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Enhanced transformation of sulfonamide antibiotics by manganese(IV) oxide in the presence of model humic constituents
Water Research 153 (2019) 200e207
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Enhanced transformation of sulfonamide antibiotics by manganese(IV) oxide in the presence of model humic constituents Yang Song a, c, Jin Jiang b, ** , Jun Ma e, Yang Zhou e, Urs von Gunten c, d, * a Key Laboratory for Water Quality and Conservation of the Pearl River Delta, Ministry of Education, Institute of Environmental Research at Greater Bay, Guangzhou University, Guangzhou, 510006, China b Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, Guangdong, 510006, China c School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique F ed erale de Lausanne (EPFL), CH-1015, Lausanne, Switzerland d Eawag, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, CH-8600, Düebendorf, Switzerland e State Key Laboratory of Urban Water Resource and Environment, School of Municipal and Environmental Engineering, Harbin Institute of Technology, Harbin, 150090, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 November 2018 Received in revised form 8 January 2019 Accepted 10 January 2019 Available online 21 January 2019
In this study, a manganese(IV) oxide-mediator (MnO2-mediator) system for the abatement of sulfonamide antibiotics was evaluated. Two simple model humic constituents, syringaldehyde (SA) and acetosyringone (AS), could promote the transformation of sulfonamides at pH 5e8. Two additional potential mediators, tannic acid and 2,20 -azino-bis(3-ethylbenzothiazoline)-6-sulfonate (ABTS), had negligible enhancement on the transformation of sulfonamides by MnO2. The enhancing effect was attributed to the reaction of the oxidized mediator (i.e., phenoxy radical or benzoquinone-like compounds) produced from the oxidation of the mediators by MnO2 with SMX. Thereby cross-coupling products from sulfamethoxazole (SMX) with oxidized SA were formed in the MnO2-SA system, which was confirmed by liquid chromatography/electrospray ionization-triple quadrupole mass spectrometry. Coexisting metal ions (i.e., Ca(II), Mg(II) and Mn(II)) showed inhibitory effects in the order of Mn(II)> Ca(II)> Mg(II). For repetitive runs of the MnO2-SA-SMX system, MnO2 lost its oxidative capacity due to the sorption of Mn(II) on the reactive sites of the MnO2 surface. A full regeneration of partially deactivated MnO2 by oxidation of the sorbed Mn(II) with Mn(VII) could be achieved. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Manganese oxide (MnO2) Sulfonamide antibiotics Mediators Cross-coupling Metal ions Regeneration
1. Introduction Sulfonamide antibiotics consisting of synthetic sulfanilamide derivatives are widely used in both human medicine and livestock production (Mellon et al., 2001). They include compounds such as sulfamethoxazole, sulfacetamide, sulfadoxine, sulfadiazine, sulfamethizole, sulfasalazine, sulfanilamide, and sulfisoxazole (Mellon et al., 2001; Garoma et al., 2010). The antibiotic effect is based on (i) a delay of the regeneration of bacterial cells, and (ii) prevention of cell growth via inhibition of the formation of folic acid (Craig and
* Corresponding author. School of Architecture, Civil and Environmental Engi de rale de Lausanne (EPFL), CH-1015, Launeering (ENAC), Ecole Polytechnique Fe sanne, Switzerland. ** Corresponding author. Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, Guangdong, 510006, China. E-mail addresses: [email protected] (J. Jiang), [email protected] (U. von Gunten). https://doi.org/10.1016/j.watres.2019.01.011 0043-1354/© 2019 Elsevier Ltd. All rights reserved.
Stitzel, 2004). Sulfonamide antibiotics have already been identified in soils and aquatic environments where they are emitted via several pathways (Kümmerer, 2003; Miao et al., 2004). Treating fields with manure from treated animals is a major pathway of sulfonamide antibiotics entering soils (Kümmerer, 2003). Sulfonamides in soils are introduced into groundwater or surface water via infiltration or runoff, respectively. In addition, sulfonamides from domestic and hospital applications are discharged into municipal wastewater (Gao and Pedersen, 2005). It has been reported previously that sulfonamides are not readily biodegradable (Ingerslev and Halling Sørensen, 2000), hence chemical oxidation processes, such as ozonation (Huber et al., 2005), chlorination (Dodd and Huang, 2004), and chloramination (Chamberlain and Adams, 2006) are promising for the transformation of sulfonamides. Furthermore, it has been demonstrated that the relative antimicrobial potency of sulfamethoxazole decreases proportionally with its relative residual concentration for oxidation with ozone and hydroxyl radical (Dodd et al., 2009). This demonstrates
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that oxidation processes are promising options for the treatment of this class of antibiotics. Manganese oxides (MnO2) are abundant natural oxidants in sediments and soils, and can affect the transformation of organic pollutants through direct oxidation, adsorption, and surface catalysis (Stone, 1987; Wang et al., 1999). Recently, MnO2 has been suggested as a passive barrier against micropollutants during recharge of stormwaters (Grebel et al., 2016; Charbonnet et al., 2018). It is well documented that MnO2 can oxidize phenols and anilines (Stone, 1987; Laha and Luthy, 1990; Ukrainczyk and McBride, 1993). Furthermore, it has been shown that various types of antimicrobial agents, such as fluoroquinolone, tetracyclines, and phenols can be transformed by MnO2 (Zhang and Huang, 2005; Zhang et al., 2008; Forrez et al., 2011). The following general reaction mechanism has been proposed: (i) Precursor complex formation on the MnO2 surface, (ii) electron transfer from the target compound to MnO2, and (iii) release of the reaction products including the organic transformation products and partially Mn(II) (Zhang and Huang, 2005; Zhang et al., 2008). A previous study (Gao et al., 2012) reported that a transformation of sulfamethazine (SMZ) by MnO2 occurred at acidic pH (4, 5, and 5.6), while no transformation was observed at higher pH (i.e., pH 6.3 and 7.6), due to the decreasing reduction potential of MnO2 (depending on the reactive surface sites on the MnO2 surface) with increasing pH (Zhang et al., 2008). Therefore, strategies for an enhanced transformation of sulfonamides by MnO2 over a wide pH range need to be developed. In a previous study, it has been demonstrated that the transformation of chloroanilines by birnessite was considerably enhanced by adding phenolic humic constituents at pH 5.6. Phenolic humic constituents in natural organic matter are ubiquitous in the aquatic environment containing numerous moieties, such as syringaldehyde, acetosyringone, ferulic acid, and protocatechuic acid (Park et al., 1999). The mechanism of the mediated transformation of chloroanilines involves two stages, (i) free radicals (including phenoxy and aniline radicals) are produced from the oxidation of the phenolic humic constituents and the target compounds (i.e., chloroanilines), respectively by MnO2. (ii) Cross-coupling reactions including radical-radical coupling between different oxidation products or nucleophilic addition to aromatic amines occur, resulting in the formation of quinones, dimers, and polymeric oxidation products (Stone, 1987; Dec et al., 2001; Wang et al., 2002; Thorn and Kennedy, 2002). Similarly, an enhanced transformation of sulfonamides by laccase in the presence of several mediators such as syringaldehyde (SA), acetosyringone (AS), and 2,2-azinobis(3-ethylbenzothiazoline)-6-sulfonic acid diammonium (ABTS) with the formation of cross-coupling products from the free radicals and amine moieties has been reported (Margot et al., 2015), and the toxicity of product mixtures was found to be lower than for untreated sulfonamides (Margot et al., 2015). Based on this information, the present study examines the feasibility of model humic constituents (i.e., SA, AS, tannic acid), or synthetic electron shuttles (i.e., ABTS) to enhance the transformation of SMX, which is normally not abated by MnO2 in MnO2mediator systems. SA, AS and tannic acid were selected as natural mediators, which were classified as common natural organic matter constituents in aquatic environments (Park et al., 1999). ABTS was the most commonly used synthetic electron shuttle, which can be oxidized forming the ABTS radical (Song et al., 2015). The potential of MnO2-mediated transformations of other selected sulfonamides including SMZ, sulfamethizole (SMZO), sulfathiazole (STZ), sulfapyridine (SPD), and sulfadiazine (SDZ) was also investigated. Transformation products of SMX in the MnO2-SA system were identified, and a reaction mechanism is proposed. Furthermore, influencing factors such as mediator concentrations, pH, and
