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Application of powdered activated carbon for the adsorption of cylindrospermopsin and microcystin toxins from drinking water supplies
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Application of powdered activated carbon for the adsorption of cylindrospermopsin and microcystin toxins from drinking water supplies Lionel Ho a,b,*, Paul Lambling c, Heriberto Bustamante d, Phil Duker d, Gayle Newcombe a a
Australian Water Quality Centre, SA Water Corporation, 250 Victoria Square, Adelaide, SA 5000, Australia School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia c ´ Ecole Supe´rieure de Chimie Physique E´lectronique de Lyon, 43, Boulevard du 11 Novembre 1918, BP 2077, 69616 Villeurbanne Cedex, France d Sydney Water, PO Box 399, Parramatta NSW 2124, Australia b
article info
abstract
Article history:
Cylindrospermopsin (CYN) and microcystin are two potent toxins that can be produced by
Received 17 September 2010
cyanobacteria in drinking water supplies. This study investigated the application of
Received in revised form
powdered activated carbon (PAC) for the removal of these toxins under conditions that
8 March 2011
could be experienced in a water treatment plant. Two different PACs were evaluated for
Accepted 9 March 2011
their ability to remove CYN and four microcystin variants from various drinking water
Available online 17 March 2011
supplies. The removal of natural organic material by the PACs was also determined by measuring the levels of dissolved organic carbon and UV absorbance (at 254 nm). The PACs
Keywords:
effectively removed CYN and the microcystins from each of the waters studied, with one of
Adsorption
the PACs shown to be more effective, possibly due to its smaller particle diameter. No
Cylindrospermopsin (CYN)
difference in removal of the toxins was observed using PAC contact times of 30, 45 and
Microcystin
60 min. Furthermore, the effect of water quality on the removal of the toxins was minimal.
Natural organic material (NOM)
The microcystin variants were adsorbed in the order: MCRR > MCYR > MCLR > MCLA. CYN
Powdered activated carbon (PAC)
was found to be adsorbed similarly to MCRR. ª 2011 Elsevier Ltd. All rights reserved.
1.
Introduction
The microcystins and cylindrospermopsin (CYN) (see Fig. 1 for structures) are potent hepatotoxins produced by a number of species of freshwater cyanobacteria, of which Microcystis aeruginosa and Cylindrospermopsis raciborskii are two of the more commonly encountered. Consumption of waters containing these cyanobacterial toxins (cyanotoxins) can lead to serious health risk with events such as diarrhoea, nausea, vomiting and even death occurring (Falconer, 1989). The microcystins have also been implicated as promoters of liver tumours (Nishiwaki-Matsushima et al., 1992), while CYN has been
associated with serious tissue damage and cell necrosis in the liver, kidney and other organs (Falconer, 2005). In addition, studies have also suggested that CYN is carcinogenic, genotoxic and involved in the inhibition of protein synthesis (Froscio et al., 2001, 2003; Falconer, 2005). As a result of the concerns about the effect of microcystins, a guideline value of 1 mg L1 for microcystin-LR (MCLR) in drinking water has been issued by the World Health Organisation (WHO). Similarly, the Australian Drinking Water Guideline value for microcystin has been set at 1.3 mg L1 as MCLR toxicity equivalents. While no official guideline value currently exists for CYN, the WHO is in the midst of proposing
* Corresponding author. Australian Water Quality Centre, SA Water Corporation, 250 Victoria Square, Adelaide, SA 5000, Australia. Tel.: þ61 8 7424 2119; fax: þ61 8 7003 2119. E-mail address: [email protected] (L. Ho). 0043-1354/$ e see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2011.03.014
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Fig. 1 e Molecular structures of: (a) microcystin and (b) cylindrospermopsin. Note: The generic structure of microcystin-XY is shown with the corresponding variants presented in the accompanying table.
a 1 mg L1 level, due to concerns regarding the effect of CYN (Rodriguez et al., 2007). In Australia, CYN has predominantly been detected in more tropical and subtropical areas, in particular Queensland. A survey of 47 water sources by McGreggor and Fabbro (2000) detected CYN in 14 of those sources at an average concentration of 3.4 mg L1 with a maximum concentration of 20 mg L1 in subsurface samples. In contrast, considerably higher concentrations of microcystin have been detected in Australian water bodies, in the g L1 concentration range in some cases (Falconer, 2005; Kemp and John, 2006); however, unlike CYN a majority of the microcystins would be contained within the cell (Falconer, 2005). Conventional water treatment methods such as coagulation, flocculation, sedimentation and filtration are ineffective at removing dissolved (extracellular) cyanotoxins (Himberg et al., 1989; Mouchet and Bonne´lye, 1998; Chow et al., 1999; Newcombe and Nicholson, 2004). Treatment options which have had success in removing extracellular cyanotoxins include activated carbon (both powdered and granular), nanofiltration, ozonation and chlorination (provided a specific chlorination exposure level is applied, typically w30 mg min L1) (Mouchet and Bonne´lye, 1998; Newcombe and Nicholson, 2004; Dixon et al., 2010). Powdered activated carbon (PAC) is one of the major treatment barriers for the removal of extracellular
cyanotoxin in most Australian water treatment plants (WTPs) as it can be applied when required, which is generally advantageous for cyanotoxin control since cyanobacterial problems are of a transient, intermittent nature. PAC adsorption has been shown to be effective in many studies if the application is optimised (Donati et al., 1994; Cook and Newcombe, 2002, 2008; Newcombe and Nicholson, 2004; Ho et al., 2008; Campinas and Rosa, 2010a,b). While PAC is a widely used and accepted method of water treatment, there have been few studies undertaken into its effective use in removing cyanotoxins such as CYN and the microcystins under conditions that could be experienced in a WTP. Consequently, more in depth systematic studies are required to ascertain the effectiveness of PAC for the removal of these cyanotoxins under such conditions. Most of studies relating to the PAC adsorption of cyanotoxins have been conducted on the microcystins, in particular, MCLR (Falconer et al., 1989; Donati et al., 1994; Pendleton et al., 2001; Cook and Newcombe, 2002, 2008; Campinas and Rosa, 2010a,b). Many of these studies have suggested that coal- and wood-based carbons are the best for microcystin adsorption due to their large mesopore volume. Cook and Newcombe (2002) conducted PAC adsorption experiments on four variants of microcystin and showed differences in the adsorption of each variant with the ease of removal following the order: MCRR > MCYR > MCLR > MCLA. These results were confirmed
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using a range of PACs with different starting materials and activation methods. Cook and Newcombe (2002) attributed the differences to a combination of factors including the hydrophobicity of the variants and electrostatic interactions. Previous studies have also suggested that the PAC adsorption of cyanobacterial metabolites, such as the microcystins, may be significantly influenced by the size and conformation of the adsorbate (Donati et al., 1994; Pendleton et al., 2001; Cook and Newcombe, 2002; Sathishkumar et al., 2010). Moreover, Donati et al. (1994) and Pendleton et al. (2001) suggest that the size and conformation of the microcystin molecules, along with the pore volume characteristics of the carbon, appear to be the dominant mechanism for microcystin adsorption, with minimal influences from electrostatic interactions due to the hydrophobic nature of the microcystin molecule and low number of ionisable functional groups. Another factor which can influence the adsorption of cyanobacterial metabolites is the presence of natural organic material (NOM), in particular, the concentration and character of NOM (Donati et al., 1994; Newcombe et al., 1997, 2002; Cook and Newcombe, 2008). These studies have shown that NOM can simultaneously compete with the cyanobacterial metabolites for adsorption sites on the surface of the activated carbon, thereby reducing the adsorption efficiency of the cyanobacterial metabolites. To date, only one study has been published in the peerreviewed literature with respect to the evaluation of PAC for the removal of CYN (Ho et al., 2008). However, no studies have been conducted relating the PAC adsorption of a combination of cyanotoxins, such as the microcystins and CYN. This is important since the onset of climate change is predicted to increase both the occurrence and intensity of cyanobacterial blooms (Paerl and Huisman, 2008). Coupled with warmer water temperatures and invading blooms of CYN-producing cyanobacteria (Chapman and Schelske, 1997; Padisa´k, 1997; Stirling and Quilliam, 2001), there is a greater likelihood that multiple cyanotoxins will be present in drinking water supplies. Consequently, knowledge pertaining to the parallel removal of a range of cyanotoxins by PAC will enable water authorities to have plans to mitigate issues caused by these cyanotoxins, including selection of the most appropriate PAC. The major aim of this study was to investigate the PAC adsorption of extracellular cyanotoxins, in particular, CYN and four microcystin variants, MCLR, MCLA, MCYR and MCRR. Two different PACs were evaluated in various Australian drinking water supplies under conditions that would be experienced in a WTP. The adsorption of NOM was also examined, with respect to its impact on the adsorption of the cyanotoxins. A final aim was to relate the adsorption of CYN with that of the microcystins under equivalent conditions.
2.
