Photocatalytic Degradation of Microcystin-LR and Off-Odor

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Photocatalytic Degradation of Microcystin-LR and Off-Odor Compounds in Water under UV‑A and Solar Light with a Nanostructured Photocatalyst Based on Reduced Graphene Oxide− TiO2 Composite. Identification of Intermediate Products. Theodora Fotiou,† Theodoros M. Triantis,† Triantafyllos Kaloudis,‡ Luisa M. Pastrana-Martínez,§ Vlassis Likodimos,⊥ Polycarpos Falaras,⊥ Adrián M.T. Silva,§ and Anastasia Hiskia†,* †

Laboratory of Catalytic−Photocatalytic Processes (Solar Energy−Environment) and ⊥Laboratory of Photo-redox Conversion and Storage of Solar Energy, Institute of Advanced Materials, Physicochemical Processes, Nanotechnology and Microsystems, National Center for Scientific Research “Demokritos”, Patriarchou Grigoriou & Neapoleos, 15310 Agia Paraskevi, Athens, Greece ‡ Quality Control Department, Athens Water Supply and Sewerage Company (EYDAP SA), Oropou 156, 11146 Galatsi, Athens, Greece § LCMLaboratory of Catalysis and Materials−Associate Laboratory LSRE/LCM, Faculdade de Engenharia, Universidade do Porto, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal S Supporting Information *

ABSTRACT: Microcystin-LR (MC-LR) is the most common and toxic variant of the group of microcystins (MCs) produced during the formation of harmful cyanobacterial blooms. Geosmin (GSM) and 2-methylisoborneol (MIB) may also be produced during cyanobacterial blooms and can taint water causing undesirable taste and odor. The photocatalytic degradation of MC-LR, GSM, and MIB in water under both UV-A and solar light in the presence of reduced graphene oxide−TiO2 composite (GO− TiO2) was studied. Two commercially available TiO2 materials (Degussa P25 and Kronos) and a reference TiO2 material prepared in the laboratory (ref-TiO2) were used for comparison. Under UV-A irradiation, Degussa P25 was the most efficient photocatalyst for the degradation of all target analytes followed by GO−TiO2, ref-TiO2, and Kronos. Under solar light irradiation GO−TiO2 presented similar photocatalytic activity to Degussa P25, followed by Kronos and ref-TiO2 which were less efficient. Intermediate products formed during the photocatalytic process with GO−TiO2 under solar light were identified and were found to be almost identical to those observed by Degussa P25/UV-A. Assessment of the residual toxicity of MC-LR during the course of treatment with GO−TiO2 showed that toxicity is proportional only to the remaining MC-LR concentration. The photocatalytic performance of GO−TiO2 was also evaluated under solar light illumination in real surface water samples, and GO−TiO2 proved to be effective in the degradation of all target compounds.

1. INTRODUCTION The presence of cyanobacteria causes many water-quality concerns, since some of them can potentially produce toxins called cyanotoxins and off-odor compounds.1 Microcystins (MCs) are the most widespread cyanotoxins that are present in diverse aqueous environments.2,3 MCs in drinking water can cause acute and chronic toxicity to humans.4 They can also cause mortality, loss of production, and decrease in productivity in aquaculture and have the potential to harm consumers through the food-web, via accumulation in fresh-water fish.5 These are cyclic heptapeptides consisting of five invariant and two variant protein amino acids.2,6 About 89 MC variants have been identified so far, with microcystin-LR (MC-LR) being the most common and most toxic variant (Supporting Information, Figure S1a).7 The provisional limit for MC-LR in drinking water, set by the World Health Organization (WHO) is 1 μg L−1.8 The most commonly occurring off-odor compounds produced by eutrophication and algal blooms are geosmin (GSM) (Supporting Information, Figure S1b) and 2-methylisoborneol (MIB) (Supporting Information, Figure S1c).9,10 © XXXX American Chemical Society

Even though they are considered nontoxic, they have strong earthy-muddy (GSM) and musty (MIB) odors that are the reasons for the waterworks to receive complaints by the consumers.11 These compounds also cause serious problems and revenue losses in aquaculture-fisheries, through accumulation in fish-tissues that results in unacceptable off-flavours.12 GSM and MIB have very low odor threshold concentrations in water (9 and 4 pg mL−1, respectively).13,14 Treatment processes are required in order to degrade or remove MC-LR, GSM, and MIB released into water during cyanobacterial bloom events. Coagulation, filtration, chlorination, ozonation, activated carbon, and certain chemical oxidation technologies have been tested for the removal of MCs from water, with different removal extent.15,16 Studies Special Issue: Recent Advances in Nanotechnology-based Water Purification Methods Received: January 31, 2013 Revised: May 31, 2013 Accepted: June 5, 2013

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dx.doi.org/10.1021/ie400382r | Ind. Eng. Chem. Res. XXXX, XXX, XXX−XXX

Industrial & Engineering Chemistry Research

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in inert atmosphere.40 These GO−TiO2 composites outperformed the Degussa P25 catalyst for the degradation of both methyl orange azo-dye and diphenhydramine, an important pharmaceutical water pollutant, under a GO loading of 3.3−4.0% wt, where optimal assembly and interfacial coupling between the reduced GO sheets and TiO2 nanoparticles was attained.40 The aim of this study was to investigate the photocatalytic activity of a GO−TiO2 composite photocatalyst for the degradation of target analytes (MC-LR, GSM, and MIB) in water, under UV-A and solar light irradiation. Commercially available Degussa P25, Kronos, and reference-TiO2 (ref-TiO2) nanocatalysts were used for comparison. A study of the reaction mechanism was also carried out, through identification of intermediate products formed during the photocatalytic degradation of MC-LR using GO−TiO2 under solar light irradiation. Assessment of the residual toxicity was also carried out during the course of photocatalysis.