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metal ions (e.g., Ca(II), Mg(II), and Mn(II)) on SMX transformation in MnO2-mediator systems were investigated. Since permanganate (Mn(VII)) reacts rapidly with Mn(II) (Van Benschoten et al., 1992; Song et al., 2017), Mn(VII) was tested as a regeneration agent to recover the oxidizing capacity of MnO2 in this study. Finally, the potential of the application of MnO2-mediator systems for the treatment of sulfonamides in a wastewater effluent was assessed. 2. Experimental methods 2.1. Chemicals and reagents All chemicals were analytical grade or higher quality and obtained from commercial suppliers (see Text S1 for details). The abbreviations, structures, and pKa values (Lucida et al., 2000; Camarero et al., 2005; Babi c et al., 2007) of the sulfonamides and humic constituents are presented in Table 1. All stock solutions were prepared with ultrapurified water (18.2 MU cm) obtained from a Millipore Milli-Q water purification system. A wastewater effluent sample was obtained from the nitrified Eawag pilot plant in Dübendorf (EPPWW), Switzerland (DOC ¼ 7.6 mg C/L, [Ca(II)] ¼ 2.58 mM, [Mg(II)] ¼ 0.79 mM, [Mn(II)] ¼ 0.14 mM, carbonate alkalinity ¼ 5.99 mM, and pH ¼ 7.8). After filtering through a nylon membrane with a pore size of 0.45 mm (Membrane Solutions), the samples were buffered to pH 7 with borate buffer (10 mM) and stored at 4 C. 2.2. MnO2 preparation MnO2 was prepared by the method of Murray (1974) by the stoichiometric reaction between potassium permanganate (Mn(VII)) and manganese(II) chloride (MnCl2). The permanganate stock solution (ca. 0.24 M) in ultrapurified water was diluted and then standardized spectrophotometrically by measuring the absorbance at 525 nm (ε ¼ 2500 M1 cm1) (Song et al., 2015). To synthesize MnO2 suspensions, permanganate and sodium hydroxide (NaOH) were added to nitrogen purged ultrapurified water, followed by a dropwise addition of a solution of MnCl2 under constant stirring. The formed MnO2 was settled and the supernatant was replaced with ultrapurified water several times until the conductivity of the supernatant was less than 2 mS/cm. The MnO2 suspensions were characterized by determination of the total manganese concentration after dissolution by ascorbic acid by (i) an inductively coupled plasma optical emission spectrometer (ICPOES) and (ii) the 2,2-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid diammonium (ABTS) spectrophotometric method (Jiang et al., 2012). The MnO2 suspensions were stored in the dark at 4 C until use within a week. 2.3. Reaction kinetics All the experiments were performed for pH values of 5, 6, 7, and 8 at 25 ± 1 C. Sodium acetate and sodium borate buffers (10 mM) were used for pH 5, 6 and pH 7, 8, respectively. The MnO2 stock slurry was kept stirring before use to obtain a homogeneous MnO2 suspensions sample. Reactions were initiated by spiking a certain volume of a MnO2 stock slurry into pH-buffered solutions containing one selected sulfonamide and a mediator at desired concentrations. MnO2 was dosed in excess of sulfonamides to warrant pseudo first-order conditions. At specific time intervals, samples were collected and quenched by dosing 10 mL 0.5 M ascorbic acid to measure the concentration of sulfonamides by high-performance liquid chromatography (HPLC) with UV detection. Further experiments were performed to examine the effects of
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Table 1 Sulfonamides and model humic constituents.
Sulfonamides
Abbreviation
pKa
Reference
Sulfamethoxazole
SMX
R group
pKa1 ¼ 1.7 pKa2 ¼ 5.6
Lin et al. (1997)
Sulfamethizole
SMZO
pKa1 ¼ 1.9 pKa2 ¼ 5.3
Babi c et al. (2007)
Sulfathiazole
STZ
pKa1 ¼ 2.1 pKa2 ¼ 7.1
Lin et al. (1997)
Sulfapyridine
SPD
pKa1 ¼ 2.2 pKa2 ¼ 8.6
(Lo and Hayton, 1981; Challis et al., 2013)
Sulfamethazine
SMZ
pKa1 ¼ 2.3 pKa2 ¼ 7.4
Lin et al. (1997)
Sulfadiazine
SDZ
pKa1 ¼ 2.1 pKa2 ¼ 6.3
Lin et al. (1997)
Syringaldehyde
SA
7.34
Bialk et al. (2005)
Acetosyringone
AS
7.88
Ragnar et al. (2000)
Model humic constituents
For sulfonamides, pKa1 is for the aniline group and pKa2 is for sulfonamide group.
metal ions (i.e., Ca(II), Mg(II), and Mn(II)) on transformation of SMX in MnO2-mediator system following the same procedure as described above. 2.4. MnO2 regeneration The partially deactivated MnO2 with adsorbed Mn(II) was regenerated as follows: The spent MnO2 particles were separated by centrifugation and washed with ultrapurified water. After an additional centrifugation step of the MnO2 suspension, the supernatant was decanted and replaced with an aqueous Mn(VII) solution to regenerate MnO2. Finally, the regenerated MnO2 was recovered by centrifugation, and then washed with ultrapurified water several times. 2.5. Analytical methods Selected sulfonamides and DOM model moieties were determined using a HPLC (Dionex Ultimate 3000) equipped with a UV detector (see detailed information in Table S1). To identify transformation products from the reaction of SMX with MnO2 in the presence of SA, SMX (20 mM) and SA (40 mM) in borate buffer (10 mM, pH 7) were treated by MnO2 (150 mM). Reactions were
quenched at 90 min by dosing excess ascorbic acid, followed by high performance liquid chromatography and electrospray ionizationtriple quadrupole mass spectrometry (HPLC/ESI-QqQMS) analysis. The HPLC/ESI-QqQMS analysis was conducted to identify transformation products using an ABSciex QTrap 5500 MS equipped with an Agilent series 1260 HPLC. The analyses were performed in full scan mode (50e700 Da, scan time 3.25 s) with a scan rate of 200 Da/ s and a positive electrospray ionization mode (ESIþ). Detailed MS and HPLC parameters are provided in Text S2. Dissolved organic carbon (DOC) was measured using a total organic carbon analyzer (Shimadzu). An ICP-OES (ICPE-9000, Shimadzu) was used to measure cations (i.e., Ca(II), Mg(II), and Mn(II)). The UV/Vis spectra were measured on a Shimadzu UV-1800 spectrophotometer. More detailed information on the applied analytical methods is presented in Text S2, with method detection limits, relative standard deviations, and measuring ranges.
3. Results and discussion 3.1. Kinetics of the abatement of sulfonamides by MnO2 in the presence of various mediators The effect of mediators (i.e., SA, AS, tannic acid, and ABTS) on the
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transformation of sulfamethoxazole (SMX) in a MnO2-mediator system was examined. Fig. 1a shows that SMX reacts very slowly with MnO2 at pH 7 in the absence of mediators when the initial SMX and MnO2 concentrations were 6 mM and 120 mM, respectively. No significant enhancement effect on SMX abatement was observed in the MnO2-tannic acid or the MnO2-ABTS systems. In another study, ABTS could promote the transformation of SMX in the presence of laccase, which was attributed to the formation of ABTS2þ (rather than ABTSþ) from the reaction between laccase and ABTS (Margot et al., 2015). However, we found that ABTSþ, a green stable radical (rather than ABTS2þ), was produced from the oxidation of ABTS by MnO2, and ABTSþ reacted only slowly with SMX. In contrast, the presence of SA and AS significantly enhanced the abatement of SMX by MnO2 at pH 7 (Fig. 1a), and SA and AS were rapidly consumed in these systems (Fig. 1b). A similar enhancement effect of SA was also observed for the abatement of the other selected sulfonamides (i.e., SMZO, STZ, SPD, SMZ, and SDZ) in presence of MnO2 at pH 7 (Fig. S1). Fig. 2 shows a schematic representation of the promoting effect of SA and AS on the transformation of sulfonamides in presence of MnO2. The suggested mechanism is similar to the previously investigated laccase-SA and laccase-AS systems (Margot et al., 2015). The rate of the abatement of SA/AS decreased with increasing reaction time and deviated from pseudo first-order kinetics (Fig. 1b). This might be attributable to (i) the loss of active surface sites on MnO2 by gradual accumulation of reaction products on the surface (Zhang and Huang, 2003), and (ii) the decreasing amount of SA/AS (Fig. 1b). This effect also leads to the gradual decrease of the rate of SMX abatement in the MnO2-SA/AS systems (Fig. 1a).