Experimental procedures
2.1.
Materials and reagents
Experiments were conducted using purified CYN (95% pure) isolated from a laboratory culture of C. raciborskii (Palm Island, Queensland, CYP020). The toxin was dissolved in ultrapure water (Millipore Pty Ltd, USA) and stored at 20 C prior to use.
Purified (95% pure) microcystin variants, MCLA, MCYR, MCRR and MCLR were purchased from a commercial supplier (Sapphire Bioscience, Australia). Stock solutions of each of the microcystin variants were prepared in 50% methanol and stored at 20 C prior to use. Aliquots were taken from the dissolved stock solution and dosed into experiments at specified concentrations. Table 1 lists some of the characteristics of the cyanotoxins. Unfiltered raw water obtained from the inlet of three WTPs was stored at 4 C until used. Warragamba Dam water (dissolved organic carbon (DOC) ¼ 5.0 mg L1, UV absorbance at 254 nm (UV254) ¼ 0.093 cm1, pH ¼ 7.5) was supplied by Sydney Water in New South Wales. Waikerie (DOC ¼ 4.3 mg L1, UV254 ¼ 0.076 cm1, pH ¼ 7.7) and Swan Reach (DOC ¼ 3.9 mg L1, UV254 ¼ 0.072 cm1, pH ¼ 7.6) waters were supplied by United Utilities Australia in South Australia. Waikerie and Swan Reach WTPs are situated along the River Murray in South Australia with Swan Reach WTP (coordinates 34 340 0400 S 139 350 5900 E) downstream of Waikerie WTP (coordinates 34 100 6000 S 139 580 6000 E). Warragamba Dam (coordinates 33 530 0000 S 150 350 4400 E) is located approximately 65 km west of Sydney in New South Wales. Historically, only very low concentrations of CYN and the microcystins have been detected in the three water sources, in most cases the toxins have been undetectable in these waters; however, high concentrations of cyanobacterial species known to produce these toxins have been detected in these waters. Two commercially available PACs were used in this study. PAC-A was obtained from the Waikerie WTP where it is used to mitigate cyanobacterial metabolites; this PAC is also routinely used at the Swan Reach WTP. PAC-B was supplied from Sydney Water and used at WTPs which source water from Warragamba Dam. Some general characteristics of the PACs are listed in Table S1 of the Supporting Information. The PACs were dried in an oven at 110 C for 24 h, then cooled and stored in a desiccator prior to use. For adsorption experiments, PAC slurries were prepared by mixing the required carbon dose with 5 mL of ultrapure water.
2.2.
PAC adsorption experiments
All PAC jar tests were conducted at room temperature (25 C). An FMS6V (SEM, Australia) variable speed, six paddle gang stirrer with 7.6 cm diameter flat paddle impellers and B-Ker2 gator jars (Phipps and Bird, USA) containing 1 L of sample waters was used. PAC doses of 5, 10, 25, 50 and 100 mg L1
Table 1 e Characteristics of the cyanotoxins used in this study. Cyanotoxin
Cylindrospermopsin Microcystin RR YR LR LA
Molecular LD50 (ug kg1 Charge at body weight) pH 6.0e8.5 weight (g mol1) 415.43 1038.20 1045.19 995.17 910.06
2100 600 70 50 50
0 (þ & ) 0 ( & þþ) 1 ( & þ) 1 ( & þ) 2 ()
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were employed as this range represents low to high doses that can be applied at the respective WTPs (Ho et al., 2009). The cyanotoxins were spiked into the waters (20 mg L1 of CYN and 4 mg L1 each of MCRR, MCYR and MCLA, and 10 mg L1 of MCLR) and constantly stirred at 100 rpm throughout the experiment to ensure PAC remained suspended in solution. PAC slurries were added at time zero and experimental samples were taken at three time intervals; 30, 45 and 60 min. Samples were collected and immediately filtered through prerinsed 0.45 mm cellulose nitrate filters (Schleicher and Schuell, Germany) prior to analysis. Any losses of the cyanotoxins other than PAC adsorption were accounted for by jar test experiments performed in the absence of PAC. Microcystin adsorption experiments were conducted where all variants were spiked into the same experiments, while CYN adsorption experiments were conducted separately. Cook and Newcombe (2008) previously showed no competitive adsorption between the microcystin variants.
2.3.
Analyses
Prior to high performance liquid chromatographic (HPLC) analysis, the cyanotoxins were concentrated from the sample waters by solid phase extraction using methods described previously by Metcalf et al. (2002) and Nicholson et al. (1994) for CYN and the microcystins, respectively. An Agilent 1100 series HPLC system comprising of a quaternary pump, autosampler and photodiode array detector (Agilent Technologies, Australia) was employed for the analysis of the cyanotoxins. For CYN analysis, sample volumes of 25 mL were injected into a 150 4.6 mm Apollo C8 column (Alltech, Australia) at a flow rate of 0.6 mL min1 (column temperature 30 C). Two mobile phases (mobile phase A: 0.5% formic acid and mobile phase B: 100% acetonitrile) were used during the gradient run (0 min, 100% A; 25 min, 90% A, 10% B; 25.01 min, 70% A, 30% B, 30.01 min, 100% A, 55 min, 100% A). CYN concentrations were determined by calibrating the peak areas with that of a certified reference standard (Institute of Marine Biosciences, National Research Council, Canada). The method has a detection limit of 0.5 mg L1. For microcystin analysis the volume of sample injected into the 150 4.6 mm Luna C18 column (Phenomenex, Australia) was 25 mL at a flow rate of 1.0 mL min1 (column temperature 30 C). Two mobile phases (mobile phase A: 30% acetonitrile and mobile phase B: 55% acetonitrile) were used during the gradient run (0 min, 100% A; 12.5 min, 50% A, 50% B; 15 min, 100% B; 23 min 100% A; 32 min, 100% A). Microcystin concentrations were determined by calibrating the peak areas with that of certified reference standards (Sapphire Bioscience Pty Ltd, Australia). The method has a detection limit of 0.1 mg L1. DOC measurements were made on an 820 Total Organic Carbon Analyser (Sievers Instruments Inc, USA). UV254 measurements were carried out on a UV-1201 UV/VIS Spectrophotometer (Shimadzu Corporation, Japan). Molecular weight distributions of the waters were determined using high performance size exclusion chromatography (HPSEC) according to the method of Chow et al. (2008). Briefly, the HPSEC method utilised a 2690 separation module and 996 photodiode array detector operating at 260 nm (Waters Pty Ltd, Australia). Separation was performed with a Shodex KW 802.5 column
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(Shoko Co. Ltd, Japan) and a 0.1 M phosphate buffer solution (pH 6.8, ionic strength adjusted to 1.0 M with sodium chloride). An injection volume of 100 mL was used at a flow rate of 1 mL min1. The column had an effective resolving range of 50e50,000 Da and the retention time was calibrated for apparent molecular weight using polystyrene sulphonate standards (Polysciences Inc, USA) of molecular weights 35,000, 18,000, 8000, and 4600 Da.
3.
Results and discussion
3.1.
Adsorption of NOM
The concentration and character of NOM can affect the adsorption of cyanobacterial metabolites through competitive adsorption mechanisms (Donati et al., 1994; Newcombe et al., 1997, 2002; Cook and Newcombe, 2008). In particular, it is believed that the greatest adsorption competition would exist between compounds of similar size and shape (Newcombe et al., 1997, 2002). However, competitive adsorption is not only dependent upon the size of the competing compound, but also highly dependent upon the pore volume distribution of the adsorbent (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Li et al., 2003; Ho et al., 2009). In addition, previous studies have shown that solution and surface chemistry (eg. pH and PAC surface charge) have minimal influence on the adsorption of cyanobacterial metabolites (Pendleton et al., 2001; Cook and Newcombe, 2002, 2008). The initial DOC and UV254 values of Swan Reach and Waikerie WTP inlet waters were similar, attributed to the fact that both WTPs source water from the River Murray in South Australia. In contrast, Warragamba Dam water, which is sourced from New South Wales, contained NOM of higher DOC and UV254 values. Fig. 2 shows the removal of DOC and UV254 by the PACs after a contact time of 60 min. Negligible difference was observed for the removals of DOC in each of the waters (Fig. 2a), while some differences were observed for the removal of UV254 (Fig. 2b). PAC-B in Warragamba water removed more UV absorbing compounds than PAC-A in the South Australian waters, with the differences increasing with PAC dose. For example, at a PAC dose of 10 mg L1 the difference was 5%, while for a dose of 100 mg L1 the difference was 14%. It is unclear as to whether these differences were attributed to differences between the PACs or the waters, although it is likely to be a combination of both. The higher PAC doses employed (50 and 100 mg L1) are generally not achievable at most conventional WTPs due to PAC carryover affecting downstream processes, including filtration. Such high PAC doses would dramatically reduce the filter run times in direct/contact filtration causing reductions in water production. However, at the Swan Reach and Waikerie WTPs, these high PAC doses can be applied due to the construction of large contact tanks prior to coagulation to facilitate removal of cyanobacterial metabolites. These high doses resulted in excellent removal of DOC and UV254 of between 60 and 74%. Fig. 3a shows the molecular weight distributions (using HPSEC with UV absorbance as the detection method) of the organics in the three waters. The waters exhibited similar
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profiles although Warragamba water displayed higher UV absorbance than Swan Reach and Waikerie waters across the wavelengths, in particular between 800 and 1200 Da, consistent with Warragamba water’s higher UV254. Previous studies have suggested that the NOM within this region is humic in nature and contains compounds which are highly aromatic and/or contain a higher degree of conjugation (Westerhoff et al., 1999; Newcombe et al., 2002; Chow et al., 2008). Furthermore, Chow et al. (2008) have indicated that NOM in this molecular weight region are hydrophobic and more easily removed by conventional water treatment processes.