have shown that GSM and MIB are generally resistant to conventional water treatment, including common disinfectants and oxidants such as ozone, chlorine dioxide, and potassium permanganate.17−19 Previous studies have demonstrated that titanium dioxide (TiO2) photocatalysis can effectively degrade both cyanotoxins as well as off-odor compounds in aqueous solutions.20−28 Heterogeneous TiO2 photocatalysis has been considered as a very promising advanced oxidation process (AOP), which in combination with solar energy could effectively address the ever increasing concerns for pollution abatement and water purification. The process efficiency is based on the ability of TiO2 in the photoinduced generation of highly reactive oxygen species upon illumination with UV light. In specific, hydroxyl radicals are produced that can nonselectively attack most recalcitrant organic pollutants leading to their mineralization with no harmful end products when applied at optimum conditions.29,30 Despite the relatively high reactivity of TiO2, the overall efficiency and its performance in solar light photocatalytic applications is essentially hindered by the relatively low quantum yield of TiO2, meaning the ratio of the quantity of reactant molecules consumed or the product molecules formed during the photocatalytic reaction with respect to the quantity of absorbed photons at a given wavelength. This is determined by the competition of interfacial charge transfer with charge recombination of the photogenerated electron−hole pairs as well as by the wide band gap of TiO2 (3.0−3.2 eV) that allows photoexcitation only in the UV range.29−31 Heterostructures of TiO2 with other technologically relevant materials are considered as a promising strategy to improve photocatalytic efficiency of TiO2 by inhibiting electron−hole recombination and enhancing its light harvesting ability by coupling with visible light absorbing materials. Among the diverse nanocomposite photocatalysts that are currently investigated,32 a combination of TiO2 with carbonaceous materials has been attracting considerable attention, owing to the unique texture and adsorption capacity of carbon nanomaterials along with their advantageous optoelectronic properties.33,34 Graphene and its derivatives have recently emerged as one of the most promising candidates for the development of efficient composite photocatalysts, because of their exceptional charge carrier mobility and electrical and thermal conduction as well as large specific surface area and high transparency.35−37 In particular, graphene oxide (GO) provides a highly functional substrate with abundant anchoring sites for efficient binding with TiO2, whose electronic properties can be further tailored toward those of pristine graphene by judicious thermal and/or chemical reduction.38 Several studies have been focused on the development of tailored graphene-based-TiO2 composite photocatalysts employing different synthetic routes that establish GO as a highly adsorptive substrate.37 The GO− TiO2 composite photocatalysts exhibit systematically enhanced photocatalytic activity that is mainly related to the scavenging and subsequent transport of photogenerated electrons by GO after excitation in the conduction band of TiO2 by UV illumination, promoting thus charge separation as well as the enhanced capacity of the composites for the physical and chemical adsorption of pollutant molecules.39 However, performance evaluation of the GO−TiO2 composites has been limited, in most cases, only to the photocatalytic degradation of dyes.37 Recently, reduced GO−TiO2 composite photocatalysts were prepared using the liquid phase deposition method and subsequent postreduction upon thermal treatment

2. EXPERIMENTAL SECTION 2.1. Materials. Synthesis of the GO−TiO2 composite was performed using the liquid phase deposition method followed by post-thermal treatment at 200 °C under N2 flow as described elsewhere.40 On the basis of our previous studies, the optimal GO loading of 4.0% wt in TiO2 was used.40 The refTiO2 nanopowder was prepared using the same method but without the addition of graphene oxide, while thermal treatment was applied under the same conditions (N2, 200 °C). Degussa P25 (Degussa AG, Germany) and Kronos (Kronos Titan GmbH, Germany) were used as standard materials for comparison purposes. MC-LR (>95%) was purchased from Abraxis, USA. GSM (98.0%) and MIB (99.8%) were purchased by Wako Pure Chemical Industries, Ltd. High purity oxygen was used for oxygenation of the solutions. Water was purified with a Millipore Milli-Q Plus System. 2.2. Instrumentation. Irradiation with UV-A (λmax = 365 nm) was performed with a laboratory constructed illumination box equipped with four F15W/T8 black light tubes (Sylvania GTE, USA), emitting 71.7 mW cm−2 at a distance of 25 cm. An Oriel photolysis apparatus (Photomax) equipped with a 150 W Xe arc lamp was used as the source for solar light irradiation. A cool water circulating liquid filter is used to absorb the near IR radiation. Finally an Oriel AM1.5 G air mass filter is used to correct the output of the lamp to approximate the solar spectrum when the sun is at a zenith angle of 48.2°. The light intensity was measured to be 115 mW cm−2 by a power meter (Ealing Electro-Optics). The HPLC apparatus used consisted of a Waters (Milford, MA, USA) model 600E pump connected to a Waters model 600 gradient controller, a Rheodyne (Cotati, CA, USA) model 7725i sample injector equipped with 20 μL sample loop, and a Waters model 486 tunable absorbance detector, controlled by the Millenium (Waters) software. The GC−MS system used was an Agilent 6890 series gas chromatograph interfaced to an Agilent 5973 mass selective detector. The LC−MS/MS system used was a Thermo Finnigan (San Jose, USA) consisting of a Thermo Surveyor LC pump, a Thermo Surveyor AS autosampler, and a TSQ Quantum Discovery MAX triple quadruple mass spectrometer equipped with an electrospray ionization (ESI) interface operating in the positive ionization mode. Xcalibur software 1.4 was used to control the mass spectrometric conditions and for data B



