ARTICLE pubs.acs.org/est
Bacterial Attachment to RO Membranes Surface-Modified by Concentration-Polarization-Enhanced Graft Polymerization Roy Bernstein,†,‡ Sofia Belfer,† and Viatcheslav Freger*,†,‡,§ † ‡
Zuckerberg Institute for Water Research, Ben-Gurion University of the Negev, P.O. Box 635, Sde-Boqer 84990, Israel Unit of Environmental Engineering and §Department of Biotechnology, Ben-Gurion University of the Negev, P.O. Box 635, Beer-Sheva 84105, Israel
bS Supporting Information ABSTRACT: Concentration polarization-enhanced radical graft polymerization, a facile surface modification technique, was examined as an approach to reduce bacterial deposition onto RO membranes and thus contribute to mitigation of biofouling. For this purpose an RO membrane ESPA-1 was surface-grafted with a zwitterionic and negatively and positively charged monomers. The low monomer concentrations and low degrees of grafting employed in modifications moderately reduced flux (by 2040%) and did not affect salt rejection, yet produced substantial changes in surface chemistry, charge and hydrophilicity. The propensity to bacterial attachment of original and modified membranes was assessed using bacterial deposition tests carried out in a parallel plate flow setup using a fluorescent strain of Pseudomonas fluorescens. Compared to unmodified ESPA-1 the deposition (mass transfer) coefficient was significantly increased for modification with the positively charged monomer. On the other hand, a substantial reduction in bacterial deposition rates was observed for membranes modified with zwitterionic monomer and, still more, with very hydrophilic negatively charged monomers. This trend is well explained by the effects of surface charge (as measured by ζ-potenital) and hydrophilicity (contact angle). It also well correlated with force distance measurements by AFM using surrogate spherical probes with a negative surface charge mimicking the bacterial surface. The positively charged surface showed a strong hysteresis with a large adhesion force, which was weaker for unmodified ESPA-1 and still weaker for zwitterionic surface, while negatively charged surface showed a long-range repulsion and negligible hysteresis. These results demonstrate the potential of using the proposed surface- modification approach for varying surface characteristics, charge and hydrophilicity, and thus minimizing bacterial deposition and potentially reducing propensity biofouling.
1. INTRODUCTION Biofouling, undesired attachment of microorganism communities to the membrane surface, is a major problem in water desalination as well as other membrane processes.1 Biofouling negatively affects the flux due to the added hydraulic resistance of the biofilm.24 Biofilms also hinder diffusion of rejected salts from the membrane surface back to the bulk, thus enhancing the concentration polarization, which reduces salt rejection and flux.5 In addition, the more frequent cleaning required for biofilm removal shortens the membrane lifetime.6 The problem of biofouling in NF or RO systems is exacerbated by the fact that polyamide membranes cannot be disinfected with chlorine or backwashed.1 Usually, biofilms are periodically removed following available cleaning protocols, once their negative impact on performance has exceeded certain limits, that is, when the performance has already suffered.7,8 A more effective approach would be to prevent or control biofouling. Proposed approaches include continuous or intermittent addition of biocides 9,10 and control of the nutrient level in the feed.11 Another promising method r 2011 American Chemical Society
investigated in this study is to inhibit biofilm formation by reducing the membrane propensity to biofouling.12 It is generally agreed that the biofilm undergoes several stages of development. Initially, the bacteria are deposited on and adhere to the surface, thereafter quorum-sensing mechanisms trigger extracellular polymeric substances (EPS) release and, ultimately, a biofilm EPS matrix with embedded bacteria is formed and may later proliferate.13 The primary adhesion of cells onto a surface, also known as initial deposition, is a critical stage in the overall process and is also considered the only reversible stage in biofilm formation. Initial deposition is controlled by various parameters of the environment, the surface and the bacteria. The relevant factors include hydrodynamics forces,14,15 solution chemistry,1618 surface roughness and topography 19,20 and interfacial forces governed by the physicochemical Received: December 29, 2010 Accepted: June 3, 2011 Revised: May 22, 2011 Published: June 17, 2011 5973
dx.doi.org/10.1021/es1043694 | Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology
ARTICLE
Table 1. Monomers and Conditions Used for Modificationsa
a
The asteriskindicates the monomer was obtained by sulfonation of grafted poly-GMA layer.