The PACs removed a wide range of molecular weight compounds with removal increasing with PAC dose (Fig. 3bed). It is presumed that the removal of the wide range of molecular weight compounds by PAC is attributed to the pore structure of the PACs (Newcombe, 2002). More importantly, the removal of the wide range of molecular weights, suggest that the character of NOM may not have a significant influence in the adsorption of the cyanotoxins when using these PACs, which may be attributed to the PACs containing a broad pore size distribution (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Li et al., 2003; Ho et al., 2009). This will be discussed further in subsequent sections of this manuscript.
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Fig. 3 e Molecular weight distributions of: (a) Swan Reach, Waikerie and Warragamba waters; (b) Swan Reach water after treatment with sequential doses of PAC-A; (c) Waikerie water after treatment with sequential doses of PAC-A; (d) Warragamba water after treatment with sequential doses of PAC-B. In each case, PAC contact time was 60 min.
3.2.
Adsorption of microcystin
Four microcystin variants were studied for the PAC adsorption experiments, MCLR, MCYR, MCRR and MCLA. Whilst a majority of studies have focused on MCLR, as it is one of the most toxic variants, it is important to study other variants as most microcystin-producing blooms generally yield others, and in many cases MCLR is not always the most abundant. The water was spiked with 22 mg L1 total microcystin; consisting 4 mg L1 each of MCRR, MCYR and MCLA, and 10 mg L1 MCLR. These concentrations were chosen as they represent an upper limit or worst case scenario of what could be expected to enter a WTP (Falconer, 2005). Fig. 4a and b show the removal of total microcystins by the PACs in Waikerie and Warragamba waters, respectively. The removal trends for Swan Reach (results not shown) were identical to Waikerie water. The increased contact times did not appear to enhance microcystin adsorption using both PACs in their respective waters as negligible difference was observed using contact times of 30, 45 and 60 min. This suggests that the kinetics of adsorption for both PACs were rapid. The addition of PAC-B in Warragamba water yielded the
highest removal of the microcystins where a PAC dose of 50 mg L1 resulted in removals to below the WHO guideline level of 1 mg L1. In contrast, Waikerie and Swan Reach waters required a PAC-A dose of 100 mg L1 to achieve the same level of microcystin removal. Realistically, a WTP may expect to treat total microcystin concentrations of between 2 and 5 mg L1 and possibly up to 10 mg L1. In these scenarios the predicted PAC doses required to achieve the WHO guideline level in Warragamba water would be 5, 11 and 23 mg L1, respectively. In Waikerie and Swan Reach waters, the corresponding predicted PAC doses would be 9, 23 and 45 mg L1. These predictions were made using the homogenous surface diffusion model (HSDM) and are based on the assumption that the amount of microcystin adsorbed is directly proportional to its initial concentration. Previous studies have shown that the percent removal of microcystin at equilibrium for a given carbon dose in natural water is independent of the cyanotoxin’s initial concentration (Cook and Newcombe, 2002; Ho and Newcombe, 2007). The more favourable adsorption of the microcystins in Warragamba water compared with Waikerie and Swan Reach waters is consistent with the UV254 results where greater
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Fig. 4 e Removal of total microcystins (22 mg LL1) by PAC in: (a) Waikerie water; and (b) Warragamba water. Differences in the PAC adsorption of the microcystin variants after a contact time of 30 min in: (c) Waikerie water; and (d) Warragamba water.
removal was also observed in this PAC-water combination (Fig. 2b). The reasons for this will be discussed later. The trends for removal of each of the four microcystin variants in Waikerie and Warragamba waters after a PAC contact time of 30 min are shown in Fig. 4 c and d In both waters using the respective PACs, the order of the ease of removal of the microcystin variants followed the trend: MCRR > MCYR > MCLR > MCLA, which is consistent with previous studies (Cook and Newcombe, 2002, 2008). The overall charges for the four variants are shown in Table 1. The negative groups are attributed to the dissociated carboxyl groups of D-glutamic acid and D-erythro-b-methyl aspartic acid and the positive charges to the amino group on arginine. It is these differences that may result in the different adsorption characteristic being observed. Attractive or repulsive forces between the cyanotoxin molecule and the activated carbon surface could either enhance or hinder adsorption. Molecular size and conformation of the microcystin molecules may also affect the interaction that the cyanotoxin has with the PAC surface, with smaller conformations favouring adsorption. The observed trend shows that MCRR has the greatest affinity with both PACs and MCLA, the least. Therefore, for effective PAC use in removing microcystins, it is important that all
microcystin variants present are identified due to the differences in their adsorption behaviour.
3.3.
Adsorption of CYN
The adsorption of CYN was also evaluated where CYN was spiked into the waters at a concentration of 20 mg L1; a concentration thought to represent a worst case scenario for a WTP (Falconer, 2005). Swan Reach showed identical trends to Waikerie as observed with the microcystin adsorption experiments (results not shown). Warragamba water, dosed with PAC-B, had higher CYN removal than Waikerie and Swan Reach waters with PAC-A, similar to the microcystin results (see Fig. S1 of the Supporting Information). PAC contact time again did not appear to have significant impact on the removal. The results show that PAC doses required for CYN removal to below the proposed WHO guideline value of 1 mg L1 are 25 mg L1 for Warragamba water and 50 mg L1 for Waikerie and Swan Reach waters. To date, limited studies have been undertaken with respect to the PAC adsorption of CYN under WTP conditions. Ho et al. (2008) used the HSDM to predict the adsorption of CYN using
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two PACs in Hope Valley reservoir water. They determined that PAC could be effective for the removal of CYN, although relatively high doses would be required. For example, at an initial CYN concentration of 5 mg L1, the PAC dose required to remove CYN to below 1 mg L1 would be 25 mg L1 (using a contact time of 60 min). However, in that study the DOC and UV254 of Hope Valley water was appreciably higher at 10.2 mg L1 and 0.325 cm1, respectively. These NOM characteristics have been shown to influence the adsorption of cyanobacterial metabolites through competitive adsorption processes and/or pore blockage mechanisms (Cook et al., 2001; Newcombe et al., 1997).
3.4.
Fig. 5a and b show results of the removal of total microcystins and CYN in Waikerie water using both PACs (after a contact time of 30 min), while Fig. 5c and d show the same but in Warragamba water. In all cases, PAC-B was the superior carbon for the adsorption of all the cyanotoxins with large differences observed between both PACs. In contrast, Fig. 6aed directly compare the removals of microcystin and CYN between the waters using both PACs after a contact time of 30 min. The differences between the waters in Fig. 6 were not as pronounced as those observed between the PACs in Fig. 5aed, suggesting that the PACs used had a wide range of pores which could offset the influence of water quality, in particular the presence of NOM (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Newcombe et al., 2002; Li et al., 2003). This finding also strongly suggests that the PAC type was the major factor influencing cyanotoxin adsorption. The most disparate characteristic between the PACs was the effective particle size, 20e25 mm for PAC-A, and 10 mm for PAC-B. Previous studies have shown that the equilibrium adsorption of a microcontaminant is not affected by particle size (Matsu et al., 2009; Ando et al., 2010); however, the particle size can influence the adsorption kinetics, with more rapid adsorption with smaller
Differences in PAC and water quality characteristics
Further investigations were warranted to determine why the combination of PAC-B and Warragamba water was superior for the adsorption of the cyanotoxins (see Fig. 4 and Fig. S1 of the Supporting Information). It was unclear whether this was due to the differences between the PACs or the waters or a combination of both. Experiments were conducted where PAC-B was evaluated in Waikerie water and PAC-A in Warragamba water, and then compared with the original PAC-water combinations.
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Fig. 5 e Comparison in the removal of: (a) total microcystins; and (b) cylindrospermopsin (CYN) in Waikerie water by PAC-A and PAC-B after a contact time of 30 min. Comparison in the removal of: (c) total microcystins; and (d) CYN in Warragamba water by PAC-A and PAC-B after a contact time of 30 min.
