ratio of adsorbed MCs per mg of adsorbents decreased (Fig. 6). The removal ratio of the toxin then slightly decreased with higher adsorbent probably due to blockage for binding sites. In the study of Lee and Walker, 2011 the adsorption of MC-LR at the initial concentration of 100_mg/L was found to be 73% and 94% using 0.3 and 2.3 g/L of Feoxide, respectively. A 100% adsorption of MC-LR from the broken cell extracts of Microcystis PCC7813 was achieved via pumice (1e2 g) (Gurbuz and Codd, 2008) Increased volume resulted in a decrease in removal of MC-LR with 1 g of pumice. Dissolved and cell-bound MC concentrations in raw waters containing cyanobacterial blooms are frequently above the World Health Organization Provisional Guideline Value of 1 mg/l MC-LR and can be as high as 5 to at least 70 mg l1 in the case of scum formation (Welker et al., 2001). MC-LR is seldom the only MC structural variant present in a toxic cyanobacterial bloom or scum (e.g. Spoof et al., 2003; Messineo et al., 2009; Faassen and Lürling, 2013). For example, this variant may account for 23e94% of the total MC concentration; and alongside at least 7 other MC variants (Faassen and Lürling, 2013). In view of this diversity, it is advisable that investigations into the removal of MCs from potable water extend to multiple toxin variants, as determined here.

3.5. Adsorption isotherms Langmuir adsorption model (Langmuir, 1916) expressed by Eq. (3) was applied to the cryogel including 20 mg of Fe3þ-pumice using 50 ml trial volumes of PCs containing 27 mg/l MC-RR, 127 mg/l MC-LR, and 36 mg/l MC-LY to analyse the experimental data related to the binding behaviour of MCs onto Fe3þ-pumice in cryogel. This equation can be linearized to Eq. (4) to obtain semi reciprocal plot.

Qe ¼ Qm Ce =Kd þ Ce

(3)

Ce =Qe ¼ Ce =Qm þ Kd =Qm

(4)

Here, Qe is equilibrium amount of adsorbed MCs (mg/mg), Ce is the equilibrium concentration of MCs (mg/ml), Kd ¼ k2/k1 is the dissociation constant of the system. Ce versus Ce/Qe data gave a linear correlation coefficient (R2) for all adsorption experiments carried out for MCs, and results were listed in Table 2. Kd and Qm (maximum adsorption) values of adsorption experiments were extracted from slope and intercept of the straight line. In an ideal chromatographic interaction, Kd values should be

Table 2 Adsorption parameters obtained from experimental results. Microcystins

Qexp (mm/mg)

Langmuir constants Qm (mm/mg)

MC-RR MC-LY MC-LR

4.5 7.0 9.0

4.1 6.9 11.5

R2

Kd 8

2,09.10 5,34.108 1,16.105

0.9901 0.9954 0.9997

between 104e108 M for the target molecules. As seen in Table 2, Fe3þ-pumice containing cryogel column is an ideal adsorbent for MCs removal, and R2 obtained from adsorption parameters indicates that the Langmuir model assuming a monolayer adsorption takes place onto a surface could be applied to these affinity systems. 3.6. Desorption of MCs from Fe3þ-APP embedded monolithic composite cryogels Desorption which may make a treatment process more economical, may help to elucidate the mechanism of adsorption and also help in the recovery of adsorbate and adsorbent (Gurbuz and Codd, 2008). Desorption of MCs from Me2þ,3þ-APPs was initially attempted in the column system by using 100% methanol. However, 100% methanol dehydrated the cryogels. Hence70% methanol in water þ0.01% TFA was used for the desorption trials. For regeneration, Milli Q water passed through the column followed by 0.05 M NaOH. Up to 95% of the adsorbed MCs were desorbed from the columns allowing these to be used for MC adsorption up to 5 times. No detectable metal release occurred from the columns during this process and we conclude that that a solution of 70% methanol in water þ0.01% TFA solution is a suitable desorption agent for MCs removal from this laboratory-based immobilized metal ion affinity system. 4. Conclusions Fe3þ-APPs-pumice embedded monolithic composite cryogels, provides a promising adsorbent for the removal of MCs from water. Under the reported conditions,no detectable iron release occurred during the regeneration cycles of MC desorption and column reuse. Electrostatic interactions played an important role in controlling MC adsorption. The indigenous and inexpensive nature of pumice, embedded into cryogel, merits further investigation as an adsorbent for cyanotoxin removal from water with the prospect of significantly lowering water treatment costs. Acknowledgement This study was supported by Cost ES1105 (Tubitak 110Y316).

adsorbed MC ( ug/mg)

References 10

RR

9

LR

8

LY

7 6 5 4 3 2

1 10

20

Fe-pumice (mg)

30

40

Fig. 6. The effect of Fe-pumice quantity on MC adsorption from Microcystis PCC 7806 extracts.

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