Membrane biofouling control using polyvinylidene fluoride membrane blended with quaternary ammonium compound assembled on carbon material

Journal of Membrane Science 539 (2017) 229–237

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Membrane biofouling control using polyvinylidene fluoride membrane blended with quaternary ammonium compound assembled on carbon material

MARK

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Xingran Zhanga, Zhiwei Wanga, , Mei Chena, Jinxing Mab, Shipei Chenc, Zhichao Wua a State Key Laboratory of Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Tongji University, 1239 Siping Road, Shanghai 200092, China b School of Civil and Environmental Engineering, University of New South Wales, Sydney, NSW 2052, Australia c School of Chemical Science and Engineering, Tongji University, 1239 Siping Road, Shanghai 200092, China

A R T I C L E I N F O

A B S T R A C T

Keywords: Antibiofouling Membrane fabrication Membrane separation Polyvinylidene fluoride Wastewater treatment

Widespread applications of membrane technology call for the development of antibiofouling membranes. For the in-situ membrane surface modification, the antibiofouling efficacy is always hindered by the inefficient presence of antimicrobial agents on membrane surface since they are blended with the polymers and distributed into the bulk membrane matrix. In this study, a compatible carbon carrier was adopted to assemble the quaternary ammonium compound (QAC@Carbon) for enhancing its surface segregation of polyvinylidene fluoride (PVDF) microfiltration membranes and simultaneously controlling QAC release, thereby improving the efficiency in mitigating biofouling. The results indicated that carbon carrier was capable of driving surface segregation of QAC without deteriorating the physicochemical properties of membranes. The QAC concentration on surface of the membrane modified by QAC@Carbon (MCQ) was 2.5-fold of membrane blended with QAC alone (MQ). Meanwhile, carbon carrier was capable of improving QAC stability in membrane matrix to ensure a lasting antibiofouling efficacy for engineering applications. Batch tests clearly exhibited that both MCQ and MQ had antibiofouling efficiency, while MCQ membrane under cross-flow filtration demonstrated better antibiofouling behaviors compared to MQ. This is mainly attributed to the reduced accumulation of microbial biomass and improved membrane physicochemical properties (higher permeability and porosity) compared to MQ. These findings highlight the potential of introducing QAC@Carbon into polymeric membranes as an effective strategy for fabricating antibiofouling membranes.

1. Introduction In the last two decades, membrane separation technology, being an important innovation, has been widely used in advanced water and wastewater treatment [1,2]. However, membrane fouling, particularly biofouling due to the undesired attachment of bacteria to membrane surfaces and the subsequent growth of biofilms, is a thorny issue limiting the practical applications of membrane processes [3,4]. A number of approaches have been developed to mitigate biofouling [5–7], such as using low-fouling membrane, optimizing membrane operational conditions (e.g., using a moderate membrane flux) [8], pretreating feed solution (e.g., pre-chlorination) [9] and periodically cleaning membrane [10]. However, the above technologies may be energy-intensive, produce toxic byproducts and require delicate operation [11,12]. Therefore, fabricating anti-biofouling membranes has been recognized

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Corresponding author. E-mail address: [email protected] (Z. Wang).

http://dx.doi.org/10.1016/j.memsci.2017.06.008 Received 9 March 2017; Received in revised form 13 May 2017; Accepted 3 June 2017 0376-7388/ © 2017 Elsevier B.V. All rights reserved.

as a robust, and environmentally-friendly alternative for sustainable water purification. Recent studies on preparation of antibiofouling composite membranes involve graft polymerization/coating on the membrane surface and in-situ membrane modification during fabrication (e.g., blending) [13,14]. The latter may be a good alternative because the introduced antimicrobial agents such as nanomaterials [15,16], biocides [17,18], and antimicrobial polymers [19] may have higher structural stability in membrane matrixes, lower partial blocking of surface pores and thus long-lasting antimicrobial activity. While, compared to the method of graft polymerization/coating, critical concerns remain in the in-situ membrane modification method with regard to the insufficient surface coverage of antimicrobial agents since they are blended with the polymers and distributed into the bulk membrane matrixes [6], recent evidence shows that surface segregation of antibacterial agents during