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80
100
d
100
80
60
PAC-B dose (mg L )
c
100
40
-1
PAC-A dose (mg L )
60
40
20
80
PAC-B Waikerie Warragamba
60
40
20
0
0 0
20
40
60
80
100
-1
PAC-A dose (mg L )
0
20
40
60
80
100
-1
PAC-B dose (mg L )
Fig. 6 e Comparison in the removal of total microcystins in Waikerie and Warragamba water using: (a) PAC-A; and (b) PAC-B after a contact time of 30 min. Comparison in the removal of cylindrospermopsin (CYN) in Waikerie and Warragamba water using: (c) PAC-A; and (d) PAC-B after a contact time of 30 min.
particle size (Sontheimer et al., 1988; Najm et al., 1990; Traegner et al., 1996). The results in this study confirm this contention as although PAC-B was the superior carbon at 30 min contact time (Fig. 5), the removals of all cyanotoxins by both PACs was similar at equilibrium (contact time of 3 d, results not shown). Furthermore, negligible difference in the removal of the cyanotoxins was observed between the PACs when PAC-A was ground down to the same particle size as PAC-B, providing additional evidence that particle size influenced the adsorption kinetics (results not shown).
3.5.
Comparison of microcystin and CYN adsorption
The similar adsorption trends for the microcystins and CYN by both PACs prompted an investigation in comparing the adsorption of both cyanotoxin classes. Prior to this study, no known attempt has been made to relate the PAC adsorption of the microcystins with that of CYN. This is partly due to a lack of studies investigating the PAC adsorption of CYN. Fig. 7 shows the percent removal of each of the cyanotoxins as a function of PAC-B dose for the 60 min contact time in Warragamba water. The results for Waikerie and Swan Reach
waters (using PAC-A) were similar (results not shown). CYN was shown to be removed similarly to MCRR. Coincidentally, both compounds have a net neutral charge between pH 6.0e8.5, compared with the other microcystin variants which have net negative charges (see Table 1). Furthermore, CYN is considered a hydrophilic compound (Froscio et al., 2009); likewise, MCRR is considered more hydrophilic than the other microcystins (Fastner et al., 1998). It is likely that there are other factors which contribute to the similarities in their adsorption, including, but not limited to, the molecular size and structural conformations of the compounds in solution. Studies have shown that some molecules may become smaller in solution due to electrostatic forces between neighbouring charged sites (Huang et al., 2007; Sathishkumar et al., 2010). This can reduce the overall molecular dimension which could favour adsorption. In addition, intramolecular hydrogen bonds may be formed during the reduction in molecular size, which could enhance adsorption. The presence of counterions and associated water molecules may also influence the size of molecules in solution and their subsequent adsorption (Wang and Morgner, 2010). Van der Bruggen et al. (1999) showed that the Stokes diameter was a parameter
w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 2 9 5 4 e2 9 6 4
crucial in achieving optimum cyanotoxin removal with differences observed between the two PACs tested for the removal of the cyanotoxins.
100 90
Warragamba CYN MCRR MCYR MCLR MCLA
80
Percent remaining
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70 60 50
Acknowledgements This project was financially supported by Sydney Water and United Utilities Australia. The assistance of Debra Owers is duly acknowledged.
40 30 20 10 0 0
20
40
60
80
100
Appendix. Supporting information
-1
PAC-B dose (mg L )
Fig. 7 e Comparison of the removal of cylindrospermopsin (CYN) and the microcystin variants MCRR, MCYR, MCLR and MCLA in Warragamba water using PAC-B at a contact time of 60 min.
which could be used to estimate the size of a molecule in solution. This is due to the Stokes diameter taking into account the water jacket surrounding the molecule which other size parameters preclude. According to the Stokes equation, the Stokes diameter is inversely proportional to the surface diffusion coefficient (Ds). The Ds for CYN and MCLR has been estimated to be w109 cm2 s1 and w1011 cm2 s1, respectively, from previous studies (Cook and Newcombe, 2008; Ho et al., 2008). Based on these values and the molecular weight of the toxins, CYN would be the smaller molecule in solution, lending support to its more favourable adsorption than MCLR. To date, no studies have determined the Ds for MCRR and hence a direct comparison could not be made with CYN. Nevertheless, the similar removal of CYN and MCRR is an interesting finding which has not been previously reported and suggests that there is potential in using MCRR as a surrogate for CYN adsorption, particularly when only microcystin analyses are being conducted on water samples.
4.
Summary and conclusions
With increasing global detection of CYN and microcystins in water supplies, it is imperative that effective treatment options are employed for the removal of such harmful cyanotoxins. This study provided insights into the effectiveness of PAC for the removal of CYN and microcystin variants, MCLR, MCRR, MCYR and MCLA. The results demonstrated that PAC could be an effective treatment option for the removal of the cyanotoxins from the studied waters under WTP conditions. No difference was observed in the removal of the cyanotoxins using contact times of 30, 45 and 60 min. Differences were observed in the PAC adsorption of the four microcystin variants which were consistent with previous findings. CYN was shown to adsorb to a similar extent to MCRR, a finding which has not been previously reported. Furthermore, this study suggested that selection of the most appropriate PAC is
Supplementary information associated with this article can be found, in the online version, at doi:10.1016/j.watres.2011.03.014.
references
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Falconer, I.T., 1989. Effects on human health of some toxic cyanobacteria (blue-green algae) in reservoirs, lakes, and rivers. Toxicity Assesment 4, 175e184. Falconer, I.R., Runnegar, M.T.C., Buckley, T., Huyn, Y.L., Bradshaw, P., 1989. Using activated carbon to remove toxicity from drinking water containing cyanobacterial blooms. Journal of the American Water Works Association 81, 102e105. Falconer, I.R., 2005. Cyanobacterial Toxins in Drinking Water Supplies: cylindrospermopsins and Microcystins. CRC Press, Boca Raton, Florida, USA. Fastner, J., Flieger, I., Neumann, U., 1998. Optimised extraction of microcystins from field samples - a comparison of different solvents and procedures. Water Research 32, 3177e3181. Froscio, S.M., Cannon, E., Lau, H.M., Humpage, A.R., 2009. Limited uptake of the cyanobacterial toxin cylindrospermopsin by vero cells. Toxicon 54, 862e868. Froscio, S.M., Humpage, A.R., Burcham, P.C., Falconer, I.R., 2001. Cell-free protein synthesis inhibition assay for the cyanobacterial toxin cylindrospermopsin. Environmental Toxicology 16, 408e412. Froscio, S.M., Humpage, A.R., Burcham, P.C., Falconer, I.R., 2003. Cylindrospermopsin-induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environmental Toxicology 18, 243e251. Himberg, K., Keijola, A.M., Hiisvirta, L., Pyysalo, H., Sivonen, K., 1989. The effect of water treatment processes on the removal of hepatotoxins from Microcystis and Oscillatoria cyanobacteria; a laboratory study. Water Research 23, 979e984. Ho, L., Newcombe, G., 2007. Evaluating the adsorption of microcystin toxins using granular activated carbon (GAC). Journal of Water Supply: Research and Technology - Aqua 56, 281e291. Ho, L., Slyman, N., Kaeding, U., Newcombe, G., 2008. Optimizing PAC and chlorination practices for cylindrospermopsin removal. Journal of the American Water Works Association 100, 88e96. Ho, L., Tanis-Plant, P., Kayal, N., Slyman, N., Newcombe, G., 2009. Optimising water treatment practices for the removal of Anabaena circinalis and its associated metabolites, geosmin and saxitoxins. Journal of Water and Health 7, 544e556. Huang, W.J., Cheng, B.L., Cheng, Y.L., 2007. Adsorption of microcystin-LR by three types of activated carbon. Journal of Hazardous Materials 141, 115e122. Kemp, A., John, J., 2006. Microcystins associated with Microcystis dominated blooms in the Southwest wetlands, Western Australia. Environmental Toxicology 21, 125e130. Li, Q., Snoeyink, V.L., Marinas, B.J., Campos, C., 2003. Pore blockage effect of NOM on atrazine adsorption kinetics of PAC: the roles of PAC pore size distribution and NOM molecular weight. Water Research 37, 4863e4872. Matsui, Y., Ando, N., Sasaki, H., Matsushita, T., Ohno, K., 2009. Branched pore kinetic model analysis of geosmin adsorption on super-powdered activated carbon. Water Research 42, 3095e3103. McGreggor, G.B., Fabbro, L.D., 2000. Dominance of Cylindrospermopsis raciborskii (Nostocales, Cyanoptokaryota) in Queensland tropical and subtropical reservoirs: implications for monitoring and management. Lakes and Reservoirs: Research and Management 5, 195e205. Metcalf, J.S., Beattie, K.A., Saker, M.L., Codd, G.A., 2002. Effects of organic solvents on the high performance liquid chromatographic analysis of the cyanobacterial toxin cylindrospermopsin and its recovery from environmental eutrophic waters by solid phase extraction. FEMS Microbiology Letters 216, 159e164. Mouchet, P., Bonne´lye, V., 1998. Solving algae problems: french expertise and world-wide applications. Journal of Water Supply: Research and Technology - Aqua 47, 125e141. Najm, I.N., Snoeyink, V.L., Suidan, M.T., Lee, C.H., Richard, Y., 1990. Effect of particle size and background natural organics