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LC−MS/MS for MC-LR intermediates identification was carried out using a Kromasil 100−5C18 (5 μm, 150 mm × 2.1 mm) reversed-phase LC column. Acetonitrile (A) and highpurity water (B), both containing 0.1% HCOOH, were the mobile phase solutions, and gradient elution was programmed from 15 to 25% of acetonitrile in 10 min, followed by an increase to 40% in 10 min and to 80% in the next 15 min.43 Flow rate was set at 0.2 mL min−1, and the injection volume was 50 μL, using a full loop injection. MC-LR eluted at 25.9 min. 2.4. Photocatalytic Experiments. In a typical experiment for MC-LR degradation, 5 mL of aqueous MC-LR solution (10 mg L−1) containing 200 mg L−1 of the photocatalyst (GO− TiO2, ref-TiO2, Degussa P25, or Kronos) were added to a cylindrical pyrex cell, oxygenated for 20 minutes and covered air tightly with a serum cap. Illumination was carried out at 25 °C in the photolysis apparatus under constant stirring. In the case of GSM and MIB, the same experimental procedure was used with the volume of aqueous solution being 20 mL, spiked with GSM or MIB to give a concentration of 1 mg L−1. The observed rate constants were calculated from the trace of the variation of the concentration of substrates divided by their initial concentration with time for the first 30% of the reaction (Figure 1−6) and are roughly within 20%. For the identification of MC-LR intermediates, a solution of 12 mL containing 10 mg L−1 of MC-LR and 200 mg L−1 of the photocatalyst (Degussa P25 and GO- TiO2), was irradiated and the samples were taken at certain time intervals during the process. Samples were then filtered and analyzed by LC−MS/ MS. The pH of the solutions was monitored during photocatalysis and ranged from 5.6 to 6.3. 2.5. Toxicity Measurements. Residual toxicity associated with MC-LR was assessed by the protein phosphatase inhibition assay (PPIA) using the MicroCystest kit (ZeuImmunotec S.L., Spain) in 96-well microtiter plate format according to manufacturer’s instructions. A Tecan Sunrise microplate reader was used for measurements of OD at 410 nm (Tecan Group Ltd., Switzerland). PPIA was developed on the basis of the ability of MCs to inhibit serine and threonine phosphatase enzymes.44 The extent of inhibition of these enzymes is associated to hepatotoxicity and tumor promotion. The PPIA colorimetric assay is fast and easy to use and provides important toxicological information regarding the bioactivity of MCs, since detection is based on functional activity rather than on recognition of chemical structure.

acquisition. Detection was carried out in full scan mode (300− 1200 m/z). Mass axis calibration was performed by infusion of a polytyrosine-1,3,6 standard solution at 5 μL min−1. Highpurity nitrogen was used as sheath and auxiliary gas, and argon was used as collision gas. Sheath gas was set at 20 arbitrary units (au), auxiliary gas was set at 5 au, and spray voltage was 5 kV. Capillary temperature was set at 350 °C and collision pressure was 1.5 mbar. Collision energy and tube lens offset were optimized for MC-LR. For full scan MS/MS spectra, the selected precursor ions were isolated with an isolation width of 1 Da and product ions were formed with normalized collision energy of 30. 2.3. Analytical Procedures. The concentration of MC-LR during the degradation process was monitored by HPLC. Acetonitrile (A) and water (B) both containing 0.05% TFA were the elution solvents. An Agilent Eclipse XDC-C18 analytical column (15 cm × 4.6 mm ID, 3.5 μm) was used, and the gradient elution program was as follows: 35% A−65% B at 0.00 min, 70% A at 2.00 min, 100% A at 2.10 min, 0% A at 3.00 min, 35% A at 3.10 min, at a flow rate of 1.2 mL min−1.22,41 Injection volume was 20 μL. Detection was at 238 nm. Before analysis, solutions were filtered with Millex PVDF Durapore-GF 13 mm 0.22 μm, low protein binding filters. Filters were tested under three different concentrations of MCLR (1, 5, and 10 ppm) and in all cases over 98% of the initial toxin concentration was extracted. Experiments were performed in triplicate, and the error bars on Figures 1−6 represent the meant ± SD of the three separate measurements.

Figure 1. Photocatalytic degradation of 10 mg L−1 of MC-LR under UV-A (λmax = 365 nm) irradiation in the presence of different TiO2 based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO−TiO2, and ref-TiO2).