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macroporous carbon was produced. The purified products (washed in succession with water, 30% HCl and ethanol) were then oxidized by KMnO4 and NaNO3 in concentrated H2SO4 for hydrophilic modification. Ultimately, the dried hydrophilic carbon carrier was mixed with CTAB in DI water (mass ratio of 1:8) and stirred for 12 h, producing QAC@Carbon composite. Morphologies were obtained using a field emission scanning electron microscope (SEM, SU8010, Hitachi, Japan). The thermal behaviors of QAC@Carbon composite were analyzed by differential scanning calorimetry and thermogravimetric analysis (DSCTGA, Netzsch STA409, German) at a heating rate of 10 °C min−1 in air from 20 °C to 800 °C. Fourier-transform infrared (FTIR) spectrometer (Thermo Nicolet 5700) was used for determining the functional groups. The zeta potential of carbon carrier, QAC and QAC@Carbon powders was measured by Zetasizer analyzer (Nano-ZS90, Malvern Instruments Crop., UK) with pH of 7.0 at 25 °C.

membrane fabrication is possible. Segregation can be triggered by the change of entropy and molecular structure and/or the enhancement of exchange rate during phase inversion process, leading to an efficient modification of the surface characteristics whilst exerting minor impacts on bulk properties [6,20–22]. The mechanism of surface segregation is associated with self-organization of the amphiphilic compounds at the water/membrane interface during the phase-inversion process [11,21]. This illuminated us to put forward a hypothesis that the amphiphilic antimicrobial agents assembled on a compatible carrier might enhance their surface segregation and consequently improve the cost-effectiveness in suppressing membrane biofouling, because biofouling is mainly governed by the contact of bacteria with the functionalized membrane surfaces [8,23]. Quaternary ammonium compound (QAC), which has positively charged polyatomic ions of the structure NR4+ with R being alkyl, aryl or aralkyl groups, exhibits efficient antibacterial abilities [24]. In this study, QAC was chosen as a biocide and assembled on negatively charged and hydrophilic carbon (QAC@Carbon) through electrostatic interaction. These assembled antibacterial agents were further incorporated into the polyvinylidene fluoride (PVDF) matrix to prepare the anti-biofouling membranes using a phase inversion method. The objectives of the present work were therefore to elucidate the antibiofouling mechanisms of PVDF membrane modified by QAC@Carbon. Surface segregation of QAC was examined by X-ray photoelectron spectroscopy (XPS). QAC release behaviors were monitored to investigate the stability of the antimicrobial agents incorporated in the modified PVDF membranes. The anti-biofouling properties of the modified membranes were further characterized using model bacterial suspensions in microbial incubation cells and also cross-flow filtration tests. Key questions addressed in the study include: (i) what scenario accounts for the surface segregation inducing an improved surface coverage of biocides, (ii) what about the mechanism in improving the stability of QAC in the membrane, and (iii) what mechanism is likely prevailing for the enhanced anti-biofouling performance of the modified membranes.

2.3. Membrane preparation Membranes used in this study were prepared via an immersion precipitation phase inversion process. The detailed chemical composition for membrane preparation can be found in Supporting Information (SI) Table S1. Briefly, upon drying at 80 °C for 24 h to eliminate the moisture, a predetermined amount of PVDF and PEG were dissolved in DMSO to obtain a homogeneous solution. Meanwhile, a pre-weighed amount of QAC@Carbon was uniformly dispersed in DMSO. Subsequently, the two solutions were mixed and stirred at 80 °C overnight in order to form the homogenous casting solution followed by vacuum degassing for at least half an hour. A casting knife with a clearance of 250 µm was used to spread the casting solution onto non-woven fabrics (Shanghai Tianlue Textile Co., Ltd.) using an Elcometer 4340 motorized film applicator (Elcometer Ltd., U.K.) at an appropriate casting rate (4 cm s−1). These solution films together with the non-woven fabrics were submerged into the coagulation bath (DI water) at room temperature to prepare the porous membranes after shortly (30 s) exposed to ambient air (25 ± 1 °C, 30 ± 5% relative humidity) to allow partial evaporation of the solvents. The resultant QAC@Carbon-blended PVDF membrane was denoted as MCQ. In the meantime, pristine PVDF membrane and membranes separately blended with carbon carrier and QAC were fabricated using the above-mentioned procedures, which served as control membranes and were termed M0, MC, MQ, respectively.