characteristics of the bacteria and surface. The latter combine electrostatic and Lifshitzvan der Waals forces, hydrophobic interactions and/or a variety of specific interactions.2124 In desalination systems additional engineering factors may be important, such as the design of the membrane element and spacers.25 Usually, in actual applications the water chemistry, hydrodynamic conditions, and physicochemical characteristics of commercial polyamide RO membranes (surface charge, hydrophobicty and roughness) can be varied within fairly narrow limits. In absence of chlorine-stable membranes or an efficient alternative to chlorine disinfection that membranes can tolerate, the conditions are quite favorable for formation of viable and persistent biofilms when the nutrient level is sufficient. In this respect, variation of the membrane surface properties through surface modification appears to be an attractive and versatile approach to mitigation of biofouling. Some examples may be found in a recent review on membrane modification by Naturea et al.26 However, the use of this approach for NF/RO membranes has been surprisingly limited, possibly, since previous attempts showed a significant negative impact on permeability 2731 and rejection.32 Nevertheless, there is still much room for optimization. Since only the outer surface of the membrane needs to be modified, the impact of modification on flux and rejection could be kept to a minimum. We demonstrated recently that the performance of membranes modified via graft polymerization may be acceptable and even superior to that of commercial membranes with similar permeability, while the potential cost of modification and consumption of chemical could be greatly reduced using the concentration-polarization-enhanced version of this technique.33,34 In this work this facile method is used for modifying low pressure RO (LPRO) membranes with different monomers to obtain negatively and positively charged and zwitterionic surfaces. Using
thus prepared membranes we gain insight into the effect of the surface properties and membrane-bacteria interactions on bacterial deposition and membrane performance relative to unmodified membrane under well-defined physicochemical and hydrodynamic conditions.
2. EXPERIMENTAL SECTION Materials. Fully aromatic polyamide (PA) membrane ESPA-1 (Hydranautics) was kindly supplied by the manufacture as flat sheets. The membranes were stored at 4 C° and cleaned prior to the modification as described elsewhere.33 All chemicals were purchased from Aldrich-Sigma and used as received. Modification Setup and Procedure. The modification was carried inside a laboratory scale cross-flow test cell of area 17 cm2. For modification, the cell was connected to a small vessel containing a monomer solution that was directly pressurized with nitrogen from a cylinder (20 bar) thereby the solution filled the flow cell while the retentate line of the flow cell was closed. The membranes were modified with three monomers using a mixture of persulfate and metabisulfite as redox initiators at conditions specified in Table 1. The surface bearing negative fixed charge was obtained by postmodification of GMA-modified surface via conversion of the epoxy group of GMA using reaction with 10% Na2SO3 in 15% aqueous isopropanol solution at 3540 °C for 1216 h. Preparation of Bacterial Suspension for Deposition Experiments. Pseudomonas fluorescens tagged with green flourecent protein (GFP) was first precultured by incubating at 31 °C in LuriaBertani broth (containing 10 g/L tryptone, 5 g/L yeast extract, and 10 g/L sodium chloride) in the presence of 10 μg/mL Kanamycin and harvested in the midlog growth phase (12 h). 0.1 mL of precultured cell suspension was transferred to a 5974
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology
ARTICLE
fresh LB solution with 10 μg/mL Kanamycin for additional 12 h. The cultured cells were centrifuged at 4000g for 10 min and resuspended three times in a fresh background solution (10 mM NaCl, pH 6.57.2). The optical density of the final suspension subsequently used as feed in deposition experiments was adjusted to 0.1, as measured at 600 nm by a UVvis spectrophotometer (Lambda EZ 201 Perkin-Elmer), which corresponded to cell concentration 2.6 107 cells/mL. Bacterial Characteristics and Deposition Experiments. The experiments were carried out in a parallel plate flow cell setup (FC 271 flow cell, BioSurface Technologies Corporation) at room temperature (2225 °C). A 2.5 cm long piece of membrane was mounted inside the cell on a plastic stab. The feed flow rate was 1 mL/min, corresponding to wall shear rate 240 cm1. The bacteria deposited on the membrane surface were imaged and counted using a fluorescence microscope (Zeiss AX10) equipped with a 20 objective lens and a digital camera. The imaged area was 334 443 μm2 large and was located in the middle of the cell. Images were taken every 5 min for 30 min. At the end of 30 min additional control images were taken from a few other locations within 1 cm along the centerline to verify the results were representative. The mass transfer (deposition) coefficient kd was calculated under the assumption of linear kinetics, as follows kd ¼
1 dN CA dt
ð1Þ