3. RESULTS AND DISCUSSION 3.1. Photocatalytic Degradation of MC-LR and OffOdor Compounds by TiO2 Based Nanomaterials under UV-A Light. Illumination of an aqueous solution of MC-LR under UV-A irradiation (λmax = 365 nm) in the presence of Degussa P25, Kronos, GO−TiO2, and ref-TiO2 nanomaterials resulted in the photodegradation of the cyanotoxin (Figure 1). Experiments performed in the absence of photocatalysts indicated that the contribution of photolysis is negligible since no degradation was observed. These results are in agreement with those reported in a previous study concerning commercial Degussa P25.20,22 Experiments performed concerning adsorption of MC-LR on the catalysts’s surface showed that an adsorption of 25% was noticed on the GO−TiO2, followed by Kronos, ref- TiO2, and Degussa P25, with 11%, 8%, and 5%, respectively. After the first hour of stirring in the dark,

GSM and MIB were monitored by headspace solid phase microextraction (HS-SPME) followed by gas chromatography− mass spectrometry (GC−MS).42 Samples of 2 mL were placed in screw-capped headspace vials with PTFE-lined silicone septa. Sodium chloride (750 mg) and a magnetic stirrer were added, the SPME fiber (Polydimethylsiloxane, 100 μm, Supelco) was inserted, and the vial was placed for extraction at 70 °C for 30 min under stirring. A HP-5 MS capillary column (30 m × 0.25 mm × 0.25 mm film thickness) was used with a temperature gradient program from 50 °C (held for 1 min) to 250 °C (held for 6 min), using a temperature ramp (12 °C min−1) under constant flow (1 mL·min−1). Detection was in selected ion monitoring (SIM) mode at m/z: 112 (GSM) and 95 (MIB), respectively. C



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As can be seen in Figures 2 and 3, under UV-A irradiation all photocatalysts were effective against GSM and MIB. Once again Degussa P25 was the most effective photocatalyst for both compounds with complete degradation taking place after 20 min of irradiation. The rest of the photocatalysts showed almost the same behavior for both compounds. Degradation of GSM was 93%, 75%, and 73% and of MIB was 90%, 75%, and 74% for Kronos, GO−TiO2, and ref-TiO2, respectively. Under the experimental conditions used, the observed rate constants (k, ×10−3) of GSM were 25, 3.4, 2.6, and 4.7 min−1, and of MIB were 27, 5.9, 4.6, and 3.0 min−1 for Degussa P25, GO−TiO2, ref-TiO2, and Kronos, respectively. 3.2. Photocatalytic Degradation of MC-LR and OffOdor Compounds by TiO2 Based Nanomaterials under Solar Light. As discussed in the previous section (3.1), all tested TiO2-based photocatalysts exhibit remarkable efficiency in photocatalytic degradation of the target compounds, however, requiring high cost UV radiation. Activation of TiO2 can facilitate the development of promising processes for the remediation of contaminated water resources using solar light replacing costly facilities for generation of UV light. The GO−TiO2 photocatalyst used in this study absorbs in the whole visible region of the spectrum.40 The band gap narrows upon addition of graphene oxide to TiO2 due to the chemical bonding between TiO2 and the specific sites of the carbon face (Ti−O−C bond).40 For this reason, the GO−TiO2 photocatalyst was used for the degradation of target analytes under solar light irradiation. The illumination apparatus employed, provided a very close spectral match to solar spectra offering significant advantages such as reproducible experimental conditions and control of the local environmental parameters. Under these experimental conditions, the GO−TiO2 material exhibited high photocatalytic activity, similar to that of Degussa P25, followed by Kronos and ref-TiO2 (Figure 4, 5, and 6) for MC-LR, GSM, and MIB, respectively. The observed rate constants (k, ×10−3) followed the order: (I) MC-LR: Degussa P25 15.3 min−1 > GO−TiO2 8.7 min−1 > Kronos 7.7 min−1 > ref-TiO2 0.3 min−1, (II) GSM: Degussa P25 12.6 min−1 > GO−TiO2 10.1 min−1 > Kronos 2.5 min−1 >

adsorption in the solutions came to equilibrium (Supporting Information, Figure S2). As can be seen in Figure 1, Degussa P25 was found to be the most effective for MC-LR degradation followed by GO−TiO2 and ref-TiO2 that exhibited similar photocatalytic performance. Kronos was found to be the least effective of all nanocatalysts tested. Under these experimental conditions, observed rate constants (k, × 10−3) were 25.1, 22.6, 23.1, and 5.9 min−1 for Degussa P25, GO−TiO2, ref-TiO2, and Kronos, respectively. In all cases, after 20 min of irradiation almost complete destruction of the cyanotoxin was observed by all photocalysts (100% with Degussa P25, 95% with ref-TiO2, 94% with GO− TiO2, and 89% with Kronos), as shown in Figure 1. As far as concerning GSM and MIB, illumination under UVA in the presence of different TiO2 based nanostructured materials (Degussa P25, Kronos, GO−TiO2, and ref-TiO2 nanocomposites) resulted in photodegradation of both substrates (Figures 2 and 3, for GSM and MIB, respectively).

Figure 2. Photocatalytic degradation of 1 mg L−1 GSM under UV-A (λmax = 365 nm) irradiation in the presence of different TiO2-based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO− TiO2, and ref-TiO2).

Figure 3. Photocatalytic degradation of 1 mg L−1 MIB under UV-A (λmax = 365 nm) irradiation in the presence of different TiO2-based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO− TiO2, and ref-TiO2).

Results showed that photolysis in the absence of photocatalysts is negligible. Results for Degussa P25 agree with those reported in another study.25 Adsorption percentages of both GSM and MIB were lower than the errors associated with their detection suggesting that they had negligible adsorption on all photocatalysts used.