2. Materials and methods 2.1. Reagents Unless specified otherwise, all chemicals and reagents used in this study were of analytical grade and used as received without further purification. Commercial grade PVDF (Solef® 6020, Mw = 670–700 kDa) was used as membrane material obtained from Solvay Corporation. Dimethysulfoxide (DMSO) used as solvents and polyethylene glycol (PEG 600) as a pore-forming additive were purchased from Sinopharm (Shanghai, China). Cetyl trimethyl ammonium bromide (CTAB), a kind of QAC, was purchased from Sigma Aldrich. Sodium chloroacetate was obtained from Aladdin used as the temporary template in the carbon carrier synthesis process. NaClO (∼6%, reagent grade) as a membrane cleaning agent was obtained from Aladdin. 1 M NaOH and 1 M HCl were used for the adjustment of solution pH when necessary. McFarland bacterial suspensions of Gram-negative and Gram-positive bacteria for inoculation were prepared by dispersing the colonies from agar slants (Shanghai Weike) in sterile saline at pH 7. Deionized (DI) water was used in all experiments.

2.4. Membrane characterization Surface hydrophilicity of the membranes was determined by sessile drop contact angle measurement of water on membranes [28]. Water permeability using DI water was measured according to the protocol described previously [29], while membrane volume porosity was determined by a gravimetric method [30]. Each value was shown by averaging triplicate measurements. Membrane morphologies were observed by SEM and atomic force microscopy (AFM, Multimode IV, Bruker Nano Surface, USA) [31]. Surface pore sizes of membranes were calculated by the Image-pro plus 6.0 software (Media Cybernetics, USA). The rejection behaviors of membranes were tested using 1 g L−1 of BSA (Mw=67 kDa, in 10 mM PBS solution, pH=7.4) solution in a dead-end filtration cell (see further details in SI Section S1). X-ray photoelectron spectroscopy measurements (XPS, AXIS UltraDLD, Kratos Analytical Ltd., U.K., using C 1 s = 284.6 eV as a reference) were performed to determine the elemental composition of the membrane surface. Nitrogen distribution along cross-section was detected by EDXmapping (FEI Nova Nano SEM 450, USA). Zeta potential of the membrane surface was measured by a streaming potential analyzer (EKA 1.00, Anton-Paar, Swiss) at a solution ionic strength of 10 mM KCl.

2.2. QAC@Carbon synthesis and characterization Carbon carrier was produced by ultrasonic spray pyrolysis as a continuous, one-step process for the generation of meso- and macroporous carbon powders [25] which were subsequently modified by Hummers method to increase hydrophilicity [26,27]. In brief, the porous carbons were prepared by ultrasonically nebulizing aqueous solutions of sodium chloroacetate into droplets using a humidifier. After the droplets were carried by Ar gas-flow through a furnace, a 230

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Fig. 1. Characterization of QAC@Cabon composite. (A) SEM image of composite. (B) TEM image of composite. The yellow bar represents a length of 500 nm. (C) Zeta potential of carbon carrier, QAC and QAC@Carbon composite (pH=7.0); (D) FTIR spectra identifying the different functional groups of composite; (E) TGA curves for QAC, carbon carrier and QAC@Carbon composite.

shown in SI Section S2) [32,33]. Antibacterial activity of these presoaked membrane coupons were assessed by re-immersing the samples in the solution containing 1 mL of nutrient broth and 10 μL of bacterial suspension. Membrane cleaning tests were also performed to evaluate the stability of QAC during exposure to chemical agents. Membrane coupons were immersed in the 5 vol‰ NaClO solution with different time (from 2 h to 72 h), among which cleaning duration of 72 h satisfied the total maintenance cleaning time (2 h per 1–2 month, 3–6 years of service life) of commercial membranes for engineering applications [34].