3.2. Reaction mechanism for SMX transformation in the MnO2-SA system 3.2.1. Transformation products Transformation products of SMX treated by MnO2 in the presence of SA were detected using HPLC/ESI-QqQMS in full scan mode (Table 2). Fig. S2a shows that two transformation products (product ID: I and II) appear at retention times of 35.00 and 37.83 min, respectively, compared to the control (pH-buffered solution containing SMX and SA without MnO2) shown in Fig. S2b (product III at 30.81 min: SMX; product IV at 28.15 min: SA). Product I had molecular ions of m/z 404 and 426 ([MþH]þ ¼ 404 and [MþNa]þ ¼ 426, Fig. S2c) and it was proposed as a coupling product between 2,6-dimethoxy-1,4-benzoquinone (DMBQ) and SMX (i.e., SMX-DMBQ, m/z 403) based on a similar product identified in a laccase-based system (Margot et al., 2015). According to previous
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Fig. 2. Potential MnO2-mediator reaction model for the abatement of sulfonamides.
studies, the molecular ions of product II, m/z 319 and 341 ([MþH]þ ¼ 319 and [MþNa]þ ¼ 341, Fig. S2d), was likely a dimeric product of SA (i.e., SA-SA, m/z 318) (Bialk et al., 2005; Ibrahim et al., 2013). 3.2.2. Reaction mechanism Based on the suggested products (i.e., SMX-DMBQ and SA-SA) formed during abatement of SMX in the MnO2-SA system, a MnO2-mediated oxidation model is proposed and shown in Scheme S1 and the Graphical abstract. First, MnO2 oxidizes SA producing a SA radical (i.e., the phenoxy radical, SA), followed by the formation of DMBQ according to previous studies (Bialk et al., 2005; Margot et al., 2015). MnO2þSA/SA/DMBQ
(1)
The SA radical also reacts by a radical-radical coupling reaction, forming the SA-SA coupling product (eq. 2). SAþSA/SA-SA
(2)
DMBQ formed from the SA radical (eq. (1)) can react as a nucleophile with amines (Wang et al., 2002). The anilinic nitrogen of SMX participates in a nucleophilic addition to the quinone group in DMBQ, leading to the formation of the unprotonated imine quinone (Thorn et al., 1996) (eq. 3). DMBQ þ SMX/ SMX-DMBQ
(3)
This mechanism is similar to laccase-mediator and H2O2/ peroxidase-mediator systems (Bialk et al., 2005; Margot et al., 2015). For the abatement of SMX by MnO2-SA, Mn(III) could be formed from the reaction of MnO2 with SA via a one-electron transfer. Since the cross-coupling reaction product, SMX-DMBQ was the final product, which cannot be formed by reaction with
Fig. 1. (a) Kinetics of the abatement of sulfamethoxazole (SMX) in a MnO2-mediator system at pH 7. Mediators: syringaldehyde (SA), acetosyringone (AS), tannic acid, and ABTS. (b) Abatement of SA and AS during the transformation of SMX in the MnO2-SA and MnO2-AS systems at pH 7. Experimental condition: [MnO2] ¼ 120 mM, [SA] ¼ 12 mM, [AS] ¼ 12 mM, [tannic acid] ¼ 12 mM, [ABTS] ¼ 50 mM, and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
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Table 2 Oxidation products of SMX in the MnO2-SA system detected by LC-MS/MS. Product ID
Retention time (min)
ESI(þ) MS/MS m/za
Molar mass (g/mol)
Types of product
I
37.83
404, 426
403
SMX-DMBQ
II
35.00
319, 341
318
Dimeric SA
III
30.81
254, 276
253
SMX
IV
28.15
183, 205
182
SA
a
Proposed structure
The molecular ions of products with two m/z values equal to [MþH]þ (i.e., [Mþ1]þ) and [MþNa]þ (i.e., [Mþ23]þ), respectively (see detailed information in Section 3.2.1).
Mn(III), it can be concluded that Mn(III) has little effect on the abatement of SMX. In addition, the effect of the mediator (i.e., SA) on the transformation of sulfamethoxazole (SMX) was tested with Mn(VII). Fig. S3 shows no enhancement of the transformation of SMX in the Mn(VII)-SA system. This result may be attributed to the fact that no benzoquinone-like compounds are formed during Mn(VII) oxidation of humic constituents (Matsuda and Schnitzer, 1972). Instead, organic acids (i.e., dicarboxylic, benzenecarboxylic, or phenolic acids) are observed. 3.3. Influencing factors on the abatement efficiency of sulfonamides in the MnO2-mediator system 3.3.1. Effect of mediator concentration The promoting effect of SA at different concentrations (0, 6, and 12 mM) was evaluated by comparing the degree of abatement of SMX under otherwise identical conditions. Fig. 3aed shows that the rate of the relative abatement of SMX increases with increasing SA concentrations for the pH range 5e8. For example, at pH 6, the extent of SMX abatement at 60 min was roughly proportional to the SA concentration with 49% at 12 mM, 27% at 6 mM and 4% at 0 mM, respectively (Fig. 3b). For a given pH, high initial concentrations of SA result in a fast formation of SAox which in turn leads to a faster transformation of SMX. A similar concentration-dependent enhancing effect was observed for AS in a system containing MnO2 and SMX (Figs. S4aed). 3.3.2. Effect of pH For 12 mM SA at 60 min, the extent of SMX abatement at different pH followed the order of pH 6 (49%) > pH 7 (29%) z pH 5 (27%) > pH 8 (14%) (Fig. 3aed). The pH effect can be explained as follows: The oxidation rate of SA by MnO2 decreases with increasing pH (Fig. S5a) because MnO2 is a stronger oxidant at lower pH. According to a previous study (Dodd and Huang, 2004), sulfonamides exhibit two acid dissociation constants, one involving deprotonation of the anilinium N, and the other corresponding to the deprotonation of the sulfonamide NH. The deprotonation of the latter leads to an anionic form of SMX at higher pH values. SMX has
a pKa2 of 5.6 (Lin et al., 1997) and changes from a neutral to negatively charged species with increasing pH (i.e., 5e8). The anionic SMX species is considerably more reactive than the neutral species (Dodd and Huang, 2004). Therefore, SMX becomes more reactive when the pH increases from 5 to 8, whereas the formation rate of DMBQ became lower (Fig. S5a). These two factors could explain the maximum rate of SMX abatement at pH 6 (Fig. 3). In the MnO2-AS system, the rate of AS abatement decreased with increasing pH (Fig. S5b), and the order of the extent of SMX abatement in the MnO2-AS system at different pH values was similar to the MnO2-SA system (Figs. S4aed).
3.3.3. Comparison of the extent of abatement of the various sulfonamides Figs. S6, S7, S8, S9 and S10 show the effect of SA on the abatement of SMZO, STZ, SPD, SMZ and SDZ in the presence of MnO2 in the pH range 5e8. The kinetics of the abatement of the various sulfonamides were compared by examining the extent of transformation at a certain reaction time and pH value. For 12 mM SA and pH 6 at 30 min, the extent of the abatement of various sulfonamides decreased in the order SMX (38%) >STZ (35%) > SMZ (30%) > SMZO (28%) z SPD (28%) >SDZ (24%). The order of the extents of abatement of SMX, STZ, SMZ, and SMZO at pH 6 was in reasonable agreement with the data of apparent second order rate constants for the reaction of sulfonamides with chlorine (Chamberlain and Adams, 2006). Based on previous studies, the reactive functional group in sulfonamides is the aniline moiety (Jenkins et al., 1978; Huber et al., 2005). The differences in the extent of the abatement of various sulfonamides might be caused by (i) the effect of electron donating/withdrawing of five/six-membered heterocyclic aromatic moiety on sulfonamides and (ii) the various pKa2 values of the selected sulfonamides ranging from 5.6 (SMX) (Lin et al., 1997) to 8.4 (SPD) (Lo and Hayton, 1981), which are shown in Table 1. Anionic species of sulfonamides are more reactive than their neutral species (Huber et al., 2005; Chamberlain and Adams, 2006). In contrast to SPD (99.6% neutral form), SMX is mainly present in its anionic form (72%). However, SPD had higher extent of relative abatement than SDZ (34% anionic form). This might be due to the
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Fig. 3. Kinetics of the abatement of SMX in the MnO2-SA system at (a) pH 5, (b) pH 6, (c) pH 7, and (d) pH 8 for various SA concentrations. Experimental conditions: [MnO2] ¼ 120 mM, [SA] ¼ 0, 6, and 12 mM, and [SMX] ¼ 6 mM pH 5 and 6: sodium acetate buffer (10 mM); pH 7 and 8: borate buffer (10 mM). The marked squares in each figure show the relative residual SMX concentrations at 60 min.