where N is the number of bacteria in the image, A the image area, and C is the concentration of bacteria in the feed solution. The hydrophobicity of bacteria was evaluated using microbial adhesion to hydrocarbons (MATH) using n-dodecane-water system.35 ζ-potential of bacteria was measured using the electrophoretic mobility of bacteria (ZetaPlus 1994, Brookhaven Instruments Co., Holtsville, NY). For both measurements the bacteria were harvested, separated from growth medium, and resuspended in 10 mM NaCl solution at pH 7 to yield optical density 0.3 for MATH and 0.1 for the ζpotential measurements. Viability tests followed deposition on the ESPA1-g-METMAC were performed using bacterial dead/live kit (Molecular Probes, Eugene, OR) containing propidium iodide (PI) and SYTO9. The membrane surface was covered with 5 μL of a mixture of two fluorescent markers in a 10 mM NaCl background solution inside the flow cell for 10 min, washed with background solution and florescence images were taken from different locations on the membrane surface. Membrane Performance and Surface Characterization. The filtration tests were performed in a laboratory cross-flow setup described elsewhere.36 Water permeability (Lp) was determined by collecting and weighing permeate. Salt concentration in the feed (1.5 g/L) and permeate was determined from electric conductance of solutions. The rejection of salt was calculated using the relation R ¼ 1 Λp =Λf 100% where Λp and Λf are the permeate and the feed conductivity. Attenuated total reflection (ATR)-FTIR spectra (average of 40 scans at 4 cm1 resolution) were recorded on a Vertex 70 FTIR spectrometer (Bruker) using a Miracle ATR attachment with a one-reflection diamond-coated KRS-5 element (Pike). The contact angles were measured using a sessile drop of water
on an OCA-20 contact angle analyzer (DataPhysics). Every measurement was repeated and averaged for at least five drops (0.25 μL) on each membrane sample. ζ-potential measurements were performed at Anton Paar GmbH (Austria) using a SurPASS streaming potential analyzer with an adjustable gap cell. General survey spectra and high-resolution X-ray photoelectron spectroscopy (XPS) spectra were recorded using ESCALAB 250 (Thermo Fisher Scientific Inc., Waltham, UK) with Al X-ray source and monochromator. Binding-energies for probed elements were corrected for the charging effect with reference to the 285 eV C1s peak. Roughness and Force Measurements by AFM. AFM topographic images of modified and unmodified samples were acquired under water using a Nanoscope 3D Multimode AFM microscope (Veeco) and NP-S cantilevers (Veeco) in the tapping mode. The reported rms roughness is the average of three different samples, each sample measured at three different locations. The forcedistance measurements were performed using SiN cantilevers with an attached polystyrene sphere of diameter 1 μm functionalized with carboxyl groups (Novascan). The tests were conducted in 10 mM NaCl at pH 7 and pH 3. Prior to the measurement the cantilever sensitivity (vertical displacement vs cantilever bending signal) was calibrated using a Si wafer as rigid substrate and keeping the cantilever at a fixed position during both calibration and subsequent measurements. The force was calculated from the measured sensitivity and the nominal spring constant (0.06 N/m, as reported by the manufacturer). Three identically prepared samples were used to measure force distance curves for each sample. Each reported curve (Section 3.4) was the average of 16 separate curves for a 4 4 array of 16 spots spaced by 1 μm at a given location on each membrane. The pull-off (adhesion) force was evaluated from the forcedistance curves using the multiforce function of the built-in software (Nanoscope 6.14, Veeco) and the reported value was the average of three locations for three identically prepared membrane samples of a given type.
3. RESULTS AND DISCUSSION 3.1. Surface Characteristics of Membranes. Figure 1a and b presents ATR-FTIR spectra of pristine ESPA-1 and membranes modified with SPE and METMAC, respectively, in conditions specified in Table 1. A new band at 1724 cm1 in Figure 1a and 1726 cm1 in Figure 1b assigned to the carbonyl group of methacrylate ester appeared for the modified membranes. The bands at 1040 cm1 and 954 cm1, characteristic of the of the sulfonate group of SPE and quaternary amine of METMAC, respectively, are well observed in Figure 1a and b. The weak quaternary amine band of SPE at 962 cm1 could also be observed in Figure 1a. Figure 1c shows the spectrum of the membrane first modified with GMA (Table 1) and postconverted to sulfonate (Table 1). A 1730 cm1 band of ester carbonyl and a 907 cm1 bands of epoxy group appeared after modification with GMA. The latter band disappeared after sulfonation, while a band of sulfonate at 1045 cm1 appeared. Expected change in surface elemental composition was confirmed by XPS (see Supporting Information (SI)). The C:O and C:N ratios for pristine ESPA-1 were 4.35 and 7.16 in agreement with the typical composition of aromatic polyamide membranes.37 After grafting with GMA that does not contain N the C:N ratio increased to 11.96, yet the N peak was still 5975
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology
ARTICLE
Figure 1. ATR-FTIR spectrum of pristine ESPA1 and SPE (a) pristine ESPA1 and METMAC (b) and GMS modified ESPA1 membranes before and after sulfonation (c).