2.5. Evaluation of antibacterial behavior and QAC stability After UV sterilization for 30 min, membrane coupons (active surface area = 0.5 cm2) were rinsed with sterile phosphate buffered saline (PBS) (0.01 M, pH = 7.4) thrice. The coupons were then placed in a 24well plate followed by the addition of 1 mL of nutrient broth (Sinopharm) and 10 μL of bacterial suspension (about 107 cells mL−1). Subsequently, the plate was incubated in a dark rotary shaker at 100 rpm at 37 °C. Growth curves of E. coli and S. aureus were measured by quantifying the optical density values of culture solutions at 600 nm (i.e., OD600) using a multi-mode microplate reader (Synergy 4, Bio-Tek Instruments Inc., America). After different incubation times (t = 0, 3, 6, 18, and 24 h), OD600 value was measured and reported by averaging 24 individual tests. Data of the exponential growth phases (3–24 h for E. coli and 6–24 h for S. aureus) was fitted by the pseudo-first-order kinetics equation:

ln

Xt = μt X0

2.6. Membrane biofouling experiments Biofouling experiments were carried out in a closed-loop, cross-flow filtration reactor with an effective volume of 1.44 L. Details about this experimental setup can be found in SI Section S3 and Fig. S2. The active membrane area was 48.0 cm2. Prior to the experiments, the MQ and MCQ membranes were subject to 4-h soaking in sterile DI water to remove loosely bound QAC. A saline containing S. aureus of an initial concentration of 107 cells L−1 was used as a feed solution at pH = 7. The system was operated for 24 h at 50 L m−2 h−1 permeate flux and the temperature maintained at 25 ± 1 °C. At the end of the biofouling experiment, membrane coupons were collected for biofilm characterization. Membrane coupons (1 cm2) were cut from the center of the biofouled membrane, stained with LIVE/DEAD BacLight Bacterial Viability Kits (Molecular Probes, Inc.) and Concavalin A (Con A, Molecular Probes, Inc.) to respectively label viable/dead cells and extracellular polysaccharide (EPS) [35], and mounted in a custom-made chamber for confocal laser scanning microscopy (CLSM, Nikon A1, Japan). Image analysis was performed using NIS-Elements Viewer and Image-pro plus 6.0. Total biovolume was calculated by summing live cells, dead cells, and EPS. Quantitative analysis of the biofilm was also performed by

(1)

where Xt and X0 are the OD600 values representing the bacterial concentrations at t h and 0 h respectively, and μ (h−1) is the specific growth rate. After 24 h of incubation, the membrane coupons were withdrawn and rinsed three times with sterile PBS to remove any nonadhesive or loosely adhesive bacteria. Visualization of the attached bacteria was performed using SEM as described previously. Further tests were performed to verify whether the carbon carrier was capable of improving QAC stability in the membrane matrix (see experimental procedure in SI Fig. S1). In brief, after immersion in sterile water for 4 h to remove any loosely bound QAC, membrane coupons (MQ and MCQ, active surface area = 0.5 cm2) were placed in a 24-well plate soaked in 2 mL deionized water with different times (from 1 h to 20 d). QAC concentration in the suspension was analyzed by the modified Orange II method (the detailed experimental procedure 231

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information of the surface properties. Fig. 1D illustrates the FTIR spectra of QAC, carbon carriers and QAC@Carbon. The FTIR spectra of QAC@Carbon show characteristic peaks of both carbon carriers and QAC, including stretching vibration of the O-H groups (3400 cm−1) and C=O (1720 cm−1) [37], symmetric and asymmetric stretching vibrations of CH2 (2925 and 2850 cm−1) [37] and asymmetric C-H scissoring vibrations of a CH3-N+ moiety in CTAB (1420 cm−1) [38]. The ratio of QAC to carbon in QAC@Carbon composite was evaluated by DSC-TGA from 20 °C to 800 °C. The weight loss of QAC, carbon and QAC@Carbon as a function of temperature is shown in Fig. 1E. It can be observed that QAC@Carbon composite exhibited two distinct weight loss stages. According to TGA analysis, it shows that ~11% of weight loss occurred in stage between 400 and 470 °C, corresponding to the decomposition of the carbon carriers based on the DSC curves of carbon carrier and QAC@Carbon composite (SI Fig. S4B and C). However, about 82% weight loss of composite was found at the temperature less than 400 °C (Fig. 1E), mainly due to the elimination of CTAB revealed by DSC (SI Fig. S4A). Based on the weight loss of the two stages, the corresponding CTAB to carbon carrier mass ratio was calculated to be 7.5, which is roughly consistent with the theoretical value of 8.0.