Figure 4. Photocatalytic degradation of 10 mg L−1 of MC-LR under solar light (AM 1.5 G) irradiation in the presence of different TiO2 based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO−TiO2, and ref-TiO2). D



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As far as the commercial photocatalyst, Kronos, from which GO−TiO2 was proven to be better, is a C-doped visible light activated material which is currently used for industrial purposes (i.e., air purifying paint). C-doping produces new energy states deep in the TiO2 band gap involving substitution of oxygen by carbon atoms, which are responsible for the visible light absorption.48,49 For that reason, it is effective in solar light which is mostly constituted by visible light. 3.3. MC-LR Intermediates Produced Under UV-A and Solar Light. Even though employing TiO2 photocatalysis has been proven to be very useful and successive for the degradation of organic pollutants in aquatic environment, the elucidation of the degradation pathway and the determination of intermediate products is also necessary for the verification of detoxification. So far, a number of studies have examined degradation pathways of MC-LR when conventional oxidants or AOPs are applied, including ozonation,50,51 chlorination,52 ultrasonication,53 photolysis,54 TiO2/UV-A,43,55−57 and NTiO2/UV-A.28 The fact that analytical standards for the MCLR reaction intermediates are not commercially available complicates the identification of primary intermediates.16,58 In his study, identification of intermediate products formed during the photocatalytic degradation of MC-LR using GO−TiO2 under solar light and Degussa P25 under UV-A was carried out using LC−MS/MS. The majority of byproducts detected were produced within the first 2 min of irradiation. The concentration of most of the byproducts during photocatalysis initially increased followed by a decrease over time, due to their subsequent oxidation. In this study, structural characterization of intermediates produced during photocatalysis of MC-LR was based on the analysis of LC−MS chromatograms and the respective mass spectrum. Although many of the intermediates that were identified were already known,55,57,59 a number of new intermediates were observed (m/z: 313.5, 368.5, 389, 411.5, 417, 437, 457, 515.5, 544, 781.5, 980.5 and 1031.5) and possible structures are proposed (Supporting Information, Table S1) (Supporting Information, Figures S4−S6). The majority of intermediates detected under UV-A and solar light irradiation were the same, since photocatalysis under solar light is mainly due to the UV part of the spectrum. Chromatograms resulted from photocatalytic degradation of MC-LR are presented in Figure 7a for Degussa P25 under UVA irradiation (0−15 min) and in Figure 7b for GO−TiO2 under solar light irradiation (0−70 min). Table 1 presents all products that were detected during the photocatalytic degradation of MC-LR under UV-A and solar light irradiation, their retention times (Rt), molecular weight (MW), formulas, and possible chemical structures. MC-LR consists of seven amino acids, 3-amino-9-methoxy2,6,8-trimethyl-10-phenyl-4,6-decadienoic acid (Adda), isoglutamic acid (Glu), methyl dehydroalanine (Mdha), D-alanine (Ala), L-leucine (Leu), D-methylaspartic acid (MeAsp), and Larginine (Arg), and it can be denoted as Cyclo[-Adda-GluMdha-Ala-Leu-MeAsp-Arg-].6 One of the most intense peaks observed (higher peak area in relative abundance) corresponded to a product at m/z 1029 with a mass spectrum showing a molecular ion (M + H)+. This product is generated by hydroxyl radical attack at either double bond C4 or C6 on the conjugated diene structure system, of the Adda chain [Adda(OH)2], resulting in double hydroxylation of MCLR.43,53−55,57 In a relative abundance chromatogram (Supporting Information, Figure S3), multiple peaks for m/z 1029 appeared, suggesting that except for C4−C5 and C6−C7

Figure 5. Photocatalytic degradation of 1 mg L−1 GSM under solar light (AM 1.5 G) irradiation in the presence of different TiO2 based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO− TiO2, and ref-TiO2).

Figure 6. Photocatalytic degradation of 1 mg L−1 MIB under solar light (AM 1.5 G) irradiation in the presence of different TiO2 based nanostructured materials, 200 mg L−1 (Degussa P25, Kronos, GO− TiO2, and ref-TiO2).

ref-TiO2 0.3 min−1, and (III) MIB: Degussa P25 9.6 min−1 > GO−TiO2 5.1 min−1 > Kronos 1.7 min−1 > ref-TiO2 0.4 min−1. After the first hour of irradiation, Degussa P25 achieved complete degradation of MC-LR, followed by GO−TiO2, Kronos, and ref-TiO2 with 97%, 95%, and 18% degradation, respectively. Accordingly, the photocatalytic degradation of GSM after the first hour of irradiation was 100%, 99%, 92%, and 23% and for MIB degradation was 100%, 100%, 86%, and 25% for Degussa P25, GO−TiO2, Kronos, and ref-TiO2, respectively. The improved performance of Degussa P25 can be attributed to its mixed-phase (anatase and rutile). Because of the smaller band gap of rutile the useful range of photoactivity into the visible region is extended. In addition, electron transfer from rutile to anatase enables charge separation and the small size of the rutile crystallites facilitates this transfer, making catalytic hot spots at the rutile/anatase interface.45 The observed enhancement of the photocatalytic activity of GO−TiO2 compared to ref-TiO2 could be attributed to the interfacial charge transfer process that can effectively inhibit electron−hole recombination as well as the enhanced capacity of the GO−TiO2 composite for the physical and chemical adsorption of pollutant molecules (Supporting Information, Figure S2).40,46,47 E