Table 2. Sessile Drop Contact Angle and Surface Roughness Measured by AFM of the Pristine and Modified Membranes membrane
contact angle,°
surface roughness, nm 75 ( 8
ESPA-1
45 ( 3
ESPA-g-METMAC
25 ( 4
85 ( 10
ESPA-SPE
25 ( 4
88 ( 15
ESPA-GMS
1015
88 ( 14
observed, reflecting a relatively low thickness of the poly-GMA layer and some contribution from the underlying polyamide. On the other hand, the C:O ratio was 2.38, close to the theoretical value for GMA 2.33. After modification with SPE and postsulfonation of GMA the intensity of the sulfur band increased. Also, after sulfonation of GMA the C:O ratio decreased from 2.38 for GMA to 2.02 due to the three additional oxygens of the sulfonate group but it was still far from the theoretical ratio 1 for GMS. This could also indicate a contribution from underlying polyamide, since ATR-FTIR shows that the epoxy band completely disappeared. For the membrane modified with METMAC the C:O and C:N ratios were 3.44 and 10.19 respectively, which reasonably compares with the theoretical values of 4 and 8 for METMAC. High-resolution XPS spectra also distinguished between the different bonding states of N1s components and showed that, in addition to a single band at 400 eV assigned to the amide N, a new band at 402 eV corresponding to an amine appeared after modification with METMAC and SPE (SI,Table S1).
Figure 2. ζ-potentail of the pristine and modified membrabes in 1 mM KCl.
From the contact angle measurement summarized in Table 2 it is clear that the modified membranes were more hydrophilic than the pristine membrane because of the charged groups of the modifying polymers. Modification with SPE and METMAC reduced the contact angle from 45 ( 3° of the ESPA-1 to 25 ( 4°. After modification with GMS the surface became very hydrophilic and accurate measurements were then difficult, since 5976
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology
ARTICLE
Figure 3. (a) Normalized deposition of P. fluorescens deduced from fluorescence images taken from the same location on initially clean membrane surface at different times. Error bars show standard deviation, n e 3. (b) Bacterial deposition coefficients of P. fluorescens on pristine and modified ESPA1. Error bars show standard deviation. Deposition conditions: pH 7 ( 0.5, 10 mM NaCl.
the contact angle was close to complete wetting; it was estimated to be no more than 1015°. Table 2 also shows that the surface roughness as determined by AFM did not change considerably after modification and remain within the range 70100 nm. This is consistent with the relatively low degrees of modification.33 Figure 2 shows the results of ζ-potential measurements. The ζ-potential of the ESPA-1 membrane at pH 7 and 1 mM KCl was negative 30 mV with an iso-electric point (pI) at pH 4, as characteristic of polyamide membranes.37,38 The METMACmodified membrane had a positive ζ-potential at pH 7 with pI only slightly above this value. It was reported that ζ-potential could monotonically change with the degree of grafting,39 then this relatively low pI for could be a result of low modification, as was indeed indicated by ATR-FTIR. As expected, the ζ-potential of the membrane modified with SPE was between that of METMAC and pristine ESPA-1 and was typical for a zwitterion surface40 with pI somewhat below 7 due to the screened contribution from the underlying polyamide. The sulfonated surface (GMS) was more negatively charged than the ESPA-1 and remained negative throughout the examined pH range owing to the strongly acidic sulfonate groups. 3.2. Membrane Performance. The membrane permeability was usually reduced after modification by 2040%, even for very low modifications when the ATR-FTIR spectra showed minor changes, likely, as a result of “caulking” defects in polyamide layer.33 The salt rejection after modification with METMAC remained the same as that of ESPA-1, while modification with SPE and GMS caused some improvement, from 95 ( 2% for the pristine ESPA1 to 96.5 ( 2%. The reduced permeability of modified membranes could then be offset by improved selectivity and more sustainable fluxes as a result of lower fouling and facilitated cleaning.4143 For instance, modified LE membranes were superior to commercial membranes of similar permeability.34 However, it is important to stress that, unlike the previous study,34 where improved selectivity was sought, here there is room for minimizing modification and reducing loss of permeability, if only surface properties need to be modified. The loss of flux would also be less significant for denser and less permeable seawater RO membranes.34 3.3. Bacterial Deposition. Tests using single bacterial strains in general and deposition experiments in particular are common and have often been used as convenient well-defined
indicators 4,15,17,20,40,44,45 especially, when the emphasis is placed on physicochemical side of the problem, even though they do not fully represent actual biofouling in its entire complexity (e.g., ref 45). The GFP-tagged Pseudomonas fluorescens bacteria are negatively charged at pH 7 with ζ-potential 40 ( 5 mV. Examination using MATH showed that the bacteria are hydrophilic with a partitioning coefficient between water and n-dodecane 17 ( 4%. These characteristics are fairly representative of many bacteria 23,46 including many biofilm-forming ones,47 making P. fluorescens a convenient model organism in bacterial deposition, biofilm and biofouling studies.19,48,49 Figure 3a shows the average number of bacteria adhered to the membrane surface counted at the same location in the course of deposition at different times (530 min) and normalized to the image area and the bacteria concentration in the bulk solution. It is seen that for flow conditions used and deposition times the kinetics was linear, that is, interaction between bacteria and detachment from the surface did not affect the deposition rate and the deposition coefficients