measuring the total organic carbon (TOC, LipuiTOC trace, Elementar, Germany) extracted from the membrane surface [36]. 3. Results and discussion 3.1. QAC@Carbon characterization QAC@Carbon composite was fabricated through hydrophilic and electrostatic interaction between positively charged hydrophilic quaternary ammonium groups of CTAB and negatively charged hydrophilic carbon carriers which were synthesized by chemical oxidation of mesoporous carbon powders via the Hummers method. SEM and TEM images show the morphology of mesoporous carbon spheres before and after oxidation treatment (Fig. S3). The mesoporous carbon spheres suffered from oxidation to form uniform micron-sized carbon fragments with porous structure. It can be observed from Fig. 1A and B that the QAC@Carbon composite exhibited the same porous structure as hydrophilic carbon carrier. Furthermore, after surface modifications, the zeta-potential value of QAC@Carbon with pH of 7 was drastically shifted to 50.8 ± 1.2 mV from −46.6 ± 0.5 mV of the pristine carbon material (Fig. 1C) due to the positively charged quaternary ammonium groups in the QAC compound (zeta-potential value 39.0 ± 4.8 mV), suggesting a successful immobilization of QAC on the carbon carriers. QAC@Carbon composite was further analyzed to obtain detailed

Fig. 2. Blending of QAC, carbon carrier and QAC@Carbon into the PVDF membrane and its influence on membrane properties. (A) contact angle of membranes (n = 7); (B) Roughness. Rq, root mean square roughness; Ra, average roughness; Rmax, maximum roughness (n = 3); (C) porosity (n = 4) and (D) water permeability (n = 3). The inset figure in part A is the chemical structure of CTAB. Asterisks (*) denote a statistically significant difference between M0 and the rest membranes (p < 0.05).

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distribution along the cross-section was detected by EDX-mapping measurement (SI Fig. S7). The results showed that both membranes had a comparable nitrogen atom, confirming that the higher QAC/PVDF ratio for MCQ was due to surface segregation. It was further confirmed by the changes of zeta potential, i.e., −26.9 ± 0.7 mV for MQ and −11.6 ± 2.6 mV for MCQ (Table 1). QAC, as a kind of surfactant, has a long hydrophobic alkyl (hydrophobic tail) and a hydrophilic ionic group (hydrophilic head) in its structure. According to the XPS and EDX results, it is speculated that when the MQ casted film was exposed to the air in the pre-evaporation process, the free QAC molecules tended to move toward membrane surface driven by hydrophobic alkyl chains [42], thus leading to a surface concentration (Fig. 3). In the meantime, the accumulation of hydrophobic alkyl chains on the membrane surface might result in a decline of solvent evaporation rate [39]. Subsequently, when the MQ casting solution film was immersed into coagulation bath, the exchange rate between the solvent and non-solvent might be decreased [43,44]. The lowered exchange rate might thus hinder the transfer of QAC molecules to membrane surface during the phase inversion process, inducing a decreased QAC segregation on membrane surface. In contrast, hydrophilic carbon carrier might compromise the segregation rate during the pre-evaporation process for the MCQ membrane. This mitigated segregation in the pre-evaporation process might cause less significant impacts on the exchange rate between solvent and non-solvent for MCQ in the following phase inversion process [45,46], providing a larger exchange rate in comparison to MQ. This might contribute to the concentration of QAC@Carbon on membrane surface during phase inversion process thanks to the hydrophilic carbon material, serving as a core of QAC@Carbon composite (Fig. 3).