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triple hydroxylation of MC-LR (one on the aromatic ring and two on the Adda chain or one on the aromatic ring and two on the side chain of the toxin between Mdha and Ala). The observation of intermediate at m/z 965 (M+Na+) is consistent with linearization of MC-LR, after cleavage (−C3O) on the side chain of the toxin between Mdha and Ala.55 After production of m/z 965, the generation of product at m/z 999.5 (M+Na)+ takes place through dihydroxylation on the Adda subsequent bonds.53,57 Further oxidation could result to a ketone with m/z 783.5. A product with m/z 965 could also result from abstraction of the methoxy group from the Adda chain [Adda(-Methoxy)]. Upon addition of amino group, a new observed product at m/z 980.5 could be formed. Products reported in Table 1, with m/z < 781.5 are observed for the first time and could be oxidation products of those with higher m/z. For example products at m/z 315.5, 368.5, and 411.5, could be formed after oxidation of product at m/z 1045.5. 3.4. Toxicity assessment. As far as drinking water treatment is concerned for the decontamination of water from MC-LR or other microcystins, an important question is raised: At what stage of treatment does the water become detoxified? Meaning, is degradation of the initial compound sufficient to remove the toxic activity, or complete mineralization is needed? The answer to this question is of major importance not only for water safety but also for the efficiency and cost-effectiveness of the treatment process, especially when intended for use in large-scale applications. In an attempt to answer this, the residual toxicity of water during the course of the photocatalytic degradation of MC-LR was studied using the protein phosphatase inhibition assay (PPIA). PPIA measurements that were carried out using two photocatalysts (GO−TiO2 and Degussa P25) showed that residual toxicity was directly proportional only to the amount of MC-LR that remained intact into solution (Figure 8 and 9 under UV-A and solar light, respectively). Reduction of MC-LR concentration resulted in reduction of a directly proportional amount of the toxic activity. Moreover, in solutions were MCLR was completely degraded, no toxic activity was observed, even though those solutions contained oxidation byproducts. This implies that MC-LR loses its toxic activity (protein phospatase inhibition) as soon as the molecule is transformed to oxidized products. This is in agreement with previously reported studies25 where it was shown that hydroxyl radical attack on the Adda amino acid of MC-LR is the first oxidation step and results in loss of toxic activity. This finding is very important for real applications of the photocatalytic process, since it denotes that the target of the process could be degradation rather than mineralization, and therefore less energy would be needed for water detoxification. 3.5. Application in Real Water Samples. To evaluate the GO−TiO2 nanocomposite photocatalytic performance in the presence of the natural constituents of water, experiments with surface water were carried out, using solar light irradiation. Surface waters that were collected from two lakes of Greece that also serve as water reservoirs for the population of Athens (Mornos Lake and Marathonas Lake), were used as natural matrices. The basic physicochemical parameters of these waters are shown in Table 2. Water samples were spiked with known concentrations of MC-LR, MIB, and GSM at concentrations of 10 mg L−1, 1 mg L−1, and 1 mg L−1, respectively.

Figure 7. Chromatograms resulted from MC-LR photocatalytic degradation using (a) Degussa P25 under UV-A irradiation and (b) GO−TiO2 under solar light irradiation.

dihydroxy addition, geometrical isomers of dihydroxy-MC-LR could be deduced, which was also suggested by Antoniou et al., 2008.60 Further oxidation of dihydroxylated MC-LR with cleavage of the dihydroxylated bond at positions C4−C5 or C6− C7 on the Adda chain, results in products with m/z 795 (aldehyde intermediate) and m/z 835 (ketone intermediate), respectively. Further oxidation of product m/z 795 forms m/z 811 intermediate, consistent with a carboxylic acid structure. A new intermediate observed at m/z 1031.5 could be possibly formed from double hydration of the double bonds of Adda [Adda(OH2)2] or one hydration on the Adda chain and another one on the Mdha chain [Mdha(OH2)]. Also, m/z 1029 product could result from double hydroxylation of the double bond on the chain of Mdha [Mdha(OH)2]. Consecutive oxidation leads to the formation of an aldehyde (m/z 1011.5)43,53,55 and cleavage on the C′CO bond results to the m/z 1015.5 product.55 Another multiple peak observed was that at m/z = 1011.5 (Supporting Information, Figure S3). There are different possible pathways for the formation of intermediates with this molecular ion. One possibility is a hydroxyl substitution of the hydrogen at C7 to form enol-MC-LR [Adda(O)] or on the Mdha [Mdha(O)], which rapidly isomerizes to a more stable tautomer of ketone-MC-LR.59 Another possibility is a hydroxyl substitution on aromatic hydrogen (o-, p-, and to a lesser extent the m-hydroxylated product). A second hydroxylation of the aromatic ring follows, yielding m/z 1027.543,53,55 intermediate (explaining multiple peaks), (Supporting Information, Figure S3). Demethoxylated-MC-LR on the methoxy group of Adda, through the formation of the formic acid ester results in intermediate at m/z = 1009.5 (double peak, E-Z isomers),55 (Supporting Information, Figure S3). Another intermediate observed with multiple peaks at m/z = 1045.5,53 consists of F



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Table 1. Products Observed from MC-LR Degradation Using Degussa P25/UV-A and GO−TiO2/Solar Light Irradiation no.

peak (m/z)

Rt (min)