on the adsorption efficiency of PAC. Journal of the American Water Works Association 82, 65e72. Newcombe, G., 2002. Removal of Algal Toxins from Drinking Water Using Ozone and GAC. AwwaRF Report 90904. American Water Work Association, Denver, CO, USA. Newcombe, G., Drikas, M., Hayes, R., 1997. The influence of characterised natural organic material on activated carbon adsorption: II effect of on pore volume distribution and adsorption of MIB. Water Research 31, 1065e1073. Newcombe, G., Morrison, J., Hepplewhite, C., Knappe, D.R.U., 2002. Simultaneous adsorption of MIB and NOM onto activated carbon. II. competitive effects. Carbon 40, 2147e2156. Newcombe, G., Nicholson, B., 2004. Water treatment options for dissolved cyanotoxins. Journal of Water Supply: Research and Technology - Aqua 53, 227e239. Nicholson, B.C., Rositano, J., Burch, M.D., 1994. Destruction of cyanobacterial peptide hepatotoxins by chlorine and chloramines. Water Research 28, 1297e1303. Nishiwaki-Matsushima, R., Ohta, T., Nishiwaki, S., Suganuma, M., Kohyama, J., Ishikawa, T., Carmichael, W.W., Fujiki, H., 1992. Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. Journal of Cancer Research and Clinical Oncology 118, 420e424. Padisa´k, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding highly adaptive blue green algal species: worldwide distribution and review of its ecology. Archiv Fu¨r Hydrobiologie Supplementband 107, 563e593. Paerl, H.W., Huisman, J., 2008. Climate. Blooms like it hot. Science 320, 57e58. Pelekani, C., Snoeyink, V.L., 1999. Competitive adsorption in natural water: role of activated carbon pore size. Water Research 33, 1209e1219. Pendleton, P., Schumann, R., Wong, S.H., 2001. Microcystin adsorption by activated carbon. Journal of Colloid and Interface Science 240, 1e8. Rodriguez, E., Onstad, G.D., Kull, T.P.J., Metcalf, J.S., Acero, J.L., von Gunten, U., 2007. Oxidative elimination of cyanotoxins: comparison of ozone, chlorine, chlorine dioxide and permanganate. Water Research 41, 3381e3393. Sathishkumar, M., Pavagadhi, S., Vijayaraghavan, K., Balasubramanian, R., Ong, S.L., 2010. Experimental studies on removal of microcystin-LR by peat. Journal of Hazardous Materials 184, 417e424. Sontheimer, H., Crittenden, J., Summers, S., 1988. Activated Carbon for Water Treatment. DVGW-Forschungsstelle, EnglerBrunte-Institute, Germany. Stirling, D.J., Quilliam, M.A., 2001. First report on the cyanobacterial toxin cylindrospermopsin in New Zealand. Toxicon 39, 1219e1222. Traegner, U.K., Suidan, M.T., Kim, B.R., 1996. Considering age and size distributions of activated-carbon particles in a completely-mixed adsorber at steady state. Water Research 30, 1495e1501. Van der Bruggen, B., Schaep, J., Wilms, D., Vandecasteele, C., 1999. Influence of molecular size, polarity and charge on the retention of organic molecules by nanofiltration. Journal of Membrane Science 156, 29e41. Wang, C., Morgner, H., 2010. Effects of counterions on adsorption behavior of anionic surfactants on solution surface. Langmuir 26, 3121e3125. Westerhoff, P., Aiken, G., Amy, G., Debroux, J., 1999. Relationships between the structure of natural organic matter and its reactivity towards molecular ozone and hydroxyl radicals. Water Research 33, 2265e2276.
Available at www.sciencedirect.com
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Application of powdered activated carbon for the adsorption of cylindrospermopsin and microcystin toxins from drinking water supplies Lionel Ho a,b,*, Paul Lambling c, Heriberto Bustamante d, Phil Duker d, Gayle Newcombe a a
Australian Water Quality Centre, SA Water Corporation, 250 Victoria Square, Adelaide, SA 5000, Australia School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia c ´ Ecole Supe´rieure de Chimie Physique E´lectronique de Lyon, 43, Boulevard du 11 Novembre 1918, BP 2077, 69616 Villeurbanne Cedex, France d Sydney Water, PO Box 399, Parramatta NSW 2124, Australia b
article info
abstract
Article history:
Cylindrospermopsin (CYN) and microcystin are two potent toxins that can be produced by
Received 17 September 2010
cyanobacteria in drinking water supplies. This study investigated the application of
Received in revised form
powdered activated carbon (PAC) for the removal of these toxins under conditions that
8 March 2011
could be experienced in a water treatment plant. Two different PACs were evaluated for
Accepted 9 March 2011
their ability to remove CYN and four microcystin variants from various drinking water
Available online 17 March 2011
supplies. The removal of natural organic material by the PACs was also determined by measuring the levels of dissolved organic carbon and UV absorbance (at 254 nm). The PACs
Keywords:
effectively removed CYN and the microcystins from each of the waters studied, with one of
Adsorption
the PACs shown to be more effective, possibly due to its smaller particle diameter. No
Cylindrospermopsin (CYN)
difference in removal of the toxins was observed using PAC contact times of 30, 45 and
Microcystin
60 min. Furthermore, the effect of water quality on the removal of the toxins was minimal.
Natural organic material (NOM)
The microcystin variants were adsorbed in the order: MCRR > MCYR > MCLR > MCLA. CYN
Powdered activated carbon (PAC)
was found to be adsorbed similarly to MCRR. ª 2011 Elsevier Ltd. All rights reserved.
1.
Introduction
The microcystins and cylindrospermopsin (CYN) (see Fig. 1 for structures) are potent hepatotoxins produced by a number of species of freshwater cyanobacteria, of which Microcystis aeruginosa and Cylindrospermopsis raciborskii are two of the more commonly encountered. Consumption of waters containing these cyanobacterial toxins (cyanotoxins) can lead to serious health risk with events such as diarrhoea, nausea, vomiting and even death occurring (Falconer, 1989). The microcystins have also been implicated as promoters of liver tumours (Nishiwaki-Matsushima et al., 1992), while CYN has been
associated with serious tissue damage and cell necrosis in the liver, kidney and other organs (Falconer, 2005). In addition, studies have also suggested that CYN is carcinogenic, genotoxic and involved in the inhibition of protein synthesis (Froscio et al., 2001, 2003; Falconer, 2005). As a result of the concerns about the effect of microcystins, a guideline value of 1 mg L1 for microcystin-LR (MCLR) in drinking water has been issued by the World Health Organisation (WHO). Similarly, the Australian Drinking Water Guideline value for microcystin has been set at 1.3 mg L1 as MCLR toxicity equivalents. While no official guideline value currently exists for CYN, the WHO is in the midst of proposing
* Corresponding author. Australian Water Quality Centre, SA Water Corporation, 250 Victoria Square, Adelaide, SA 5000, Australia. Tel.: þ61 8 7424 2119; fax: þ61 8 7003 2119. E-mail address: [email protected] (L. Ho). 0043-1354/$ e see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2011.03.014
w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 2 9 5 4 e2 9 6 4
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Fig. 1 e Molecular structures of: (a) microcystin and (b) cylindrospermopsin. Note: The generic structure of microcystin-XY is shown with the corresponding variants presented in the accompanying table.