3.2. Intrinsic membrane properties Fig. 2 shows membrane physicochemical properties after modification by carbon, QAC and QAC@Carbon. It can be observed that membrane hydrophilicity was changed after modification, with the measured contact angles of 80.4 ± 0.6°, 73.1 ± 2.0°, 83.2 ± 0.9° and 76.9 ± 1.1° for M0, MC, MQ and MCQ, respectively. The incorporation of carbon enhanced the hydrophilicity of membranes, while the blending of QAC with PVDF membrane (MQ) caused an increase in contact angle, which should be attributed to the hydrophobic alkyl chains of QAC [17,18]. The introduction of QAC@Carbon into PVDF membrane (MCQ) thus resulted in a contact angle in between (Fig. 2A). It should be noted that this change in hydrophilicity is unlikely attributed to the change in surface roughness because AFM analysis of all the membranes reveals there was no obvious difference in the membrane surface roughness (~30 nm of average surface roughness Ra in Fig. 2B). Fig. 2C shows that the porosity of MQ was significantly decreased compared to the pristine membrane (M0), mainly due to a decline of the solvent evaporation rate and thus a delay in the coagulation of polymer in the presence of QAC [39]. In contrast, MC and MCQ had larger porosity than M0 and MQ. This indicates that the incorporation of carbon material in PVDF membranes increased its porosity due to its hydrophilic nature, which caused the rapid mass exchange rate between solvent and non-solvent during phase inversion. This will result in the formation of large pore channels and increase in the porosity [40,41]. Water permeability (Fig. 2D) showed similar trend to porosity and contact angle, i.e., MC and MCQ had higher permeability compared to M0 and MQ. Furthermore, MQ demonstrated a larger pore size (SI Fig. S5A), possibly ascribed to the release of QAC into the non-solvent during phase inversion that caused the formation of larger pores on membrane surface [39] and consequently lower retention of BSA (SI Fig. S5B). In comparison, MCQ membrane, with a smaller pore size due to the introduction QAC@Carbon into the membrane matrix, showed a higher retention of BSA. SI Fig. S6 shows the surface and cross-sectional morphologies of membranes. All the membranes exhibited a porous top layer and there were no obvious differences among the membrane structures. It suggests that QAC/Carbon/QAC@Carbon did not trigger the change of membrane structure at relatively low dosages. The abovementioned results clearly demonstrate that the introduction of carbon carriers avoids the drawbacks brought by QAC by taking advantage of the nature of carbon material, leading to a relatively lower contact angle, higher porosity and larger water permeability compared to M0 and MQ.

3.4. Antibacterial behavior evaluation Antibacterial properties of the modified membranes were determined using Gram-negative (E. coli) and Gram-positive (S. aureus) bacteria. The OD600 values during 24-h incubation are shown in SI Fig. S8. Specifically, cell proliferation modeling was conducted for the exponential growth phases [47] (i.e., 3–24 h for E. coli and 6–24 h for S. aureus), and experimental results showed there were no obvious differences between the culture solutions with and without M0 or MC (without membrane denoted as NM in Fig. 4) in terms of the bacterial growth rates (Fig. 4A and F). In contrast, bacterial growth was inhibited with the use of QAC incorporated membranes (MQ and MCQ). These findings suggest that the carbon carrier had minimal inhibition of bacterial growth activity against the model strains, while the QAC blended membranes demonstrated an outstanding antibacterial property against E. coli and S. aureus. Consistent with the OD600 measurements, SEM images (Fig. 4B, C, D, E and G, H, I, J) confirm that MQ and MCQ had prominent antibacterial effects in comparison to M0 and MC following the exposure of the membranes to bacterial culture suspensions for 24 h. The antibacterial experiments clearly demonstrated that the QAC-blended PVDF membranes presented efficient antibacterial activity for both Gram-positive and Gram-negative bacteria, while the membranes blended with the carbon carriers alone were incapable of inhibiting bacterial proliferation and adhesion on the membrane surfaces.

3.3. Surface segregation Based on XPS data (see SI Table S2), the QAC/PVDF ratio of MQ and MCQ was determined (see detailed calculations in SI Section S4). MCQ had a much higher QAC/PVDF ratio (15.1%) on the membrane surface, which is 2.5-fold of the MQ (6.8%) (Table 1). This indicates that QAC@Carbon showed substantial surface segregation during membrane formation process compared to QAC alone. Nitrogen element Table 1 QAC/PVDF ratio derived from XPS measurement and zeta potential of MQ and MCQ membranes. Membranes

MQ MCQ a b

3.5. Stability of QAC in MQ and MCQ membranes

Zeta potentialb (mV)

XPS measurement QAC (wt %)

PVDF (wt %)

QAC/ PVDFa

6.06 9.19

88.82 61.03

0.068 0.151

The stability of QAC in the modified membranes determines the antimicrobial effects particularly in long-term filtration. To verify whether carbon carriers were capable of improving QAC stability in the membrane matrix, QAC leaching tests were performed for MQ and MCQ membranes (Fig. 5). It can be seen that the release amount of QAC from MQ increased significantly at an initial rate of 585 ± 69 μg cm−2 d−1 (Fig. 5A) with a final loss accounting for 30% QAC (about 300 μg cm−2 of total QAC) in MQ membrane matrix. In contrast, the MCQ membrane

−26.9 ± 0.7 −11.6 ± 2.6

The theoretical bulk ratio of QAC/PVDF is 0.05. Zeta potential was measured at pH=7.0.

