Prevention of bacterial adhesion on polyamide

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polymer containing cationic amino groups, poly[2-methacryloyloxyethyl phosphorylcholine (MPC)-co-. 5. 2-aminoethylmethacrylate (AEMA)] (p(MPC-co-AEMA)).
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Prevention of bacterial adhesion on polyamide reverse

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osmosis membranes via electrostatic interactions using a

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cationic phosphorylcholine polymer coating

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Daisuke Saeki, Tatsuya Tanimoto, Hideto Matsuyama*

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Center for Membrane and Film Technology, Department of Chemical Science and Engineering, Kobe

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University, 1-1 Rokkodai, Nada, Kobe 657-8501, Japan

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* Corresponding author. E-mail: [email protected]. Phone & FAX: +81-78-803-6180.

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ABSTRACT

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A simple and easy anti-adhesive coating method against bacteria via electrostatic interaction was

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developed for polyamide reverse osmosis (RO) membranes using a cationic phosphorylcholine polymer.

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A commercial polyamide RO membrane was immersed into an aqueous solution of phosphorylcholine

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polymer containing cationic amino groups, poly[2-methacryloyloxyethyl phosphorylcholine (MPC)-co-

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2-aminoethylmethacrylate (AEMA)] (p(MPC-co-AEMA)). From the results of contact angle and

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surface potential measurements, the surface of the coated RO membrane became more hydrophilic than

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that of raw membranes and had a neutral charge. Conversely, the surface of an RO membrane immersed

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in an aqueous solution of MPC homopolymer without AEMA groups was not coated by the polymer.

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Therefore, p(MPC-co-AEMA) was adsorbed via electrostatic interaction between the cationic amino

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groups of AEMA and anionic carboxylic groups on the polyamide RO membrane. X-ray photoelectron

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spectroscopy showed the existence of phosphorylcholine groups from p(MPC-co-AEMA) on the coated

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membranes. The result of quartz crystal microbalance with dissipation monitoring measurements

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showed that adsorbed p(MPC-co-AEMA) was hardly desorbed from the polyamide surface in a high

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ionic strength solution at least for one day. The coated RO membrane had high resistance to bacterial

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adhesion and retained its original rejection performance.

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KEYWORDS: Reverse osmosis membrane; phosphorylcholine polymer; anti-biofouling; electrostatic

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interaction

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MANUSCRIPT TEXT

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1. Introduction

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Water treatment using reverse osmosis (RO) membranes saves energy and space compared with other

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processes and has therefore been widely applied to various systems, such as desalination and waste

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water recycle. Commercially available RO membranes are mainly polyamide composite membranes

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composed of a polyamide rejection layer and polysulfone support membrane [1], which have advantages

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of high water permeability and good rejection performance. The use of RO membranes enables

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treatment of seawater and industrial waste water containing various organic matters, including bacteria

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[2-4], proteins and polysaccharides [5-8]. Organic matters cause a decrease in membrane performance

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by adhesion onto the membrane surface and blocking of membrane pores. In particular, bacteria grow

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onto the membrane surface and form biofilms containing extracellular polymeric substances (EPS) such

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as proteins and polysaccharides [3, 9]. This phenomenon is called “biofouling”. Adhered organic

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matters are generally removed by chemical treatment, including chlorine [10]. However, amide bonds in

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the polyamide membranes are cleaved by chlorine treatment, causing membrane performance to

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decrease [11]. Prevention of bacterial adhesion is important for maintaining RO membranes and long-

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term operation.

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Various approaches for preventing bacterial adhesion onto membrane surfaces have been reported

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[12]. Surface modification with polyethylene glycol (PEG) prevents the adhesion of biological materials

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such as proteins [13, 14], cells [15], and bacteria [16] because of PEG’s high hydrophilicity and large

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extruded volume [17]. PEG has already been applied as a surface modifier to prevent adhesion of

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organic materials such as surfactants and proteins [18-20]. Recently, zwitterionic polymers such as

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sulfobetaine polymers and phosphorylcholine polymers have also been reported to effectively prevent

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adhesion of biological materials [21-24]. Zwitterionic polymers have a similar structure to biological

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membranes and interact with water molecules via electrostatic interaction more strongly than PEG,

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which interacts via hydrogen bond formation [25]. Modification with zwitterionic polymers is effective

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for prevention of bacterial adhesion onto membrane surfaces [26, 27].

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Surface modification with these polymers is generally carried out using a covalent grafting method

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[13, 16, 18-20, 22, 23] or coating method [21, 24, 28, 29]. Although grafting methods have the

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advantage of long-term stability, the modification process causes complexity in the overall membrane

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fabrication process. On the other hand, coating methods, such as the dip coating method and spin

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coating method, can immobilize target molecules much more simply. In addition, modification of a

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target surface is not required. Ishigami et al. reported that RO membranes multilayer-coated using

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oppositely charged polyelectrolytes via electrostatic interaction had resistance against adsorption of

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proteins, although their water permeability was decreased [30]. For water treatment applications, surface

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modification is required to retain the water permeability of the original membranes.