a 1 mg L1 level, due to concerns regarding the effect of CYN (Rodriguez et al., 2007). In Australia, CYN has predominantly been detected in more tropical and subtropical areas, in particular Queensland. A survey of 47 water sources by McGreggor and Fabbro (2000) detected CYN in 14 of those sources at an average concentration of 3.4 mg L1 with a maximum concentration of 20 mg L1 in subsurface samples. In contrast, considerably higher concentrations of microcystin have been detected in Australian water bodies, in the g L1 concentration range in some cases (Falconer, 2005; Kemp and John, 2006); however, unlike CYN a majority of the microcystins would be contained within the cell (Falconer, 2005). Conventional water treatment methods such as coagulation, flocculation, sedimentation and filtration are ineffective at removing dissolved (extracellular) cyanotoxins (Himberg et al., 1989; Mouchet and Bonne´lye, 1998; Chow et al., 1999; Newcombe and Nicholson, 2004). Treatment options which have had success in removing extracellular cyanotoxins include activated carbon (both powdered and granular), nanofiltration, ozonation and chlorination (provided a specific chlorination exposure level is applied, typically w30 mg min L1) (Mouchet and Bonne´lye, 1998; Newcombe and Nicholson, 2004; Dixon et al., 2010). Powdered activated carbon (PAC) is one of the major treatment barriers for the removal of extracellular
cyanotoxin in most Australian water treatment plants (WTPs) as it can be applied when required, which is generally advantageous for cyanotoxin control since cyanobacterial problems are of a transient, intermittent nature. PAC adsorption has been shown to be effective in many studies if the application is optimised (Donati et al., 1994; Cook and Newcombe, 2002, 2008; Newcombe and Nicholson, 2004; Ho et al., 2008; Campinas and Rosa, 2010a,b). While PAC is a widely used and accepted method of water treatment, there have been few studies undertaken into its effective use in removing cyanotoxins such as CYN and the microcystins under conditions that could be experienced in a WTP. Consequently, more in depth systematic studies are required to ascertain the effectiveness of PAC for the removal of these cyanotoxins under such conditions. Most of studies relating to the PAC adsorption of cyanotoxins have been conducted on the microcystins, in particular, MCLR (Falconer et al., 1989; Donati et al., 1994; Pendleton et al., 2001; Cook and Newcombe, 2002, 2008; Campinas and Rosa, 2010a,b). Many of these studies have suggested that coal- and wood-based carbons are the best for microcystin adsorption due to their large mesopore volume. Cook and Newcombe (2002) conducted PAC adsorption experiments on four variants of microcystin and showed differences in the adsorption of each variant with the ease of removal following the order: MCRR > MCYR > MCLR > MCLA. These results were confirmed
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w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 2 9 5 4 e2 9 6 4
using a range of PACs with different starting materials and activation methods. Cook and Newcombe (2002) attributed the differences to a combination of factors including the hydrophobicity of the variants and electrostatic interactions. Previous studies have also suggested that the PAC adsorption of cyanobacterial metabolites, such as the microcystins, may be significantly influenced by the size and conformation of the adsorbate (Donati et al., 1994; Pendleton et al., 2001; Cook and Newcombe, 2002; Sathishkumar et al., 2010). Moreover, Donati et al. (1994) and Pendleton et al. (2001) suggest that the size and conformation of the microcystin molecules, along with the pore volume characteristics of the carbon, appear to be the dominant mechanism for microcystin adsorption, with minimal influences from electrostatic interactions due to the hydrophobic nature of the microcystin molecule and low number of ionisable functional groups. Another factor which can influence the adsorption of cyanobacterial metabolites is the presence of natural organic material (NOM), in particular, the concentration and character of NOM (Donati et al., 1994; Newcombe et al., 1997, 2002; Cook and Newcombe, 2008). These studies have shown that NOM can simultaneously compete with the cyanobacterial metabolites for adsorption sites on the surface of the activated carbon, thereby reducing the adsorption efficiency of the cyanobacterial metabolites. To date, only one study has been published in the peerreviewed literature with respect to the evaluation of PAC for the removal of CYN (Ho et al., 2008). However, no studies have been conducted relating the PAC adsorption of a combination of cyanotoxins, such as the microcystins and CYN. This is important since the onset of climate change is predicted to increase both the occurrence and intensity of cyanobacterial blooms (Paerl and Huisman, 2008). Coupled with warmer water temperatures and invading blooms of CYN-producing cyanobacteria (Chapman and Schelske, 1997; Padisa´k, 1997; Stirling and Quilliam, 2001), there is a greater likelihood that multiple cyanotoxins will be present in drinking water supplies. Consequently, knowledge pertaining to the parallel removal of a range of cyanotoxins by PAC will enable water authorities to have plans to mitigate issues caused by these cyanotoxins, including selection of the most appropriate PAC. The major aim of this study was to investigate the PAC adsorption of extracellular cyanotoxins, in particular, CYN and four microcystin variants, MCLR, MCLA, MCYR and MCRR. Two different PACs were evaluated in various Australian drinking water supplies under conditions that would be experienced in a WTP. The adsorption of NOM was also examined, with respect to its impact on the adsorption of the cyanotoxins. A final aim was to relate the adsorption of CYN with that of the microcystins under equivalent conditions.
2.
Experimental procedures
2.1.
Materials and reagents
Experiments were conducted using purified CYN (95% pure) isolated from a laboratory culture of C. raciborskii (Palm Island, Queensland, CYP020). The toxin was dissolved in ultrapure water (Millipore Pty Ltd, USA) and stored at 20 C prior to use.
Purified (95% pure) microcystin variants, MCLA, MCYR, MCRR and MCLR were purchased from a commercial supplier (Sapphire Bioscience, Australia). Stock solutions of each of the microcystin variants were prepared in 50% methanol and stored at 20 C prior to use. Aliquots were taken from the dissolved stock solution and dosed into experiments at specified concentrations. Table 1 lists some of the characteristics of the cyanotoxins. Unfiltered raw water obtained from the inlet of three WTPs was stored at 4 C until used. Warragamba Dam water (dissolved organic carbon (DOC) ¼ 5.0 mg L1, UV absorbance at 254 nm (UV254) ¼ 0.093 cm1, pH ¼ 7.5) was supplied by Sydney Water in New South Wales. Waikerie (DOC ¼ 4.3 mg L1, UV254 ¼ 0.076 cm1, pH ¼ 7.7) and Swan Reach (DOC ¼ 3.9 mg L1, UV254 ¼ 0.072 cm1, pH ¼ 7.6) waters were supplied by United Utilities Australia in South Australia. Waikerie and Swan Reach WTPs are situated along the River Murray in South Australia with Swan Reach WTP (coordinates 34 340 0400 S 139 350 5900 E) downstream of Waikerie WTP (coordinates 34 100 6000 S 139 580 6000 E). Warragamba Dam (coordinates 33 530 0000 S 150 350 4400 E) is located approximately 65 km west of Sydney in New South Wales. Historically, only very low concentrations of CYN and the microcystins have been detected in the three water sources, in most cases the toxins have been undetectable in these waters; however, high concentrations of cyanobacterial species known to produce these toxins have been detected in these waters. Two commercially available PACs were used in this study. PAC-A was obtained from the Waikerie WTP where it is used to mitigate cyanobacterial metabolites; this PAC is also routinely used at the Swan Reach WTP. PAC-B was supplied from Sydney Water and used at WTPs which source water from Warragamba Dam. Some general characteristics of the PACs are listed in Table S1 of the Supporting Information. The PACs were dried in an oven at 110 C for 24 h, then cooled and stored in a desiccator prior to use. For adsorption experiments, PAC slurries were prepared by mixing the required carbon dose with 5 mL of ultrapure water.
2.2.
PAC adsorption experiments
All PAC jar tests were conducted at room temperature (25 C). An FMS6V (SEM, Australia) variable speed, six paddle gang stirrer with 7.6 cm diameter flat paddle impellers and B-Ker2 gator jars (Phipps and Bird, USA) containing 1 L of sample waters was used. PAC doses of 5, 10, 25, 50 and 100 mg L1
Table 1 e Characteristics of the cyanotoxins used in this study. Cyanotoxin
Cylindrospermopsin Microcystin RR YR LR LA
Molecular LD50 (ug kg1 Charge at body weight) pH 6.0e8.5 weight (g mol1) 415.43 1038.20 1045.19 995.17 910.06
2100 600 70 50 50
0 (þ & ) 0 ( & þþ) 1 ( & þ) 1 ( & þ) 2 ()
w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 2 9 5 4 e2 9 6 4
were employed as this range represents low to high doses that can be applied at the respective WTPs (Ho et al., 2009). The cyanotoxins were spiked into the waters (20 mg L1 of CYN and 4 mg L1 each of MCRR, MCYR and MCLA, and 10 mg L1 of MCLR) and constantly stirred at 100 rpm throughout the experiment to ensure PAC remained suspended in solution. PAC slurries were added at time zero and experimental samples were taken at three time intervals; 30, 45 and 60 min. Samples were collected and immediately filtered through prerinsed 0.45 mm cellulose nitrate filters (Schleicher and Schuell, Germany) prior to analysis. Any losses of the cyanotoxins other than PAC adsorption were accounted for by jar test experiments performed in the absence of PAC. Microcystin adsorption experiments were conducted where all variants were spiked into the same experiments, while CYN adsorption experiments were conducted separately. Cook and Newcombe (2008) previously showed no competitive adsorption between the microcystin variants.
2.3.