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Fig. 3. A schematic representation of the influence of carbon carrier on QAC segregation toward membrane surface.

cells mL−1 S. aureus was used as a feed solution. Fig. 6A shows the variations of trans-membrane pressure (TMP) of MC, MQ and MCQ over the course of 24 h. All kinds of membranes were operated in the same reactor to ensure that they encountered the same operating conditions and mixed liquor. A gradual increase of TMP was observed due to the formation of a biofilm on the membrane. The TMP increase rate of MCQ was lower compared to that of MC and MQ (Fig. 6A). It confirms that QAC@Carbon was not only able to provide effective antibiofouling properties but also maintain their favorable intrinsic physicochemical properties of membranes such as contact angle and porosity. In order to further understand the role of QAC@Carbon in biofouling mitigation, visualization of the bacteria and EPS on the membrane surface was carried out using CLSM with SYTO 9, propidium iodide (PI) and Con A to stain all bacteria, dead bacteria and EPS, respectively [36]. Analysis of the side-view of the biofilm reveals the structural differences among the biofilms formed on MCQ membrane and the other two membranes (Fig. 6A). The biofilm layer on MCQ (15 μm thickness) is thinner than those on MC (30 μm) and MQ (36 μm) membranes, and the relative abundance of dead cells in the biofilm of MCQ, indicated by red color via PI staining, was clearly observed in the bottom part of the biofilm in contact with the QAC@Carbon surface (Fig. 6A). Further analysis of the CLSM images in terms of biovolumes of live cells, dead cells, and EPS in the biofilm shows that biofilm formed on

exhibited a much slower release of QAC into water at an initial rate of 195 ± 5 μg cm−2 d−1 (Fig. 5A), with about 2% QAC released at the end of the experiment. Nevertheless, Ea for both membranes maintained a stable value during 20 d (Fig. 5B). QAC leaching behaviors were further tested by exposing the membranes to NaClO cleaning solutions. It is evident that the QAC release was significantly alleviated for MCQ as compared to MQ over the entire experiment course of 72 h (Fig. 5C), confirming that the carbon carriers could suppress QAC release from membrane matrix due to the immobilization of QAC. Furthermore, the membranes after leaching tests sustained their antimicrobial efficiency (Fig. 5D). The results clearly show that QAC@Carbon composite was capable of assembling QAC on the surface of carbon carrier and achieved better QAC stability in membrane matrix without sacrificing antimicrobial efficiency. The decreased release of QAC from MCQ membranes is conducive to maintaining the long-lasting antimicrobial efficiency in long-term operation, and simultaneously prevents the possible negative impacts induced by the release of QAC into the water environment [48–50]. 3.6. Membrane biofouling under cross-flow filtration To further determine the antibiofouling potential of the MCQ membranes, dynamic biofouling experiments were conducted in a labscale cross-flow filtration reactor. Bacterial suspension containing 107 234

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Fig. 4. Antibacterial activity of M0, MC MQ and MCQ. (A) μ of E. coli upon contact with all the membranes [with NM (no membrane) as a control]; SEM images of the surfaces of (B) M0, (C) MC, (D) MQ and (E) MCQ following the exposure to E. coli for 24 h; (F) μ of S. aureus upon contact with all the membranes [with NM as a control]; SEM images of the surfaces of (G) M0, (H) MC, (I) MQ and (J) MCQ following the exposure to S. aureus for 24 h. The white bars in parts B, C, E, and F indicate the length of 10 µm. Asterisks (*) denote a statistically significant difference between M0 and MQ/MCQ (p < 0.05).