MW and formula

1 2 3 4 5

995.5 313.5 368.5 389.5 411.5 417

25.9 38.1−42.6 21.2−25.8 5.3− 6.1 4.8, 6.4 4.7- 6.1

6

437

9.4

7 8 9 10 11 12 13 14

457 515.5 544 781.5 783.5 795 811.5 835.5

9.0 20.3 21.5−23.8 6.4 5.1 4.8−6.1 4.8 9.1

C49H74N10O12, 994.5 C16H24O6, 312.2 C20H33NO5, 367.2 C15H28N6O6, 388.2 C22H38N2O5, 410.3 C17H32N6O6, 416.2 C18H32N4O7, 416.2 C17H30N6O6Na, 414.2(23) C20H36N6O6, 456.2 C21H37N7O8, 515.3 C23H41N7O8, 543.3 C34H56N10O11, 780.4 C33H54N10O12, 782.4 C34H54N10O12, 794.4 C34H54N10O13, 810.4 C37H58N10O12, 834.4

15

837.5

6.2, 9.0

C36H56N10O13, 836.4

16

965

28.7

17 18 19 20

980.5 999.5 1009.5 1011.5

26.0 26.2 24.0−25.2 21.4−25.7

C48H72N10O11, 964.5 C46H74N10O11Na, 942.5(23) C48H75N11O11, 979.5 C48H74N10O13, 998.5 C49H72N10O13, 1008.5 C49H74N10O13, 1010.5

21 22 23

1015.5 1027.5 1029

26.0 22.6−26.4 20.3−22.1

C48H74N10O14, 1014.5 C49H74N10O14, 1026.5 C49H76N10O14, 1028.6

24

1031.5

21.9−22.7

C49H78N10O14, 1030.6

25

1045.5

20−27

C47H77N10O15, 1044.6

possible structure

catalyst

MC-LR: Cyclo [-Adda-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Dihydroxy-7-(hydroxy-phenyl)-6-methoxy-3,5-dimethyl-heptanoic acid OH-Adda(H2O)2 H-Arg-NHCH(OH)CH(CH3)CO-Glu-H OH-Adda(H2O)2-NHCH2CH3 OH-Arg-MeAsp-Leu-H H-MeAsp-Leu-Ala-Mdha(OH)-H

TiO2, GO−TiO2 GO−TiO2 TiO2, GO−TiO2 GO−TiO2 TiO2, GO−TiO2

[H-Arg-NHCH(CHO)CH(CH3)CO-Glu-CH3]−Na+

TiO2, GO−TiO2

H3C-Arg-MeAsp-Leu-COCH3 Arg-MeAsp-Leu-Ala-COOH Arg-MeAsp-Leu-Ala-COCHOHCH3 Cyclo[-NHCH(CH3)CH(CH3)CO-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-NHCHOHCH(CH3)CO-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-NHCH(CHO)CH(CH3)CO-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-NHCH(COOH)CH(CH3)CO-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-NHCH(CHCHCOCH3)CH(CH3)CO-Glu-Mdha-Ala-Leu-Me Asp-Arg-] Cyclo[-NHCH(CHCHCOOH)CH(CH3)CO-Glu-Mdha-Ala-Leu-Me Asp-Arg-] Cyclo[-Adda(−Methoxy)-Glu-Mdha-Ala-Leu-MeAsp-Arg-] [H3CNH-GluAdda-Arg-MeAsp-Leu-Ala-H]−Na+

TiO2, TiO2 TiO2, TiO2, TiO2, TiO2, TiO2 TiO2,

Cyclo[-Adda(H2N)(−Methoxy)-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda-Glu(−Carboxy)-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-DmAdda-Glu-Mdha-Ala-Leu-MeAsp-Arg-] (OH)-Cyclo[-Adda-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda(O)-GluMdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda-Glu-Mdha(O)-Ala-Leu-Me Asp-Arg-] (CO)Ala-Leu-MeAsp-Arg-Adda-Glu(NCOCH3) (OH)2-Cyclo[-Adda-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda(OH)2-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda-GluMdha(OH)2-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda(OH2)2-Glu-Mdha-Ala-Leu-MeAsp-Arg-] Cyclo[-Adda(OH2)Glu-Mdha(OH2)-Ala-Leu-MeAsp-Arg-] OH-Cyclo[-Adda(OH)2-Glu-Mdha-Ala-Leu-MeAsp-Arg-] OH-Cyclo[-AddaGlu-Mdha(OH)2-Ala-Leu-MeAsp-Arg-]

GO−TiO2 TiO2, GO−TiO2 TiO2, GO−TiO2 TiO2, GO−TiO2

GO−TiO2 GO−TiO2 GO−TiO2 GO−TiO2 GO−TiO2 GO−TiO2

TiO2 TiO2, GO−TiO2

TiO2, GO−TiO2 TiO2, GO−TiO2 TiO2, GO−TiO2 TiO2, GO−TiO2 TiO2

Figure 9. Residual toxicity measured during the photocatalytic degradation of MC-LR (10 mg L−1) solar light (AM 1.5 G) irradiation in the presence of Degussa P25 and GO−TiO2 (200 mg L−1).

Figure 8. Residual toxicity measured during the photocatalytic degradation of MC-LR (10 mg L−1) under UV-A (λmax = 365 nm) irradiation in the presence of Degussa P25 and GO−TiO2 (200 mg L−1).