kd could be calculated from the slopes. Figure 3b shows the kd values averaged over three to nine experiments for different membranes. It is clearly seen that, compared to the original membrane, the bacterial deposition is much faster for the positively charged membrane and significantly slower for the membrane modified with the zwitterionic monomer and still lower for the negatively charged. The enhanced deposition of negatively charged bacteria on positively charged surface is in agreement with previous reports and is usually explained by electrostatic attraction between the oppositely charged bacteria and surface.40,50,51 In contrast, the similar charge of bacteria and GMS hinders bacteria deposition, due to repulsion between electric double layers.40,52,53 It was also suggested that bacteria adhering to similarly charged surface are trapped in a secondary energy minimum therefore the adherence is weak and they are easily detached from the surface by hydrodynamic forces.44 As well as GMS, pristine ESPA-1 has a significant negative ζ-potential at pH 7; however, it shows a much larger deposition rate. On the other hand, nearly neutral zwitterionic SPE surface shows inhibited deposition (Figure3b), in agreement with other reports.40,54 The overall trend can be best explained by the combined effect of surface charge and higher hydrophobicity of ESPA-1 compared with GMS and SPE, as indicated by contact angles in 5977
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology
ARTICLE
Figure 4. Force distance curve for intraction between the surrogate probe and surface modified with different monomers: (a) GMS, pH7 and pH3, and ESPA1, pH7, approach; (b) METMAC and SPE, pH7, approach; (c) ESPA1, METMAC, and SPE, pH7, retraction.
Table 2. Van Loosdrecht et al. suggested that bacteria should better adhere to hydrophobic surfaces, such as ESPA-1 surface, due to stronger hydrophobic interactions, that is, more favorable water removal from the region between the surface and bacteria when they come in contact.46 Similar deposition coefficient of the SPE and GMS surfaces, despite different ζ-potentials, may result from a strong hydration of the charge groups present in both surface and weakness of hydrophobic (as for ESPA1) attraction. Analogous arguments are often used to explain resistance of surfaces to protein adsorption.55,56 Although quaternary ammonium surface accelerates deposition, much evidence exists that quaternary ammonium groups at the surface, such as METMAC, have an antimicrobial activity,51,57,58 which could have affected the deposition experiments. However, viability live/dead staining test performed for the bacteria adhered to the METMAC-modified membrane at the end of the adhesion experiment (30 min) clearly showed that most bacteria were alive (see SI Figure S1). Then there was no indication that viability could be impaired and thus affect the bacteria attachment results, regardless of whether the grafting density of METMAC did not exceed the required minimum59 or the exposure time was too short. 3.4. AFM Force Measurements. A further insight into the interactions between membranes and bacteria was gained through forcedistance curves measured by AFM using a surrogate carboxylated 1 μm large particle mimicking the negatively charged bacteria. Figure 4a and b are representative forcedistance curves measured on approach to the surface
averaged over 16 curves for each location as described in the Experimental Section. The steep linear slope at large forces corresponded to bending of the cantilever after the probe touched the rigid surface. The range of repulsive (positive) force was quite short for all samples apart from the GMS modified membrane at pH 7. The long-range repulsion for GMS disappeared when pH was reduced to 3 (Figure 4a), which is consistent with neutralization of the carboxylic groups on the particle surface at this pH. This suggests that the long-range repulsion for GMS surface apparently resulted from the electrostatic interaction between the electric double layers on the surface of the probe and the modified membrane surface rather than from steric effects. Figure 4c shows representative forcedistance curves obtained upon retraction of the probe from the ESPA-1 membrane and ones modified with METMAC and SPE. The most notable feature is the strong hysteresis and a large attraction (negative) force for METMAC, fully consistent with high bacterial deposition and with strong electrostatic mechanism involved. The maximum average pull-off force was 2 ( 1 nN for different samples of this membrane. A smaller yet significant attraction force, 1 ( 0.5 nN, was also consistently measured for EPSA-1, which became slightly stronger at pH 3 (not shown), where ESPA-1 lost its negative charge. Some non-negligible attraction was also present for SPE. For ESPA-1 the moderate attraction could result from hydrophobic interactions, which was consistent with increased adhesion at pH 3 and with absence of any attraction for very hydrophilic GMS membrane at pH 7 5978
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology (not shown). It is not entirely clear what was the reason for attraction in the case of SPE; it could involve some hydrogenbonding and/or hydrophobic interactions as well. Anyway, the overall trend of the magnitude of the pull-off force was well correlated with the trend of bacterial deposition in Figure 3b. In conclusion, the presented results demonstrate the systematic relations between the surface characteristics of modified membranes, physicochemical interactions between the bacteria and kinetics of bacterial deposition. These findings in combination with the facile concentration polarization-enhanced modification technique open a route to rational design and preparation of modified membranes (including in situ modification of commercial membrane elements) for biofouling mitigation with a minimal impact on flux and selectivity.