MCQ membranes after 24-h filtration is thinner and composed of fewer live cells, and smaller EPS biovolumes than biofilms formed on MC and MQ membranes (SI Table S3), confirmed by the lower TOC concentration (SI Table S3) on MCQ membrane. Surface morphology revealed by CLSM images (Fig. 6B, C and D) again confirmed the mitigated biofouling on MCQ. Reduced accumulation and inhibited growth of biomass on MCQ membrane accounted for the milder TMP increase rate in the cross-flow filtration. Furthermore, it can be observed from Fig. 6 that the MCQ membrane had a much lower fouling rate though a fouling layer had been formed on membrane surfaces. It suggests that the formation of a biofouling layer on this modified membrane did not significantly affect the antibiofouling efficacy due to the indirect contact-killing mechanism: cells contacting the QAC-loaded membrane surface may release bacterial signals, causing growth inhibition and cell death in the vicinity of membrane surface [18]. Although the cross-flow test clearly shows the antibiofouling efficacy, further investigation on the MCQ membrane using real municipal wastewater is needed.

(QAC@Carbon). The QAC content on the surface of membrane modified by QAC@Carbon was 2.5-fold of that modified by QAC alone. The enhanced segregation can significantly improve the cost-effectiveness in biofouling mitigation, thus well addressing the drawbacks of in-situ membrane modification for preparing antibiofouling membranes. Leaching tests of the modified membranes by QAC@Carbon also demonstrated much better stability compared to the membranes blended with QAC alone, confirming that the proposed protocol can inhibit the release of antimicrobial agents and enable a long-term antibiofouling efficacy. The results highlight the potential of the introduction of QAC@Carbon into polymeric membranes as an effective strategy to fabricate antibiofouling membranes for water and wastewater treatment. Further investigation on the performance of MCQ membrane is needed in order to validate its antibiofouling efficacy using real municipal wastewater. Supporting information The Supporting Information is available free of charge on the website. Evaluation of membrane rejection behaviors (Section S1); Analysis of QAC concentration (Section S2); Details of the filtration setup (Section S3); Detailed calculation of XPS data (Section S4); A schematic illustrating the stability tests of QAC in membrane matrix (Fig. S1); A closed-loop filtration system for biofouling experiment (Fig.

4. Conclusions In this study, we developed a facile method to enhance the antimicrobial agent's segregation towards the surface of polymeric membranes by assembling QAC on hydrophilic carbon material 235

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Fig. 5. QAC stability in the MQ and MCQ membrane matrix. (A) QAC concentration and QAC release rate for MQ and MCQ immersed in water as a function of time; (B) antibacterial efficiencies (Ea) of MQ and MCQ which were soaked in water for different durations; (C) QAC concentration and QAC release rate for MQ and MCQ immersed in NaClO solution for different durations and (D) Ea of MQ and MCQ which were soaked in NaClO solution for different durations.

Acknowledgments We thank the National Natural Science Foundation of China (Grants 51422811 & 51378371) for the financial support of this work. Dr. Jinxing Ma acknowledges the receipt of a UNSW Vice-Chancellor's Postdoctoral Research Fellowship (RG152482). Appendix A. Supplementary material Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.memsci.2017.06.008. References Fig. 6. Biofouling behaviors of modified membrane. (A) Variations of TMP for MC, MQ and MCQ membranes as a function of time, and representative confocal microscopy side view of the biofilms formed on MC, MQ and MCQ membranes after 24-h operation; CLSM images of the biofilms of (B) MC, (C) MQ and (D) MCQ membranes after 24-h operation. In part A, the dashed circles indicate membrane staining point. Biofilms were stained with Con A (blue), SYTO 9 (green), and PI (red) for EPS (polysaccharides), live and/or dead cells, and dead cells, respectively. White bar represents a length of 20 μm.

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S2); Morphology of mesoporous carbon spheres before and after oxidation treatment (Fig. S3); The specific DSC profiles of QAC, carbon and QAC@Carbon samples (Fig. S4); Average pore size and retention behaviors of all the membranes (Fig. S5); SEM images of all the membranes (Fig. S6); Nitrogen element distribution along MQ and MCQ cross-section (Fig. S7); The OD600 value of all the membranes (Fig. S8); Detailed chemical composition for membrane preparation (Table S1); Surface elemental composition of membranes measured by XPS (Table S2); Biofilm characteristics of MC, MQ and MCQ membranes (Table S3).

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