fact that the diazine moiety in SDZ should have a stronger electron withdrawing effect than pyridine in SPD, rendering the latter more easily oxidizable. Similar effects could also explain the higher extent of the relative abatement of SMZ (3% anionic form) than SDZ (34% anionic form), because the methazine moiety on SMZ has two methyl groups (electron-donating) compared to the diazine moiety on SDZ. 3.3.4. Effects of metal ions The effect of metal ions (i.e., Ca(II), Mg(II), and Mn(II)) on the transformation of SMX in the MnO2-SA system at pH 7 was examined. Fig. 4 and Figure S11 show that the SMX abatement in the MnO2-SA system is generally inhibited by metal ions. Compared to the relative abatement of SMX after 240 min in absence of metals (ca. 40%) the relative abatements were 18%, 14%, 31%, 24%, 30%, and
8% for 10 mM Ca(II), 50 mM Ca(II), 10 mM Mg(II), 50 mM Mg(II), 10 mM Mn(II), and 50 mM Mn(II), respectively. This result may be attributed to the inhibiting effect of metal ions on SA oxidation and eventually DMBQ formation from the reaction of MnO2 with SA. For example, the addition of Ca(II) could suppress the oxidation of SA by MnO2 significantly (Fig. S12). In a previous study it was reported that the oxidation efficiency of MnO2 for organic compounds was inhibited by adsorption of metal ions on negatively charged reactive sites on the MnO2 surface (Lin et al., 2009b). The inhibiting effect of metal ions varied with metal type and concentrations (Fig. 4 and Figure S11). Higher metal concentrations led to higher inhibiting effects. The inhibitory effect of the metal ions followed the order of Mn(II) > Ca(II) > Mg(II), which can be ascribed to their affinity to MnO2 surfaces (Morgan and Stumm, 1964; Murray, 1975; Lin et al., 2009a). 3.4. MnO2 regeneration with permanganate
Fig. 4. Effect of Mn(II) on the kinetics of the abatement of SMX in the MnO2-SA system at pH 7. Experimental conditions: [MnO2] ¼ 120 mM, [SA] ¼ 12 mM, [Mn(II)] ¼ 10 and 50 mM and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
Experiments were conducted to test the long-term oxidative performance of MnO2. In four consecutive SMX abatement experiments in the MnO2-SA system (30 min at pH 7) its efficiency dropped gradually from 56% to 27% (Fig. 5a). This can be ascribed to a progressively decreasing oxidation efficiency (from 99% to 38%) of SA by MnO2 (Fig. S13a). As shown above, Mn(II), which is formed during SA oxidation, could partially inhibit the oxidation of SA by adsorption to the MnO2 surface. Permanganate was chosen as a regenerating agent due to the fast oxidation of Mn(II) by Mn(VII) and the concomitant regeneration of fresh MnO2 on the surface (Song et al., 2017). After regeneration, the extent of abatement of SMX remained at 50% for all four runs (30 min), similar to the first run (i.e., 54%) (Fig. 5b). In addition, SA was completely oxidized in each run (Fig. S13b). Hence, Mn(VII), a non-toxic and inexpensive
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matter, it was proposed to apply chlorine to regenerate manganese oxide-coated sand for oxidation of organic stormwater contaminants (Charbonnet et al., 2018). In this study, Mn(VII) (ca. 4 mg/L) (Guo et al., 2017) was shown to be an efficient regenerating agent for recovering the oxidation capacity of spent MnO2. However, in this case the regeneration effect was based on only Mn(II) oxidation in clean systems and it is unclear yet, if it would also work for DOMloaded MnO2. 4. Conclusions Reaction kinetics and products of MnO2-mediated transformations of sulfonamides with model humic mediators were assessed in this study. The following conclusions can be drawn:
Fig. 5. Kinetics of SMX abatement in the MnO2-SA system during four cycles with MnO2 (a) washed with deionized water and (b) regenerated with Mn(VII) in successive runs. Experimental conditions: [MnO2] ¼ 500 mM, [SA] ¼ 12 mM, and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
regenerating agent, can be applied to recover the oxidative capacity of MnO2.
MnO2-mediated transformation of sulfonamides occurs in the presence of syringaldehyde (SA) and acetosyringone (AS), while MnO2 alone has only a limited effect on the transformation of these compounds. ABTS and tannic acid have negligible enhancing effects as mediators for the selected target compounds. The cross-coupling products SMX-DMBQ and SA-SA were detected from the transformation of SMX in the MnO2-SA system. Metal ions including Mn(II), Ca(II), and Mg(II) have an inhibitory effect on the transformation of sulfonamides in the MnO2-SA system decreasing in the order Mn(II) > Ca(II) > Mg(II). Permanganate (Mn(VII)) efficiently regenerates spent MnO2 recovering partially deactivated MnO2 after successive runs of the MnO2-SA system. Mn(VII) oxidizes the adsorbed Mn(II) and regenerates the active MnO2 sites.
Declaration of interests None.
3.5. MnO2-mediator systems for wastewater treatment Acknowledgments For wastewater treatment, a MnO2-mediator system may offer an option for the transformation of micropollutants such as sulfonamide antibiotics. Fig. S14a shows that SA could also enhance the extent/kinetics of SMX during MnO2 oxidation in EPPWW, albeit the effect is significantly smaller than in synthetic water. This result may be ascribed to the fact that effluent organic matter may also consume the SA radical formed from the reaction between MnO2 and SA, resulting in a lower efficiency of the MnO2-SA system. In addition, metal ions in EPPWW ([Ca(II)] ¼ 2.58 mM, [Mg(II)] ¼ 0.79 mM, [Mn(II)] ¼ 0.14 mM, more water quality parameters are given in section 2.1) could inhibit the oxidation of SA in the MnO2-SA system (Fig. S14b), which was discussed in detail in section 3.3.4. In a previous study, the residual antibiotic activity during oxidative abatement of SMX by ozone and hydroxyl radicals was related to the residual concentrations of the parent antibacterial SMX (Dodd et al., 2009). Based on this study, only slight changes in the molecular structure are necessary to lose the antibiotic activity. Hence, it can be expected that the antibiotic activity in the MnO2-SA system decreases proportionally with the residual SMX concentration. A previous study reported that an active filter bed consisting of MnO2-loaded sand was feasible for treating water contaminated with arsenite(III) (Driehaus et al., 1995). Also, manganese oxides could be used as a geomedia amendment for the abatement of organic contaminants in engineered stormwater infiltration systems (Grebel et al., 2016), which were expected to retain their reactivity for 25 years. Since the reactivity of this filter would decrease due to metal ions and natural/effluent organic
Yang Song is grateful for a grant from the China Scholarship Council (CSC). We would like to thank Florian Breider, Minju Lee and Caroline Gachet for helpful discussions and laboratory assistance. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.watres.2019.01.011. References Babi c, S., Horvat, A.J.M., Mutavd zi c Pavlovi c, D., Kastelan-Macan, M., 2007. Determination of pKa values of active pharmaceutical ingredients. Trac. Trends Anal. Chem. 26 (11), 1043e1061. Bialk, H.M., Simpson, A.J., Pedersen, J.A., 2005. Cross-coupling of sulfonamide antimicrobial agents with model humic constituents. Environ. Sci. Technol. 39 (12), 4463e4473. Camarero, S., Ibarra, D., Martínez, M.J., Martínez, A.T., 2005. Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl. Environ. Microbiol. 71 (4), 1775e1784. Challis, J.K., Carlson, J.C., Friesen, K.J., Hanson, M.L., Wong, C.S., 2013. Aquatic photochemistry of the sulfonamide antibiotic sulfapyridine. J. Photochem. Photobiol. Chem. 262, 14e21. Chamberlain, E., Adams, C., 2006. Oxidation of sulfonamides, macrolides, and carbadox with free chlorine and monochloramine. Water Res. 40 (13), 2517e2526. Charbonnet, J.A., Duan, Y., van Genuchten, C.M., Sedlak, D.L., 2018. Chemical regeneration of manganese oxide-coated sand for oxidation of organic stormwater contaminants. Environ. Sci. Technol. 52 (18), 10728e10736. Craig, C.R., Stitzel, R.E., 2004. Modern Pharmacology with Clinical Applications.