Analyses
Prior to high performance liquid chromatographic (HPLC) analysis, the cyanotoxins were concentrated from the sample waters by solid phase extraction using methods described previously by Metcalf et al. (2002) and Nicholson et al. (1994) for CYN and the microcystins, respectively. An Agilent 1100 series HPLC system comprising of a quaternary pump, autosampler and photodiode array detector (Agilent Technologies, Australia) was employed for the analysis of the cyanotoxins. For CYN analysis, sample volumes of 25 mL were injected into a 150 4.6 mm Apollo C8 column (Alltech, Australia) at a flow rate of 0.6 mL min1 (column temperature 30 C). Two mobile phases (mobile phase A: 0.5% formic acid and mobile phase B: 100% acetonitrile) were used during the gradient run (0 min, 100% A; 25 min, 90% A, 10% B; 25.01 min, 70% A, 30% B, 30.01 min, 100% A, 55 min, 100% A). CYN concentrations were determined by calibrating the peak areas with that of a certified reference standard (Institute of Marine Biosciences, National Research Council, Canada). The method has a detection limit of 0.5 mg L1. For microcystin analysis the volume of sample injected into the 150 4.6 mm Luna C18 column (Phenomenex, Australia) was 25 mL at a flow rate of 1.0 mL min1 (column temperature 30 C). Two mobile phases (mobile phase A: 30% acetonitrile and mobile phase B: 55% acetonitrile) were used during the gradient run (0 min, 100% A; 12.5 min, 50% A, 50% B; 15 min, 100% B; 23 min 100% A; 32 min, 100% A). Microcystin concentrations were determined by calibrating the peak areas with that of certified reference standards (Sapphire Bioscience Pty Ltd, Australia). The method has a detection limit of 0.1 mg L1. DOC measurements were made on an 820 Total Organic Carbon Analyser (Sievers Instruments Inc, USA). UV254 measurements were carried out on a UV-1201 UV/VIS Spectrophotometer (Shimadzu Corporation, Japan). Molecular weight distributions of the waters were determined using high performance size exclusion chromatography (HPSEC) according to the method of Chow et al. (2008). Briefly, the HPSEC method utilised a 2690 separation module and 996 photodiode array detector operating at 260 nm (Waters Pty Ltd, Australia). Separation was performed with a Shodex KW 802.5 column
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(Shoko Co. Ltd, Japan) and a 0.1 M phosphate buffer solution (pH 6.8, ionic strength adjusted to 1.0 M with sodium chloride). An injection volume of 100 mL was used at a flow rate of 1 mL min1. The column had an effective resolving range of 50e50,000 Da and the retention time was calibrated for apparent molecular weight using polystyrene sulphonate standards (Polysciences Inc, USA) of molecular weights 35,000, 18,000, 8000, and 4600 Da.
3.
Results and discussion
3.1.
Adsorption of NOM
The concentration and character of NOM can affect the adsorption of cyanobacterial metabolites through competitive adsorption mechanisms (Donati et al., 1994; Newcombe et al., 1997, 2002; Cook and Newcombe, 2008). In particular, it is believed that the greatest adsorption competition would exist between compounds of similar size and shape (Newcombe et al., 1997, 2002). However, competitive adsorption is not only dependent upon the size of the competing compound, but also highly dependent upon the pore volume distribution of the adsorbent (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Li et al., 2003; Ho et al., 2009). In addition, previous studies have shown that solution and surface chemistry (eg. pH and PAC surface charge) have minimal influence on the adsorption of cyanobacterial metabolites (Pendleton et al., 2001; Cook and Newcombe, 2002, 2008). The initial DOC and UV254 values of Swan Reach and Waikerie WTP inlet waters were similar, attributed to the fact that both WTPs source water from the River Murray in South Australia. In contrast, Warragamba Dam water, which is sourced from New South Wales, contained NOM of higher DOC and UV254 values. Fig. 2 shows the removal of DOC and UV254 by the PACs after a contact time of 60 min. Negligible difference was observed for the removals of DOC in each of the waters (Fig. 2a), while some differences were observed for the removal of UV254 (Fig. 2b). PAC-B in Warragamba water removed more UV absorbing compounds than PAC-A in the South Australian waters, with the differences increasing with PAC dose. For example, at a PAC dose of 10 mg L1 the difference was 5%, while for a dose of 100 mg L1 the difference was 14%. It is unclear as to whether these differences were attributed to differences between the PACs or the waters, although it is likely to be a combination of both. The higher PAC doses employed (50 and 100 mg L1) are generally not achievable at most conventional WTPs due to PAC carryover affecting downstream processes, including filtration. Such high PAC doses would dramatically reduce the filter run times in direct/contact filtration causing reductions in water production. However, at the Swan Reach and Waikerie WTPs, these high PAC doses can be applied due to the construction of large contact tanks prior to coagulation to facilitate removal of cyanobacterial metabolites. These high doses resulted in excellent removal of DOC and UV254 of between 60 and 74%. Fig. 3a shows the molecular weight distributions (using HPSEC with UV absorbance as the detection method) of the organics in the three waters. The waters exhibited similar
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PAC dose (mg L ) Fig. 2 e Removal of: (a) dissolved organic carbon (DOC) and (b) UV absorbance at 254 nm (UV254) by the PACs in the waters evaluated after a contact time of 60 min. Error bars represent 95% confidence intervals from duplicate analyses.
profiles although Warragamba water displayed higher UV absorbance than Swan Reach and Waikerie waters across the wavelengths, in particular between 800 and 1200 Da, consistent with Warragamba water’s higher UV254. Previous studies have suggested that the NOM within this region is humic in nature and contains compounds which are highly aromatic and/or contain a higher degree of conjugation (Westerhoff et al., 1999; Newcombe et al., 2002; Chow et al., 2008). Furthermore, Chow et al. (2008) have indicated that NOM in this molecular weight region are hydrophobic and more easily removed by conventional water treatment processes.
The PACs removed a wide range of molecular weight compounds with removal increasing with PAC dose (Fig. 3bed). It is presumed that the removal of the wide range of molecular weight compounds by PAC is attributed to the pore structure of the PACs (Newcombe, 2002). More importantly, the removal of the wide range of molecular weights, suggest that the character of NOM may not have a significant influence in the adsorption of the cyanotoxins when using these PACs, which may be attributed to the PACs containing a broad pore size distribution (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Li et al., 2003; Ho et al., 2009). This will be discussed further in subsequent sections of this manuscript.
w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 2 9 5 4 e2 9 6 4
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Fig. 3 e Molecular weight distributions of: (a) Swan Reach, Waikerie and Warragamba waters; (b) Swan Reach water after treatment with sequential doses of PAC-A; (c) Waikerie water after treatment with sequential doses of PAC-A; (d) Warragamba water after treatment with sequential doses of PAC-B. In each case, PAC contact time was 60 min.
3.2.
Adsorption of microcystin
Four microcystin variants were studied for the PAC adsorption experiments, MCLR, MCYR, MCRR and MCLA. Whilst a majority of studies have focused on MCLR, as it is one of the most toxic variants, it is important to study other variants as most microcystin-producing blooms generally yield others, and in many cases MCLR is not always the most abundant. The water was spiked with 22 mg L1 total microcystin; consisting 4 mg L1 each of MCRR, MCYR and MCLA, and 10 mg L1 MCLR. These concentrations were chosen as they represent an upper limit or worst case scenario of what could be expected to enter a WTP (Falconer, 2005). Fig. 4a and b show the removal of total microcystins by the PACs in Waikerie and Warragamba waters, respectively. The removal trends for Swan Reach (results not shown) were identical to Waikerie water. The increased contact times did not appear to enhance microcystin adsorption using both PACs in their respective waters as negligible difference was observed using contact times of 30, 45 and 60 min. This suggests that the kinetics of adsorption for both PACs were rapid. The addition of PAC-B in Warragamba water yielded the
highest removal of the microcystins where a PAC dose of 50 mg L1 resulted in removals to below the WHO guideline level of 1 mg L1. In contrast, Waikerie and Swan Reach waters required a PAC-A dose of 100 mg L1 to achieve the same level of microcystin removal. Realistically, a WTP may expect to treat total microcystin concentrations of between 2 and 5 mg L1 and possibly up to 10 mg L1. In these scenarios the predicted PAC doses required to achieve the WHO guideline level in Warragamba water would be 5, 11 and 23 mg L1, respectively. In Waikerie and Swan Reach waters, the corresponding predicted PAC doses would be 9, 23 and 45 mg L1. These predictions were made using the homogenous surface diffusion model (HSDM) and are based on the assumption that the amount of microcystin adsorbed is directly proportional to its initial concentration. Previous studies have shown that the percent removal of microcystin at equilibrium for a given carbon dose in natural water is independent of the cyanotoxin’s initial concentration (Cook and Newcombe, 2002; Ho and Newcombe, 2007). The more favourable adsorption of the microcystins in Warragamba water compared with Waikerie and Swan Reach waters is consistent with the UV254 results where greater
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Fig. 4 e Removal of total microcystins (22 mg LL1) by PAC in: (a) Waikerie water; and (b) Warragamba water. Differences in the PAC adsorption of the microcystin variants after a contact time of 30 min in: (c) Waikerie water; and (d) Warragamba water.
removal was also observed in this PAC-water combination (Fig. 2b). The reasons for this will be discussed later. The trends for removal of each of the four microcystin variants in Waikerie and Warragamba waters after a PAC contact time of 30 min are shown in Fig. 4 c and d In both waters using the respective PACs, the order of the ease of removal of the microcystin variants followed the trend: MCRR > MCYR > MCLR > MCLA, which is consistent with previous studies (Cook and Newcombe, 2002, 2008). The overall charges for the four variants are shown in Table 1. The negative groups are attributed to the dissociated carboxyl groups of D-glutamic acid and D-erythro-b-methyl aspartic acid and the positive charges to the amino group on arginine. It is these differences that may result in the different adsorption characteristic being observed. Attractive or repulsive forces between the cyanotoxin molecule and the activated carbon surface could either enhance or hinder adsorption. Molecular size and conformation of the microcystin molecules may also affect the interaction that the cyanotoxin has with the PAC surface, with smaller conformations favouring adsorption. The observed trend shows that MCRR has the greatest affinity with both PACs and MCLA, the least. Therefore, for effective PAC use in removing microcystins, it is important that all
microcystin variants present are identified due to the differences in their adsorption behaviour.