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In this study, we developed a simple and easy modification method for coating phosphorylcholine

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polymer onto a RO membrane via electrostatic interaction to prevent bacterial adhesion. We used

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poly[2-methacryloyloxyethyl

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(p(MPC-co-AEMA)), as a cationic phosphorylcholine polymer. Cationic phosphorylcholine polymer

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has been reported as DNA careers for drug delivery [31-33]. A commercial polyamide RO membrane

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was immersed into an aqueous solution of p(MPC-co-AEMA), and coated via electrostatic interaction

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between the cationic amino groups of p(MPC-co-AEMA) and the anionic carboxyl groups on the RO

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membrane. The surface properties of the coated RO membranes were evaluated by contact angle,

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surface potential, and X-ray photoelectron spectroscopy (XPS). The coating behavior and coating

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stability of p(MPC-co-AEMA) on the RO membrane was characterized by a quartz crystal microbalance

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with dissipation (QCM-D) measurement. The water permeability, salt rejection, and anti-adhesive

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properties against bacteria were evaluated for membrane performance.

phosphorylcholine

(MPC)-co-2-aminoethylmethacrylate

(AEMA)]

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2. Methods

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2.1. Materials

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All chemicals, if not otherwise specified, were obtained from Wako Pure Chemical Industries (Osaka,

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Japan) and were used without further purification. All aqueous solutions were prepared with Milli-Q

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water. A commercial polyamide RO membrane, ES20, was obtained from Nitto Denko Corporation

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(Osaka, Japan). MPC homopolymer and p(MPC-co-AEMA) (MPC : AEMA = 9 : 1, random copolymer;

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Fig. 1), kindly provided by NOF Corporation (Tokyo, Japan), were used as phosphorylcholine polymers.

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The weight-average molecular weight of each phosphorylcholine polymer was evaluated by gel

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permeation chromatography (GPC) using a refractive index detector (RID-10A; Shimadzu Corporation,

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Kyoto, Japan) and Shodex SB-805HQ column (Showa Denko, Tokyo, Japan) at 40°C. A mixed solvent

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comprising 0.1 M NaNO3 aqueous solution and acetonitrile (8/2, v/v) was used as the eluent. The

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weight-average molecular weights of MPC homopolymer and p(MPC-co-AEMA) were 4.6 × 105 and

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9.7 × 105 , respectively.

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Fig. 1

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2.2. Membrane coating using cationic phosphorylcholine polymer

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A polyamide RO membrane was coated by phosphorylcholine polymer via electrostatic interaction. A

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commercial polyamide RO membrane was immersed into an aqueous solution of 0.1 wt%

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phosphorylcholine polymer for 3 h in a refrigerator and washed by gentle shaking twice in an aqueous

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solution of 3.5 wt% NaCl for 1 h to remove non-specifically adsorbed polymers.

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2.3. Characterization of surface properties

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We evaluated surface hydrophilicity, surface potential, and elemental composition of the membrane

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surface. To evaluate surface hydrophilicity of the membranes, the water contact angle was measured

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using a contact angle meter (DM-300; Kyowa Interface Science, Saitama, Japan). To evaluate the

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surface potential of the membranes, the zeta-potential (-potential) was measured with an

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electrophoretic light-scattering apparatus (ELS-4000K; Otsuka Electronics, Osaka, Japan) in 10 mmol/L

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NaCl aqueous solution at pH 7.0. The chemical composition of the membrane surface was analyzed

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using an XPS instrument (JPS-9010MC, JEOL, Tokyo, Japan). The membrane morphology was

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observed using a field scanning electron microscope (FE-SEM; JSF-7500F; JEOL), the same as used in

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our previous study [34].

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2.4. Characterization of coating behavior and coating stability

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The coating behavior and coating stability of p(MPC-co-AEMA) on the RO membrane were

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characterized using a QCM-D instrument (Q-sense E1; BiolinScientific, Västra Frölunda, Sweden). A

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polyamide-coated quartz sensor was prepared using an interfacial polymerization method with trimesoyl

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chloride (TMC; Sigma-Aldrich Corp., St. Louis, MO) and m-phenylenediamine (MPD), commonly used

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to fabricate polyamide RO membranes [11, 35]. Steiner et al. formed a polyamide layer on a gold

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surface, producing a surface similar to of a polyamide RO membrane [36]. We modified their protocol

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for a QCM-D sensor, as shown in Fig. 2. A gold-coated quartz sensor (QSX 301; BiolinScientific) was

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immersed into an ethanol solution of 1 mmol/L 2-aminoethanethiol overnight to aminate the sensor

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surface. The aminated sensor was washed with ethanol twice, dried, and washed with dichloromethane

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(DCM) twice. The sensor was then immersed into a DCM solution containing 1 mmol/L TMC and 1.1

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mmol/L triethylamine for 15 min, and washed twice with DCM, then twice with dimethylformamide

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(DMF). To couple TMC and MPD, the sensor was immersed into a DMF solution of 10 mmol/L MPD,

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and washed twice with DMF. These TMC and MPD coupling reactions were repeated six times. The

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prepared sensor was analyzed by water contact angle and XPS measurements.