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Enhanced transformation of sulfonamide antibiotics by manganese(IV) oxide in the presence of model humic constituents Yang Song a, c, Jin Jiang b, ** , Jun Ma e, Yang Zhou e, Urs von Gunten c, d, * a Key Laboratory for Water Quality and Conservation of the Pearl River Delta, Ministry of Education, Institute of Environmental Research at Greater Bay, Guangzhou University, Guangzhou, 510006, China b Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, Guangdong, 510006, China c School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique F ed erale de Lausanne (EPFL), CH-1015, Lausanne, Switzerland d Eawag, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, CH-8600, Düebendorf, Switzerland e State Key Laboratory of Urban Water Resource and Environment, School of Municipal and Environmental Engineering, Harbin Institute of Technology, Harbin, 150090, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 November 2018 Received in revised form 8 January 2019 Accepted 10 January 2019 Available online 21 January 2019
In this study, a manganese(IV) oxide-mediator (MnO2-mediator) system for the abatement of sulfonamide antibiotics was evaluated. Two simple model humic constituents, syringaldehyde (SA) and acetosyringone (AS), could promote the transformation of sulfonamides at pH 5e8. Two additional potential mediators, tannic acid and 2,20 -azino-bis(3-ethylbenzothiazoline)-6-sulfonate (ABTS), had negligible enhancement on the transformation of sulfonamides by MnO2. The enhancing effect was attributed to the reaction of the oxidized mediator (i.e., phenoxy radical or benzoquinone-like compounds) produced from the oxidation of the mediators by MnO2 with SMX. Thereby cross-coupling products from sulfamethoxazole (SMX) with oxidized SA were formed in the MnO2-SA system, which was confirmed by liquid chromatography/electrospray ionization-triple quadrupole mass spectrometry. Coexisting metal ions (i.e., Ca(II), Mg(II) and Mn(II)) showed inhibitory effects in the order of Mn(II)> Ca(II)> Mg(II). For repetitive runs of the MnO2-SA-SMX system, MnO2 lost its oxidative capacity due to the sorption of Mn(II) on the reactive sites of the MnO2 surface. A full regeneration of partially deactivated MnO2 by oxidation of the sorbed Mn(II) with Mn(VII) could be achieved. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Manganese oxide (MnO2) Sulfonamide antibiotics Mediators Cross-coupling Metal ions Regeneration
1. Introduction Sulfonamide antibiotics consisting of synthetic sulfanilamide derivatives are widely used in both human medicine and livestock production (Mellon et al., 2001). They include compounds such as sulfamethoxazole, sulfacetamide, sulfadoxine, sulfadiazine, sulfamethizole, sulfasalazine, sulfanilamide, and sulfisoxazole (Mellon et al., 2001; Garoma et al., 2010). The antibiotic effect is based on (i) a delay of the regeneration of bacterial cells, and (ii) prevention of cell growth via inhibition of the formation of folic acid (Craig and
* Corresponding author. School of Architecture, Civil and Environmental Engi de rale de Lausanne (EPFL), CH-1015, Launeering (ENAC), Ecole Polytechnique Fe sanne, Switzerland. ** Corresponding author. Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, Guangdong, 510006, China. E-mail addresses: [email protected] (J. Jiang), [email protected] (U. von Gunten). https://doi.org/10.1016/j.watres.2019.01.011 0043-1354/© 2019 Elsevier Ltd. All rights reserved.
Stitzel, 2004). Sulfonamide antibiotics have already been identified in soils and aquatic environments where they are emitted via several pathways (Kümmerer, 2003; Miao et al., 2004). Treating fields with manure from treated animals is a major pathway of sulfonamide antibiotics entering soils (Kümmerer, 2003). Sulfonamides in soils are introduced into groundwater or surface water via infiltration or runoff, respectively. In addition, sulfonamides from domestic and hospital applications are discharged into municipal wastewater (Gao and Pedersen, 2005). It has been reported previously that sulfonamides are not readily biodegradable (Ingerslev and Halling Sørensen, 2000), hence chemical oxidation processes, such as ozonation (Huber et al., 2005), chlorination (Dodd and Huang, 2004), and chloramination (Chamberlain and Adams, 2006) are promising for the transformation of sulfonamides. Furthermore, it has been demonstrated that the relative antimicrobial potency of sulfamethoxazole decreases proportionally with its relative residual concentration for oxidation with ozone and hydroxyl radical (Dodd et al., 2009). This demonstrates
Y. Song et al. / Water Research 153 (2019) 200e207
that oxidation processes are promising options for the treatment of this class of antibiotics. Manganese oxides (MnO2) are abundant natural oxidants in sediments and soils, and can affect the transformation of organic pollutants through direct oxidation, adsorption, and surface catalysis (Stone, 1987; Wang et al., 1999). Recently, MnO2 has been suggested as a passive barrier against micropollutants during recharge of stormwaters (Grebel et al., 2016; Charbonnet et al., 2018). It is well documented that MnO2 can oxidize phenols and anilines (Stone, 1987; Laha and Luthy, 1990; Ukrainczyk and McBride, 1993). Furthermore, it has been shown that various types of antimicrobial agents, such as fluoroquinolone, tetracyclines, and phenols can be transformed by MnO2 (Zhang and Huang, 2005; Zhang et al., 2008; Forrez et al., 2011). The following general reaction mechanism has been proposed: (i) Precursor complex formation on the MnO2 surface, (ii) electron transfer from the target compound to MnO2, and (iii) release of the reaction products including the organic transformation products and partially Mn(II) (Zhang and Huang, 2005; Zhang et al., 2008). A previous study (Gao et al., 2012) reported that a transformation of sulfamethazine (SMZ) by MnO2 occurred at acidic pH (4, 5, and 5.6), while no transformation was observed at higher pH (i.e., pH 6.3 and 7.6), due to the decreasing reduction potential of MnO2 (depending on the reactive surface sites on the MnO2 surface) with increasing pH (Zhang et al., 2008). Therefore, strategies for an enhanced transformation of sulfonamides by MnO2 over a wide pH range need to be developed. In a previous study, it has been demonstrated that the transformation of chloroanilines by birnessite was considerably enhanced by adding phenolic humic constituents at pH 5.6. Phenolic humic constituents in natural organic matter are ubiquitous in the aquatic environment containing numerous moieties, such as syringaldehyde, acetosyringone, ferulic acid, and protocatechuic acid (Park et al., 1999). The mechanism of the mediated transformation of chloroanilines involves two stages, (i) free radicals (including phenoxy and aniline radicals) are produced from the oxidation of the phenolic humic constituents and the target compounds (i.e., chloroanilines), respectively by MnO2. (ii) Cross-coupling reactions including radical-radical coupling between different oxidation products or nucleophilic addition to aromatic amines occur, resulting in the formation of quinones, dimers, and polymeric oxidation products (Stone, 1987; Dec et al., 2001; Wang et al., 2002; Thorn and Kennedy, 2002). Similarly, an enhanced transformation of sulfonamides by laccase in the presence of several mediators such as