’ ASSOCIATED CONTENT
bS
Supporting Information. It presents high resolution XPS results for pristine and modified ESPA1 membranes and analysis of viability of Pseudomonas fluorescens deposited on METMAC-modified ESPA1 using SYTO9 and propidium iodide stains.This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT We thank Prof. Sharon Walker (UC Riverside, CA), Dr. Moshe Herzberg and Ms. Vered Shapiro (Ben-Gurion University) for fruitful discussions, and Dr. Thomas Luxbacher (Anton Paar GmbH) for helping with ζ-potential measurements. Dr Rich Franks and Hydranautics are gratefully acknowledged for supplying membrane samples. This work was partly supported by a grant from the Water Authority of Israel. ’ REFERENCES (1) Ridgway, H. Flemming, H. Membrane Biofouling in Water Treatment Membrane Processes. Water Treatment Membrane Processes; McGraw-Hill: New York, 1996. (2) Jarusutthirak, C.; Amy, G. Role of soluble microbial products (SMP) in membrane fouling and flux decline. Environ. Sci. Technol. 2006, 40, 969–974. (3) Flemming, H. C. Biofouling in water systemscases, causes and countermeasures. Appl. Microbiol. Biotechnol. 2002, 59, 629–640. (4) Herzberg, M.; Kang, S.; Elimelech, M. Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. Environ. Sci. Technol. 2009, 43, 4393–4398. (5) Herzberg, M.; Elimelech, M. Biofouling of reverse osmosis membranes: role of biofilm-enhanced osmotic pressure. J. Membr. Sci. 2007, 295, 11–20. (6) Al-Amoudi, A.; Lovitt, R. W. Fouling strategies and the cleaning system of NF membranes and factors affecting cleaning efficiency. J. Membr. Sci. 2007, 303, 4–28. (7) Liikanen, R.; Yli-Kuivila, J.; Laukkanen, R. Efficiency of various chemical cleanings for nanofiltration membrane fouled by conventionally-treated surface water. J. Membr. Sci. 2002, 195, 265–276. (8) Subramani, A.; Hoek, E. Biofilm formation, cleaning, re-formation on polyamide composite membranes. Desalination 2010, 257, 73–79.
ARTICLE
(9) Li, Q.; Mahendra, S.; Lyon, D. Y.; Brunet, L.; Liga, M. V.; Li, D.; Alvarez, P. J. J. Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res. 2008, 42, 4591–4602. (10) Baker, J.; Dudley, L. Biofouling in membrane systems - A review. Desalination 1998, 118, 81–89. (11) Flemming, H. C. Reverse osmosis membrane biofouling. Exp. Therm. Fluid Sci. 1997, 14, 382–391. (12) Mansouri, J.; Harrisson, S.; Chen, V. Strategies for controlling biofouling in membrane filtration systems: Challenges and opportunities. J. Mater. Chem. 2010, 20, 4567–4586. (13) Characklis, W.; Cooksey, K. Biofilms and microbial fouling. Adv. Appl. Microbiol. 1983, 29, 93–138. (14) Eshed, L.; Yaron, S.; Dosoretz, C. Effect of permeate drag force on the development of a biofouling layer in a pressure-driven membrane separation system. Appl. Environ. Microbiol. 2008, 74, 7338–7347. (15) Purevdorj, B.; Costerton, J.; Stoodley, P. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 2002, 68, 4457–4464. (16) Rijnaarts, H. H. M.; Norde, W.; Lyklema, J.; Zehnder, A. J. B. DLVO and steric contributions to bacterial deposition in media of different ionic strengths. Colloids Surf., B 1999, 14, 179–195. (17) Chen, G.; Beving, D. E.; Bedi, R. S.; Yan, Y. S.; Walker, S. L. Initial bacterial deposition on bare and zeolite-coated aluminum alloy and stainless steel. Langmuir 2009, 25, 1620–1626. (18) Chen, G.; Walker, S. L. Role of solution chemistry and ion valence on the adhesion kinetics of groundwater and marine bacteria. Langmuir 2007, 23, 7162–7169. (19) Diaz, C.; Salvarezza, R. C.; Fernandez Lorenzo de Mele, M. A.; Schilardi, P. L. Organization of Pseudomonas fluorescens on chemically different nano/microstructured surfaces. ACS Appl. Mater. Interfaces 2010, 2, 533–538. (20) Park, N.; Kwon, B.; Kim, I. S.; Cho, J. Biofouling potential of various NF membranes with respect to bacteria and their soluble microbial products (SMP): characterizations, flux decline, and transport parameters. J. Membr. Sci. 2005, 258, 43–54. (21) Busscher, H. J.; Weerkamp, A. H. Specific and non-specific interactions in bacterial adhesion to solid substrata. FEMS Microbiol. Lett. 1987, 46, 165–173. (22) Hermansson, M. The DLVO theory in microbial adhesion. Colloids Surf., B 1999, 14, 105–119. (23) Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. The role of bacterial cell wall hydrophobicity in adhesion. Appl. Environ. Microbiol. 