The observed rate constants (k, ×10−3) for MC-LR, GSM, and MIB were 5.3, 3.2, and 5.7 min−1, respectively, for Marathonas Lake, and 4.5, 2.3, and 3.7 min−1 for Mornos Lake, respectively. Although these rate constants were generally lower than those of ultrapure water, results showed that GO−TiO2 remains an effective photocatalyst even in natural waters which

Irradiation of samples was carried out with solar light and GO−TiO2 (200 mg L−1) was used as the photocatalyst. As shown in Figure 10 and 11, all pollutants were removed from spiked natural water solutions, similarly to the experiments that were carried out in ultrapure water. G



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act as scavengers of the radical species produced, also reducing the initial degradation rates.61

Table 2. Physicochemical Parameters of Surface Water Samples (Before Spiking) parameter

Marathonas Lake

Mornos Lake

pH dissolved organic carbon (mg L−1) total alkalinity (mg CaCO3 L−1) conductivity (mS) total hardness (mg L−1) turbitity (NTU)

8.2 2.5 123 386 169 1.7

8.1 1.4 132 304 145 1.5

4. CONCLUSIONS In this work the photocatalytic efficiency of synthesized GO− TiO2 was evaluated for the degradation the hepatotoxic MC-LR and the off-odor compounds GSM and MIB in water. Under UV-A irradiation Degussa P25 was found to be the most efficient in degradation of all target compounds followed by GO−TiO2, ref-TiO2, and Kronos, which exhibited similar photocatalytic performance for GSM and MIB. In the case of MC-LR Kronos was found to have the lowest activity. Under solar light irradiation GO−TiO2 presented similar photocatalytic activity to Degussa P25 followed by Kronos and refTiO2. Furthermore, identification of the intermediate products formed during the photocatalytic degradation of MC-LR by the GO−TiO2 nanocatalyst under solar light irradiation was carried out. The majority of these products were identical to those observed by Degussa P25 under UV-A, suggesting that photodegradation mechanism takes place via a common active species, the hydroxyl radicals. Assessment of the residual toxicity of MC-LR during the course of degradation under UVA and solar light irradiation showed that toxicity is proportional only to the remaining MC-LR in the solution; therefore degradation products present no significant protein phosphatase inhibition activity. In addition, experiments performed using surface water samples have shown that GO−TiO2 is almost as effective as in the case of using ultrapure water spiked with the three target compounds. The results of this study indicate that GO−TiO2 is an effective photocatalyst for the degradation of MC-LR, GSM and MIB in water under UV-A and solar irradiation and appears to be a promising material for water treatment applications.

Figure 10. Photocatalytic degradation of MC-LR (10 mg L−1) under solar light irradiation, using GO−TiO2 photocatalyst (200 mg L−1) in real water samples.

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ASSOCIATED CONTENT

S Supporting Information *

Figure S1, structures of MC-LR (a), GSM (b), and MIB (c). Figure S2. Adsorption of MC-LR (10 mg L−1) under constant stirring in ambient conditions in the dark, in the presence of Degussa P25, ref- TiO2, GO−TiO2, and Kronos (200 mg L−1). Figure S3, LC−MS chromatograms of MC-LR photocatalytic degradation in the presence of Degussa P25 after irradiation with UV-A for 5 min. Figure S4, MS/MS spectrum of the intermediate with m/z 389.5 at Rt 5.80 min. Figure S5, MS/MS spectrum of the intermediate with m/z 437 at Rt 9.44 min. Figure S6, MS/MS spectrum of the intermediate with m/z 1031.5 at Rt 22.08 min. Table S1, showing the proposed structure and molecular formula of a number of new intermediates observed from MC-LR degradation using Degussa P25/UV-A and GO-TiO2/solar light irradiation. This material is available free of charge via the Internet at http:// pubs.acs.org.

Figure 11. Photocatalytic degradation of MIB and GSM (1 mg L−1) under solar light irradiation, using GO−TiO2 photocatalyst (200 mg L−1) in real water samples.

contain natural organic matter and other constituents (Table 2) that may compete with the target pollutants for the reactive oxidative species produced by the photocatalytic process. The results are promising for up-scaling of the process for natural water detoxification/decontamination (e.g., fisheries-aquaculture) as well as for drinking water treatment. These results are in accordance with Pelaez et al. (2011)61 who studied the effects of water parameters on the degradation of MC-LR using TiO2 based photocatalysis. In that study they showed that the solution pH is a major factor influencing the degradation rate, with higher pH values resulting in the reduction of the degradation. As far as concerning alkalinity the main responsible species are bicarbonate ion HCO3−, carbonate ion CO32−, and hydroxide ion OH−. Both HCO3− and CO32− can

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +302106503643. E-mail: [email protected]. Notes

The authors declare no competing financial interest. H



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ACKNOWLEDGMENTS This work was funded by the European Commission (Clean Water−Grant Agreement Number 227017). Clean Water is a Collaborative Project cofunded by the Research DG of the European Commission within the joint RTD activities of the Environment and NMP Thematic Priorities. T. Triantis and T. Fotiou are grateful to NCSR “Demokritos”, Institute of Advanced Materials, Physicochemical Processes, Nanotechnology and Microsystems, for postdoctoral and Ph.D. fellowships. The authors acknowledge COST Action ES 1105 “CYANOCOST- Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management” for adding value to this study through networking and knowledge sharing with European experts in the field. Financial support for this work was partially provided by projects PTDC/AAC-AMB/122312/ 2010 and PEst-C/EQB/LA0020/2011 financed by FEDER through COMPETE and by FCT−Fundacao para a Ciencia e a Tecnologia. L.P.M. acknowledges financial support from SFRH/BPD/88964/2012.

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