syringaldehyde (SA), acetosyringone (AS), and 2,2-azinobis(3-ethylbenzothiazoline)-6-sulfonic acid diammonium (ABTS) with the formation of cross-coupling products from the free radicals and amine moieties has been reported (Margot et al., 2015), and the toxicity of product mixtures was found to be lower than for untreated sulfonamides (Margot et al., 2015). Based on this information, the present study examines the feasibility of model humic constituents (i.e., SA, AS, tannic acid), or synthetic electron shuttles (i.e., ABTS) to enhance the transformation of SMX, which is normally not abated by MnO2 in MnO2mediator systems. SA, AS and tannic acid were selected as natural mediators, which were classified as common natural organic matter constituents in aquatic environments (Park et al., 1999). ABTS was the most commonly used synthetic electron shuttle, which can be oxidized forming the ABTS radical (Song et al., 2015). The potential of MnO2-mediated transformations of other selected sulfonamides including SMZ, sulfamethizole (SMZO), sulfathiazole (STZ), sulfapyridine (SPD), and sulfadiazine (SDZ) was also investigated. Transformation products of SMX in the MnO2-SA system were identified, and a reaction mechanism is proposed. Furthermore, influencing factors such as mediator concentrations, pH, and
201
metal ions (e.g., Ca(II), Mg(II), and Mn(II)) on SMX transformation in MnO2-mediator systems were investigated. Since permanganate (Mn(VII)) reacts rapidly with Mn(II) (Van Benschoten et al., 1992; Song et al., 2017), Mn(VII) was tested as a regeneration agent to recover the oxidizing capacity of MnO2 in this study. Finally, the potential of the application of MnO2-mediator systems for the treatment of sulfonamides in a wastewater effluent was assessed. 2. Experimental methods 2.1. Chemicals and reagents All chemicals were analytical grade or higher quality and obtained from commercial suppliers (see Text S1 for details). The abbreviations, structures, and pKa values (Lucida et al., 2000; Camarero et al., 2005; Babi c et al., 2007) of the sulfonamides and humic constituents are presented in Table 1. All stock solutions were prepared with ultrapurified water (18.2 MU cm) obtained from a Millipore Milli-Q water purification system. A wastewater effluent sample was obtained from the nitrified Eawag pilot plant in Dübendorf (EPPWW), Switzerland (DOC ¼ 7.6 mg C/L, [Ca(II)] ¼ 2.58 mM, [Mg(II)] ¼ 0.79 mM, [Mn(II)] ¼ 0.14 mM, carbonate alkalinity ¼ 5.99 mM, and pH ¼ 7.8). After filtering through a nylon membrane with a pore size of 0.45 mm (Membrane Solutions), the samples were buffered to pH 7 with borate buffer (10 mM) and stored at 4 C. 2.2. MnO2 preparation MnO2 was prepared by the method of Murray (1974) by the stoichiometric reaction between potassium permanganate (Mn(VII)) and manganese(II) chloride (MnCl2). The permanganate stock solution (ca. 0.24 M) in ultrapurified water was diluted and then standardized spectrophotometrically by measuring the absorbance at 525 nm (ε ¼ 2500 M1 cm1) (Song et al., 2015). To synthesize MnO2 suspensions, permanganate and sodium hydroxide (NaOH) were added to nitrogen purged ultrapurified water, followed by a dropwise addition of a solution of MnCl2 under constant stirring. The formed MnO2 was settled and the supernatant was replaced with ultrapurified water several times until the conductivity of the supernatant was less than 2 mS/cm. The MnO2 suspensions were characterized by determination of the total manganese concentration after dissolution by ascorbic acid by (i) an inductively coupled plasma optical emission spectrometer (ICPOES) and (ii) the 2,2-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid diammonium (ABTS) spectrophotometric method (Jiang et al., 2012). The MnO2 suspensions were stored in the dark at 4 C until use within a week. 2.3. Reaction kinetics All the experiments were performed for pH values of 5, 6, 7, and 8 at 25 ± 1 C. Sodium acetate and sodium borate buffers (10 mM) were used for pH 5, 6 and pH 7, 8, respectively. The MnO2 stock slurry was kept stirring before use to obtain a homogeneous MnO2 suspensions sample. Reactions were initiated by spiking a certain volume of a MnO2 stock slurry into pH-buffered solutions containing one selected sulfonamide and a mediator at desired concentrations. MnO2 was dosed in excess of sulfonamides to warrant pseudo first-order conditions. At specific time intervals, samples were collected and quenched by dosing 10 mL 0.5 M ascorbic acid to measure the concentration of sulfonamides by high-performance liquid chromatography (HPLC) with UV detection. Further experiments were performed to examine the effects of
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Y. Song et al. / Water Research 153 (2019) 200e207
Table 1 Sulfonamides and model humic constituents.
Sulfonamides
Abbreviation
pKa
Reference
Sulfamethoxazole
SMX
R group
pKa1 ¼ 1.7 pKa2 ¼ 5.6
Lin et al. (1997)
Sulfamethizole
SMZO
pKa1 ¼ 1.9 pKa2 ¼ 5.3
Babi c et al. (2007)
Sulfathiazole
STZ
pKa1 ¼ 2.1 pKa2 ¼ 7.1
Lin et al. (1997)
Sulfapyridine
SPD
pKa1 ¼ 2.2 pKa2 ¼ 8.6
(Lo and Hayton, 1981; Challis et al., 2013)
Sulfamethazine
SMZ
pKa1 ¼ 2.3 pKa2 ¼ 7.4
Lin et al. (1997)
Sulfadiazine
SDZ
pKa1 ¼ 2.1 pKa2 ¼ 6.3
Lin et al. (1997)
Syringaldehyde
SA
7.34
Bialk et al. (2005)
Acetosyringone
AS
7.88
Ragnar et al. (2000)
Model humic constituents
For sulfonamides, pKa1 is for the aniline group and pKa2 is for sulfonamide group.
metal ions (i.e., Ca(II), Mg(II), and Mn(II)) on transformation of SMX in MnO2-mediator system following the same procedure as described above. 2.4. MnO2 regeneration The partially deactivated MnO2 with adsorbed Mn(II) was regenerated as follows: The spent MnO2 particles were separated by centrifugation and washed with ultrapurified water. After an additional centrifugation step of the MnO2 suspension, the supernatant was decanted and replaced with an aqueous Mn(VII) solution to regenerate MnO2. Finally, the regenerated MnO2 was recovered by centrifugation, and then washed with ultrapurified water several times. 2.5. Analytical methods Selected sulfonamides and DOM model moieties were determined using a HPLC (Dionex Ultimate 3000) equipped with a UV detector (see detailed information in Table S1). To identify transformation products from the reaction of SMX with MnO2 in the presence of SA, SMX (20 mM) and SA (40 mM) in borate buffer (10 mM, pH 7) were treated by MnO2 (150 mM). Reactions were
quenched at 90 min by dosing excess ascorbic acid, followed by high performance liquid chromatography and electrospray ionizationtriple quadrupole mass spectrometry (HPLC/ESI-QqQMS) analysis. The HPLC/ESI-QqQMS analysis was conducted to identify transformation products using an ABSciex QTrap 5500 MS equipped with an Agilent series 1260 HPLC. The analyses were performed in full scan mode (50e700 Da, scan time 3.25 s) with a scan rate of 200 Da/ s and a positive electrospray ionization mode (ESIþ). Detailed MS and HPLC parameters are provided in Text S2. Dissolved organic carbon (DOC) was measured using a total organic carbon analyzer (Shimadzu). An ICP-OES (ICPE-9000, Shimadzu) was used to measure cations (i.e., Ca(II), Mg(II), and Mn(II)). The UV/Vis spectra were measured on a Shimadzu UV-1800 spectrophotometer. More detailed information on the applied analytical methods is presented in Text S2, with method detection limits, relative standard deviations, and measuring ranges.