1987, 53, 1893–1897. (24) Poortinga, A. T.; Bos, R.; Norde, W.; Busscher, H. J. Electric double layer interactions in bacterial adhesion to surfaces. Surf. Sci. Rep. 2002, 47, 1–32. (25) Bereschenko, L.; Heilig, G.; Nederlof, M.; Van Loosdrecht, M.; Stams, A.; Euverink, G. Molecular characterization of the bacterial communities in the different compartments of a full-scale reverseosmosis water purification plant. Appl. Environ. Microbiol. 2008, 74, 5297–5304. (26) Rana, D.; Matsuura, T. Surface modifications for antifouling membranes. Chem. Rev. 2010, 110, 2448–2471. (27) Belfer, S.; Purinson, Y.; Fainshtein, R.; Radchenko, Y.; Kedem, O. Surface modification of commercial composite polyamide reverse osmosis membranes. J. Membr. Sci. 1998, 139, 175–181. (28) Sarkar, A.; Carver, P. I.; Zhang, T.; Merrington, A.; Bruza, K. J.; Rousseau, J. L.; Keinath, S. E.; Dvornic, P. R. Dendrimer-based coatings for surface modification of polyamide reverse osmosis membranes. J. Membr. Sci. 2010, 349, 421–428. (29) Sagle, A. C.; Van Wagner, E. M.; Ju, H.; McCloskey, B. D.; Freeman, B. D.; Sharma, M. M. PEG-coated reverse osmosis membranes: Desalination properties and fouling resistance. J. Membr. Sci. 2009, 340, 92–108. (30) Wu, D.; Liu, X.; Yu, S.; Liu, M.; Gao, C. Modification of aromatic polyamide thin-film composite reverse osmosis membranes by 5979
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
Environmental Science & Technology surface coating of thermo-responsive copolymers P (NIPAM-co-Am). I: Preparation and characterization. J. Membr. Sci. 2010, 352, 76–85. (31) Van der Bruggen, B. Comparison of redox initiated graft polymerisation and sulfonation for hydrophilisation of polyethersulfone nanofiltration membranes. Eur. Polym. J. 2009, 45, 1873–1882. (32) Wei, X.; Wang, Z.; Chen, J.; Wang, J.; Wang, S. A novel method of surface modification on thin-film-composite reverse osmosis membrane by grafting hydantoin derivative. J. Membr. Sci. 2010, 346, 152–162. (33) Bernstein, R.; Belfer, S.; Freger, V. Surface modification of dense membranes using radical graft polymerization enhanced by monomer filtration. Langmuir 2010, 3168–3175. (34) Bernstein, R.; Belfer, S.; Freger, V. Toward improved boron removal in RO by membrane modification: Feasibility and challenges. Environ. Sci. Technol. 2011, 45, 3613–3620. (35) Pembrey, R. S.; Marshall, K. C.; Schneider, R. P. Cell surface analysis techniques: What do cell preparation protocols do to cell surface properties? Appl. Environ. Microbiol. 1999, 65, 2877–2894. (36) Ben-David, A.; Bason, S.; Jopp, J.; Oren, Y.; Freger, V. Partitioning of organic solutes between water and polyamide layer of RO and NF membranes: correlation to rejection. J. Membr. Sci. 2006, 281, 480–490. (37) Tang, C. Y.; Kwon, Y. N.; Leckie, J. O. Probing the nano-and micro-scales of reverse osmosis membranes--A comprehensive characterization of physiochemical properties of uncoated and coated membranes by XPS, TEM, ATR-FTIR, and streaming potential measurements. J. Membr. Sci. 2007, 287, 146–156. (38) Matsumoto, H.; Konosu, Y.; Kimura, N.; Minagawa, M.; Tanioka, A. Membrane potential across reverse osmosis membranes under pressure gradient. J. Colloid Interface Sci. 2007, 309, 272–278. (39) Susanto, H.; Ulbricht, M. Photografted thin polymer hydrogel layers on PES ultrafiltration membranes: characterization, stability, and influence on separation performance. Langmuir 2007, 23, 7818–7830. (40) Zhao, Y. H.; Zhu, X. Y.; Wee, K. H.; Bai, R. Achieving highly effective non-biofouling performance for polypropylene membranes modified by UV-Induced surface graft polymerization of two oppositely charged monomers. J. Phys. Chem. B 2010, 114, 2422–2429. (41) Zhou, Y.; Yu, S.; Gao, C.; Feng, X. Surface modification of thin film composite polyamide membranes by electrostatic self deposition of polycations for improved fouling resistance. Sep. Purif. Technol. 