3.3.
Adsorption of CYN
The adsorption of CYN was also evaluated where CYN was spiked into the waters at a concentration of 20 mg L1; a concentration thought to represent a worst case scenario for a WTP (Falconer, 2005). Swan Reach showed identical trends to Waikerie as observed with the microcystin adsorption experiments (results not shown). Warragamba water, dosed with PAC-B, had higher CYN removal than Waikerie and Swan Reach waters with PAC-A, similar to the microcystin results (see Fig. S1 of the Supporting Information). PAC contact time again did not appear to have significant impact on the removal. The results show that PAC doses required for CYN removal to below the proposed WHO guideline value of 1 mg L1 are 25 mg L1 for Warragamba water and 50 mg L1 for Waikerie and Swan Reach waters. To date, limited studies have been undertaken with respect to the PAC adsorption of CYN under WTP conditions. Ho et al. (2008) used the HSDM to predict the adsorption of CYN using
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two PACs in Hope Valley reservoir water. They determined that PAC could be effective for the removal of CYN, although relatively high doses would be required. For example, at an initial CYN concentration of 5 mg L1, the PAC dose required to remove CYN to below 1 mg L1 would be 25 mg L1 (using a contact time of 60 min). However, in that study the DOC and UV254 of Hope Valley water was appreciably higher at 10.2 mg L1 and 0.325 cm1, respectively. These NOM characteristics have been shown to influence the adsorption of cyanobacterial metabolites through competitive adsorption processes and/or pore blockage mechanisms (Cook et al., 2001; Newcombe et al., 1997).
3.4.
Fig. 5a and b show results of the removal of total microcystins and CYN in Waikerie water using both PACs (after a contact time of 30 min), while Fig. 5c and d show the same but in Warragamba water. In all cases, PAC-B was the superior carbon for the adsorption of all the cyanotoxins with large differences observed between both PACs. In contrast, Fig. 6aed directly compare the removals of microcystin and CYN between the waters using both PACs after a contact time of 30 min. The differences between the waters in Fig. 6 were not as pronounced as those observed between the PACs in Fig. 5aed, suggesting that the PACs used had a wide range of pores which could offset the influence of water quality, in particular the presence of NOM (Pelekani and Snoeyink, 1999; Ebie et al., 2001; Newcombe et al., 2002; Li et al., 2003). This finding also strongly suggests that the PAC type was the major factor influencing cyanotoxin adsorption. The most disparate characteristic between the PACs was the effective particle size, 20e25 mm for PAC-A, and 10 mm for PAC-B. Previous studies have shown that the equilibrium adsorption of a microcontaminant is not affected by particle size (Matsu et al., 2009; Ando et al., 2010); however, the particle size can influence the adsorption kinetics, with more rapid adsorption with smaller
Differences in PAC and water quality characteristics
Further investigations were warranted to determine why the combination of PAC-B and Warragamba water was superior for the adsorption of the cyanotoxins (see Fig. 4 and Fig. S1 of the Supporting Information). It was unclear whether this was due to the differences between the PACs or the waters or a combination of both. Experiments were conducted where PAC-B was evaluated in Waikerie water and PAC-A in Warragamba water, and then compared with the original PAC-water combinations.
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Fig. 5 e Comparison in the removal of: (a) total microcystins; and (b) cylindrospermopsin (CYN) in Waikerie water by PAC-A and PAC-B after a contact time of 30 min. Comparison in the removal of: (c) total microcystins; and (d) CYN in Warragamba water by PAC-A and PAC-B after a contact time of 30 min.
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Fig. 6 e Comparison in the removal of total microcystins in Waikerie and Warragamba water using: (a) PAC-A; and (b) PAC-B after a contact time of 30 min. Comparison in the removal of cylindrospermopsin (CYN) in Waikerie and Warragamba water using: (c) PAC-A; and (d) PAC-B after a contact time of 30 min.
particle size (Sontheimer et al., 1988; Najm et al., 1990; Traegner et al., 1996). The results in this study confirm this contention as although PAC-B was the superior carbon at 30 min contact time (Fig. 5), the removals of all cyanotoxins by both PACs was similar at equilibrium (contact time of 3 d, results not shown). Furthermore, negligible difference in the removal of the cyanotoxins was observed between the PACs when PAC-A was ground down to the same particle size as PAC-B, providing additional evidence that particle size influenced the adsorption kinetics (results not shown).
3.5.
Comparison of microcystin and CYN adsorption
The similar adsorption trends for the microcystins and CYN by both PACs prompted an investigation in comparing the adsorption of both cyanotoxin classes. Prior to this study, no known attempt has been made to relate the PAC adsorption of the microcystins with that of CYN. This is partly due to a lack of studies investigating the PAC adsorption of CYN. Fig. 7 shows the percent removal of each of the cyanotoxins as a function of PAC-B dose for the 60 min contact time in Warragamba water. The results for Waikerie and Swan Reach
waters (using PAC-A) were similar (results not shown). CYN was shown to be removed similarly to MCRR. Coincidentally, both compounds have a net neutral charge between pH 6.0e8.5, compared with the other microcystin variants which have net negative charges (see Table 1). Furthermore, CYN is considered a hydrophilic compound (Froscio et al., 2009); likewise, MCRR is considered more hydrophilic than the other microcystins (Fastner et al., 1998). It is likely that there are other factors which contribute to the similarities in their adsorption, including, but not limited to, the molecular size and structural conformations of the compounds in solution. Studies have shown that some molecules may become smaller in solution due to electrostatic forces between neighbouring charged sites (Huang et al., 2007; Sathishkumar et al., 2010). This can reduce the overall molecular dimension which could favour adsorption. In addition, intramolecular hydrogen bonds may be formed during the reduction in molecular size, which could enhance adsorption. The presence of counterions and associated water molecules may also influence the size of molecules in solution and their subsequent adsorption (Wang and Morgner, 2010). Van der Bruggen et al. (1999) showed that the Stokes diameter was a parameter
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crucial in achieving optimum cyanotoxin removal with differences observed between the two PACs tested for the removal of the cyanotoxins.
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Acknowledgements This project was financially supported by Sydney Water and United Utilities Australia. The assistance of Debra Owers is duly acknowledged.
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Appendix. Supporting information
-1
PAC-B dose (mg L )
Fig. 7 e Comparison of the removal of cylindrospermopsin (CYN) and the microcystin variants MCRR, MCYR, MCLR and MCLA in Warragamba water using PAC-B at a contact time of 60 min.
which could be used to estimate the size of a molecule in solution. This is due to the Stokes diameter taking into account the water jacket surrounding the molecule which other size parameters preclude. According to the Stokes equation, the Stokes diameter is inversely proportional to the surface diffusion coefficient (Ds). The Ds for CYN and MCLR has been estimated to be w109 cm2 s1 and w1011 cm2 s1, respectively, from previous studies (Cook and Newcombe, 2008; Ho et al., 2008). Based on these values and the molecular weight of the toxins, CYN would be the smaller molecule in solution, lending support to its more favourable adsorption than MCLR. To date, no studies have determined the Ds for MCRR and hence a direct comparison could not be made with CYN. Nevertheless, the similar removal of CYN and MCRR is an interesting finding which has not been previously reported and suggests that there is potential in using MCRR as a surrogate for CYN adsorption, particularly when only microcystin analyses are being conducted on water samples.
4.
Summary and conclusions
With increasing global detection of CYN and microcystins in water supplies, it is imperative that effective treatment options are employed for the removal of such harmful cyanotoxins. This study provided insights into the effectiveness of PAC for the removal of CYN and microcystin variants, MCLR, MCRR, MCYR and MCLA. The results demonstrated that PAC could be an effective treatment option for the removal of the cyanotoxins from the studied waters under WTP conditions. No difference was observed in the removal of the cyanotoxins using contact times of 30, 45 and 60 min. Differences were observed in the PAC adsorption of the four microcystin variants which were consistent with previous findings. CYN was shown to adsorb to a similar extent to MCRR, a finding which has not been previously reported. Furthermore, this study suggested that selection of the most appropriate PAC is
Supplementary information associated with this article can be found, in the online version, at doi:10.1016/j.watres.2011.03.014.
references
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