3. Results and discussion 3.1. Kinetics of the abatement of sulfonamides by MnO2 in the presence of various mediators The effect of mediators (i.e., SA, AS, tannic acid, and ABTS) on the
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transformation of sulfamethoxazole (SMX) in a MnO2-mediator system was examined. Fig. 1a shows that SMX reacts very slowly with MnO2 at pH 7 in the absence of mediators when the initial SMX and MnO2 concentrations were 6 mM and 120 mM, respectively. No significant enhancement effect on SMX abatement was observed in the MnO2-tannic acid or the MnO2-ABTS systems. In another study, ABTS could promote the transformation of SMX in the presence of laccase, which was attributed to the formation of ABTS2þ (rather than ABTSþ) from the reaction between laccase and ABTS (Margot et al., 2015). However, we found that ABTSþ, a green stable radical (rather than ABTS2þ), was produced from the oxidation of ABTS by MnO2, and ABTSþ reacted only slowly with SMX. In contrast, the presence of SA and AS significantly enhanced the abatement of SMX by MnO2 at pH 7 (Fig. 1a), and SA and AS were rapidly consumed in these systems (Fig. 1b). A similar enhancement effect of SA was also observed for the abatement of the other selected sulfonamides (i.e., SMZO, STZ, SPD, SMZ, and SDZ) in presence of MnO2 at pH 7 (Fig. S1). Fig. 2 shows a schematic representation of the promoting effect of SA and AS on the transformation of sulfonamides in presence of MnO2. The suggested mechanism is similar to the previously investigated laccase-SA and laccase-AS systems (Margot et al., 2015). The rate of the abatement of SA/AS decreased with increasing reaction time and deviated from pseudo first-order kinetics (Fig. 1b). This might be attributable to (i) the loss of active surface sites on MnO2 by gradual accumulation of reaction products on the surface (Zhang and Huang, 2003), and (ii) the decreasing amount of SA/AS (Fig. 1b). This effect also leads to the gradual decrease of the rate of SMX abatement in the MnO2-SA/AS systems (Fig. 1a).
3.2. Reaction mechanism for SMX transformation in the MnO2-SA system 3.2.1. Transformation products Transformation products of SMX treated by MnO2 in the presence of SA were detected using HPLC/ESI-QqQMS in full scan mode (Table 2). Fig. S2a shows that two transformation products (product ID: I and II) appear at retention times of 35.00 and 37.83 min, respectively, compared to the control (pH-buffered solution containing SMX and SA without MnO2) shown in Fig. S2b (product III at 30.81 min: SMX; product IV at 28.15 min: SA). Product I had molecular ions of m/z 404 and 426 ([MþH]þ ¼ 404 and [MþNa]þ ¼ 426, Fig. S2c) and it was proposed as a coupling product between 2,6-dimethoxy-1,4-benzoquinone (DMBQ) and SMX (i.e., SMX-DMBQ, m/z 403) based on a similar product identified in a laccase-based system (Margot et al., 2015). According to previous
203
Fig. 2. Potential MnO2-mediator reaction model for the abatement of sulfonamides.
studies, the molecular ions of product II, m/z 319 and 341 ([MþH]þ ¼ 319 and [MþNa]þ ¼ 341, Fig. S2d), was likely a dimeric product of SA (i.e., SA-SA, m/z 318) (Bialk et al., 2005; Ibrahim et al., 2013). 3.2.2. Reaction mechanism Based on the suggested products (i.e., SMX-DMBQ and SA-SA) formed during abatement of SMX in the MnO2-SA system, a MnO2-mediated oxidation model is proposed and shown in Scheme S1 and the Graphical abstract. First, MnO2 oxidizes SA producing a SA radical (i.e., the phenoxy radical, SA), followed by the formation of DMBQ according to previous studies (Bialk et al., 2005; Margot et al., 2015). MnO2þSA/SA/DMBQ
(1)
The SA radical also reacts by a radical-radical coupling reaction, forming the SA-SA coupling product (eq. 2). SAþSA/SA-SA
(2)
DMBQ formed from the SA radical (eq. (1)) can react as a nucleophile with amines (Wang et al., 2002). The anilinic nitrogen of SMX participates in a nucleophilic addition to the quinone group in DMBQ, leading to the formation of the unprotonated imine quinone (Thorn et al., 1996) (eq. 3). DMBQ þ SMX/ SMX-DMBQ
(3)
This mechanism is similar to laccase-mediator and H2O2/ peroxidase-mediator systems (Bialk et al., 2005; Margot et al., 2015). For the abatement of SMX by MnO2-SA, Mn(III) could be formed from the reaction of MnO2 with SA via a one-electron transfer. Since the cross-coupling reaction product, SMX-DMBQ was the final product, which cannot be formed by reaction with
Fig. 1. (a) Kinetics of the abatement of sulfamethoxazole (SMX) in a MnO2-mediator system at pH 7. Mediators: syringaldehyde (SA), acetosyringone (AS), tannic acid, and ABTS. (b) Abatement of SA and AS during the transformation of SMX in the MnO2-SA and MnO2-AS systems at pH 7. Experimental condition: [MnO2] ¼ 120 mM, [SA] ¼ 12 mM, [AS] ¼ 12 mM, [tannic acid] ¼ 12 mM, [ABTS] ¼ 50 mM, and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
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Table 2 Oxidation products of SMX in the MnO2-SA system detected by LC-MS/MS. Product ID
Retention time (min)
ESI(þ) MS/MS m/za
Molar mass (g/mol)
Types of product
I
37.83
404, 426
403
SMX-DMBQ
II
35.00
319, 341
318
Dimeric SA
III
30.81
254, 276
253
SMX
IV
28.15
183, 205
182
SA
a
Proposed structure
The molecular ions of products with two m/z values equal to [MþH]þ (i.e., [Mþ1]þ) and [MþNa]þ (i.e., [Mþ23]þ), respectively (see detailed information in Section 3.2.1).
Mn(III), it can be concluded that Mn(III) has little effect on the abatement of SMX. In addition, the effect of the mediator (i.e., SA) on the transformation of sulfamethoxazole (SMX) was tested with Mn(VII). Fig. S3 shows no enhancement of the transformation of SMX in the Mn(VII)-SA system. This result may be attributed to the fact that no benzoquinone-like compounds are formed during Mn(VII) oxidation of humic constituents (Matsuda and Schnitzer, 1972). Instead, organic acids (i.e., dicarboxylic, benzenecarboxylic, or phenolic acids) are observed. 3.3. Influencing factors on the abatement efficiency of sulfonamides in the MnO2-mediator system 3.3.1. Effect of mediator concentration The promoting effect of SA at different concentrations (0, 6, and 12 mM) was evaluated by comparing the degree of abatement of SMX under otherwise identical conditions. Fig. 3aed shows that the rate of the relative abatement of SMX increases with increasing SA concentrations for the pH range 5e8. For example, at pH 6, the extent of SMX abatement at 60 min was roughly proportional to the SA concentration with 49% at 12 mM, 27% at 6 mM and 4% at 0 mM, respectively (Fig. 3b). For a given pH, high initial concentrations of SA result in a fast formation of SAox which in turn leads to a faster transformation of SMX. A similar concentration-dependent enhancing effect was observed for AS in a system containing MnO2 and SMX (Figs. S4aed). 3.3.2. Effect of pH For 12 mM SA at 60 min, the extent of SMX abatement at different pH followed the order of pH 6 (49%) > pH 7 (29%) z pH 5 (27%) > pH 8 (14%) (Fig. 3aed). The pH effect can be explained as follows: The oxidation rate of SA by MnO2 decreases with increasing pH (Fig. S5a) because MnO2 is a stronger oxidant at lower pH. According to a previous study (Dodd and Huang, 2004), sulfonamides exhibit two acid dissociation constants, one involving deprotonation of the anilinium N, and the other corresponding to the deprotonation of the sulfonamide NH. The deprotonation of the latter leads to an anionic form of SMX at higher pH values. SMX has
a pKa2 of 5.6 (Lin et al., 1997) and changes from a neutral to negatively charged species with increasing pH (i.e., 5e8). The anionic SMX species is considerably more reactive than the neutral species (Dodd and Huang, 2004). Therefore, SMX becomes more reactive when the pH increases from 5 to 8, whereas the formation rate of DMBQ became lower (Fig. S5a). These two factors could explain the maximum rate of SMX abatement at pH 6 (Fig. 3). In the MnO2-AS system, the rate of AS abatement decreased with increasing pH (Fig. S5b), and the order of the extent of SMX abatement in the MnO2-AS system at different pH values was similar to the MnO2-SA system (Figs. S4aed).