2009, 66, 287–294. (42) Belfer, S.; Fainshtain, R.; Purinson, Y.; Gilron, J.; Nystr€om, M.; M€antt€ari, M. Modification of NF membrane properties by in situ redox initiated graft polymerization with hydrophilic monomers. J. Membr. Sci. 2004, 239, 55–64. (43) Louie, J. S.; Pinnau, I.; Ciobanu, I.; Ishida, K. P.; Ng, A.; Reinhard, M. Effects of polyether-polyamide block copolymer coating on performance and fouling of reverse osmosis membranes. J. Membr. Sci. 2006, 280, 762–770. (44) Redman, J. A.; Walker, S. L.; Elimelech, M. Bacterial adhesion and transport in porous media: Role of the secondary energy minimum. Environ. Sci. Technol. 2004, 38, 1777–1785. (45) Lee, W.; Ahn, C. H.; Hong, S.; Kim, S.; Lee, S.; Baek, Y.; Yoon, J. Evaluation of surface properties of reverse osmosis membranes on the initial biofouling stages under no filtration condition. J. Membr. Sci. 2010, 351, 112–122. (46) Van Loosdrecht, M.; Lyklema, J.; Norde, W.; Schraa, G.; Zehnder, A. Electrophoretic mobility and hydrophobicity as a measured to predict the initial steps of bacterial adhesion. Appl. Environ. Microbiol. 1987, 53, 1898–1901. (47) Simoes, M.; Pereira, M. O.; Vieira, M. J. Effect of mechanical stress on biofilms challenged by different chemicals. Water Res. 2005, 39, 5142–5152. (48) Chong, T.; Wong, F.; Fane, A. The effect of imposed flux on biofouling in reverse osmosis: Role of concentration polarisation and biofilm enhanced osmotic pressure phenomena. J. Membr. Sci. 2008, 325, 840–850. (49) O’Toole, G. A.; Kolter, R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent
ARTICLE
signalling pathways: a genetic analysis. Mol. Microbiol. 1998, 28, 449–461. (50) Terada, A.; Yuasa, A.; Tsuneda, S.; Hirata, A.; Katakai, A.; Tamada, M. Elucidation of dominant effect on initial bacterial adhesion onto polymer surfaces prepared by radiation-induced graft polymerization. Colloids Surf., B 2005, 43, 99–107. (51) Gottenbos, B.; Grijpma, D. W.; Van Der Mei, H. C.; Feijen, J.; Busscher, H. J. Antimicrobial effects of positively charged surfaces on adhering Gram-positive and Gram-negative bacteria. J. Antimicrob. Chemother. 2001, 48, 7–13. (52) Camesano, T. A.; Logan, B. E. Probing bacterial electrosteric interactions using atomic force microscopy. Environ. Sci. Technol. 2000, 34, 3354–3362. (53) Poortinga, A. T.; Bos, R.; Norde, W.; Busscher, H. J. Electric double layer interactions in bacterial adhesion to surfaces. Surf. Sci. Rep. 2002, 47, 1–32. (54) Cheng, G.; Zhang, Z.; Chen, S.; Bryers, J. D.; Jiang, S. Inhibition of bacterial adhesion and biofilm formation on zwitterionic surfaces. Biomaterials 2007, 28, 4192–4199. (55) Chen, S.; Zheng, J.; Li, L.; Jiang, S. Strong resistance of phosphorylcholine self-assembled monolayers to protein adsorption: insights into nonfouling properties of zwitterionic materials. J. Am. Chem. Soc. 2005, 127, 14473–14478. (56) Bernards, M. T.; Cheng, G.; Zhang, Z.; Chen, S.; Jiang, S. Nonfouling polymer brushes via surface-initiated, two-component atom transfer radical polymerization. Macromolecules 2008, 41, 4216–4219. (57) Madkour, A. E.; Dabkowski, J. M.; N€usslein, K.; Tew, G. N. Fast disinfecting antimicrobial surfaces. Langmuir 2008, 25, 1060–1067. (58) Huang, J.; Koepsel, R. R.; Murata, H.; Wu, W.; Lee, S. B.; Kowalewski, T.; Russell, A. J.; Matyjaszewski, K. Nonleaching antibacterial glass surfaces via “grafting onto”: The effect of the number of quaternary ammonium groups on biocidal activity. Langmuir 2008, 24, 6785–6795. (59) Kugler, R.; Bouloussa, O.; Rondelez, F. Evidence of a chargedensity threshold for optimum efficiency of biocidal cationic surfaces. Microbiology 2005, 151, 1341–1348.
5980
dx.doi.org/10.1021/es1043694 |Environ. Sci. Technol. 2011, 45, 5973–5980