3.3.3. Comparison of the extent of abatement of the various sulfonamides Figs. S6, S7, S8, S9 and S10 show the effect of SA on the abatement of SMZO, STZ, SPD, SMZ and SDZ in the presence of MnO2 in the pH range 5e8. The kinetics of the abatement of the various sulfonamides were compared by examining the extent of transformation at a certain reaction time and pH value. For 12 mM SA and pH 6 at 30 min, the extent of the abatement of various sulfonamides decreased in the order SMX (38%) >STZ (35%) > SMZ (30%) > SMZO (28%) z SPD (28%) >SDZ (24%). The order of the extents of abatement of SMX, STZ, SMZ, and SMZO at pH 6 was in reasonable agreement with the data of apparent second order rate constants for the reaction of sulfonamides with chlorine (Chamberlain and Adams, 2006). Based on previous studies, the reactive functional group in sulfonamides is the aniline moiety (Jenkins et al., 1978; Huber et al., 2005). The differences in the extent of the abatement of various sulfonamides might be caused by (i) the effect of electron donating/withdrawing of five/six-membered heterocyclic aromatic moiety on sulfonamides and (ii) the various pKa2 values of the selected sulfonamides ranging from 5.6 (SMX) (Lin et al., 1997) to 8.4 (SPD) (Lo and Hayton, 1981), which are shown in Table 1. Anionic species of sulfonamides are more reactive than their neutral species (Huber et al., 2005; Chamberlain and Adams, 2006). In contrast to SPD (99.6% neutral form), SMX is mainly present in its anionic form (72%). However, SPD had higher extent of relative abatement than SDZ (34% anionic form). This might be due to the
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Fig. 3. Kinetics of the abatement of SMX in the MnO2-SA system at (a) pH 5, (b) pH 6, (c) pH 7, and (d) pH 8 for various SA concentrations. Experimental conditions: [MnO2] ¼ 120 mM, [SA] ¼ 0, 6, and 12 mM, and [SMX] ¼ 6 mM pH 5 and 6: sodium acetate buffer (10 mM); pH 7 and 8: borate buffer (10 mM). The marked squares in each figure show the relative residual SMX concentrations at 60 min.
fact that the diazine moiety in SDZ should have a stronger electron withdrawing effect than pyridine in SPD, rendering the latter more easily oxidizable. Similar effects could also explain the higher extent of the relative abatement of SMZ (3% anionic form) than SDZ (34% anionic form), because the methazine moiety on SMZ has two methyl groups (electron-donating) compared to the diazine moiety on SDZ. 3.3.4. Effects of metal ions The effect of metal ions (i.e., Ca(II), Mg(II), and Mn(II)) on the transformation of SMX in the MnO2-SA system at pH 7 was examined. Fig. 4 and Figure S11 show that the SMX abatement in the MnO2-SA system is generally inhibited by metal ions. Compared to the relative abatement of SMX after 240 min in absence of metals (ca. 40%) the relative abatements were 18%, 14%, 31%, 24%, 30%, and
8% for 10 mM Ca(II), 50 mM Ca(II), 10 mM Mg(II), 50 mM Mg(II), 10 mM Mn(II), and 50 mM Mn(II), respectively. This result may be attributed to the inhibiting effect of metal ions on SA oxidation and eventually DMBQ formation from the reaction of MnO2 with SA. For example, the addition of Ca(II) could suppress the oxidation of SA by MnO2 significantly (Fig. S12). In a previous study it was reported that the oxidation efficiency of MnO2 for organic compounds was inhibited by adsorption of metal ions on negatively charged reactive sites on the MnO2 surface (Lin et al., 2009b). The inhibiting effect of metal ions varied with metal type and concentrations (Fig. 4 and Figure S11). Higher metal concentrations led to higher inhibiting effects. The inhibitory effect of the metal ions followed the order of Mn(II) > Ca(II) > Mg(II), which can be ascribed to their affinity to MnO2 surfaces (Morgan and Stumm, 1964; Murray, 1975; Lin et al., 2009a). 3.4. MnO2 regeneration with permanganate
Fig. 4. Effect of Mn(II) on the kinetics of the abatement of SMX in the MnO2-SA system at pH 7. Experimental conditions: [MnO2] ¼ 120 mM, [SA] ¼ 12 mM, [Mn(II)] ¼ 10 and 50 mM and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
Experiments were conducted to test the long-term oxidative performance of MnO2. In four consecutive SMX abatement experiments in the MnO2-SA system (30 min at pH 7) its efficiency dropped gradually from 56% to 27% (Fig. 5a). This can be ascribed to a progressively decreasing oxidation efficiency (from 99% to 38%) of SA by MnO2 (Fig. S13a). As shown above, Mn(II), which is formed during SA oxidation, could partially inhibit the oxidation of SA by adsorption to the MnO2 surface. Permanganate was chosen as a regenerating agent due to the fast oxidation of Mn(II) by Mn(VII) and the concomitant regeneration of fresh MnO2 on the surface (Song et al., 2017). After regeneration, the extent of abatement of SMX remained at 50% for all four runs (30 min), similar to the first run (i.e., 54%) (Fig. 5b). In addition, SA was completely oxidized in each run (Fig. S13b). Hence, Mn(VII), a non-toxic and inexpensive
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matter, it was proposed to apply chlorine to regenerate manganese oxide-coated sand for oxidation of organic stormwater contaminants (Charbonnet et al., 2018). In this study, Mn(VII) (ca. 4 mg/L) (Guo et al., 2017) was shown to be an efficient regenerating agent for recovering the oxidation capacity of spent MnO2. However, in this case the regeneration effect was based on only Mn(II) oxidation in clean systems and it is unclear yet, if it would also work for DOMloaded MnO2. 4. Conclusions Reaction kinetics and products of MnO2-mediated transformations of sulfonamides with model humic mediators were assessed in this study. The following conclusions can be drawn:
Fig. 5. Kinetics of SMX abatement in the MnO2-SA system during four cycles with MnO2 (a) washed with deionized water and (b) regenerated with Mn(VII) in successive runs. Experimental conditions: [MnO2] ¼ 500 mM, [SA] ¼ 12 mM, and [SMX] ¼ 6 mM pH 7: borate buffer (10 mM).
regenerating agent, can be applied to recover the oxidative capacity of MnO2.
MnO2-mediated transformation of sulfonamides occurs in the presence of syringaldehyde (SA) and acetosyringone (AS), while MnO2 alone has only a limited effect on the transformation of these compounds. ABTS and tannic acid have negligible enhancing effects as mediators for the selected target compounds. The cross-coupling products SMX-DMBQ and SA-SA were detected from the transformation of SMX in the MnO2-SA system. Metal ions including Mn(II), Ca(II), and Mg(II) have an inhibitory effect on the transformation of sulfonamides in the MnO2-SA system decreasing in the order Mn(II) > Ca(II) > Mg(II). Permanganate (Mn(VII)) efficiently regenerates spent MnO2 recovering partially deactivated MnO2 after successive runs of the MnO2-SA system. Mn(VII) oxidizes the adsorbed Mn(II) and regenerates the active MnO2 sites.
Declaration of interests None.
3.5. MnO2-mediator systems for wastewater treatment Acknowledgments For wastewater treatment, a MnO2-mediator system may offer an option for the transformation of micropollutants such as sulfonamide antibiotics. Fig. S14a shows that SA could also enhance the extent/kinetics of SMX during MnO2 oxidation in EPPWW, albeit the effect is significantly smaller than in synthetic water. This result may be ascribed to the fact that effluent organic matter may also consume the SA radical formed from the reaction between MnO2 and SA, resulting in a lower efficiency of the MnO2-SA system. In addition, metal ions in EPPWW ([Ca(II)] ¼ 2.58 mM, [Mg(II)] ¼ 0.79 mM, [Mn(II)] ¼ 0.14 mM, more water quality parameters are given in section 2.1) could inhibit the oxidation of SA in the MnO2-SA system (Fig. S14b), which was discussed in detail in section 3.3.4. In a previous study, the residual antibiotic activity during oxidative abatement of SMX by ozone and hydroxyl radicals was related to the residual concentrations of the parent antibacterial SMX (Dodd et al., 2009). Based on this study, only slight changes in the molecular structure are necessary to lose the antibiotic activity. Hence, it can be expected that the antibiotic activity in the MnO2-SA system decreases proportionally with the residual SMX concentration. A previous study reported that an active filter bed consisting of MnO2-loaded sand was feasible for treating water contaminated with arsenite(III) (Driehaus et al., 1995). Also, manganese oxides could be used as a geomedia amendment for the abatement of organic contaminants in engineered stormwater infiltration systems (Grebel et al., 2016), which were expected to retain their reactivity for 25 years. Since the reactivity of this filter would decrease due to metal ions and natural/effluent organic
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