4 NH 2

Cl

Cl

O

Cl

CH 3

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Gold-coated quartz sensor

HN CO

CO

NH

SH S

MPD

CO

NH 2

H2N

NH OC

O

TMC

2-aminoethanetiol

H 2N

NH

O

O

Cl

Cl

S CH 3

H 2N

NH2

S

TMC/MPD 6 cycles

CH 3

O

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Fig. 2

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The prepared sensor was placed into the QCM-D instrument. An aqueous solution of 0.1 wt%

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p(MPC-co-AEMA) was supplied for 15 min at 50 L/min, and Milli-Q water was supplied for 1 h to

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evaluate the adsorbed mass of p(MPC-co-AEMA). Consequently, an aqueous solution of 3.5 wt% NaCl,

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which is roughly equal to the salt concentration of sea water, was supplied for 24 h, and Milli-Q water

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was then supplied again for 1 h to evaluate the coating stability under high ionic strength conditions.

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The mass adsorbed onto the quartz sensor was calculated using the Sauerbrey equation [37].

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2.5. Evaluation of membrane performances

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To evaluate membrane performance, the water permeability and NaCl rejection were evaluated using

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a laboratory scale crossflow membrane test unit (Fig. S1, Supplementary data) [34]. An aqueous

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solution of 0.05 wt% NaCl was used as feed water. The effective area of sample membranes was 8.0

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cm2. The flow rate and applied pressure were 1.0 mL/min and 0.75 MPa, respectively. The feed water

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side of the membrane cell was stirred at 300 rpm by a magnetic stirrer. The water permeability and

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NaCl rejection were calculated from the accumulated mass and conductivity of permeate water, the

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latter measured by a conductance meter (CM-30R; DKK-TOA Corporation, Tokyo, Japan).

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2.6. Bacterial adhesion test

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The anti-adhesive property of the membranes was evaluated by immersion into a bacteria suspension

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using Sphingomonas paucimobilis NBRC 13935 as a model strain of Gram-negative bacteria. This

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bacteria has been observed in biofilms on water treatment membranes [38]. Bacteria was cultured in

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tryptic soy broth (Becton, Dickinson and Company, Franklin Lakes, Sparks, MD) medium for 18 h at

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150 rpm at 30°C to reach the mid-exponential growth phase. The precultured bacterial suspension was

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diluted 5 times with tryptic soy broth medium and cultured at 150 rpm at 30°C for 4.5 h. The

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membranes were immersed in the prepared bacterial suspension (adjusted to approximately 108 cfu/mL)

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at 150 rpm at 30°C for 2 h as an initial bacterial adhesion test and for 24 h as a bacterial growth test.

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The living and dead bacteria on the membranes were stained by SYTO 9 and propidium iodide (Life

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Technologies Corporation, Carlsbad, CA), respectively, and observed using a confocal laser scanning

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microscope (CLSM; FV1000D; Olympus, Tokyo, Japan). The observed images were analyzed using

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COMSTAT software [39].

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3. Results and Discussion

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3.1. Characterization of the surface of p(MPC-co-AEMA)-coated membranes

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The membrane surface structures were observed by using FE-SEM (Fig. 3). The p(MPC-co-AEMA)-

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coating did not change the morphology of the membrane surface and the coated membrane maintained

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the rough structure of the polyamide layer.

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A

B

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Fig. 3

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The water contact angles and surface potentials were measured as characteristic membrane physical

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properties (Table 1). The water contact angle measurement showed that the RO membrane immersed

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into the p(MPC-co-AEMA) solution was more hydrophilic than that of the raw RO membrane.

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Conversely, the water contact angle of the RO membranes immersed into an MPC homopolymer

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solution was similar to that of the raw membrane. The surface potential of the RO membrane immersed

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into the p(MPC-co-AEMA) solution was also changed from a negative to a neutral value. These results

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agree with a previous study in which zwitterionic polymers were immobilized by a covalent grafting

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method [26]. It was considered that zwitterionic and hydrophilic p(MPC-co-AEMA) was immobilized

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onto the polyamide RO membranes via electrostatic interaction between the cationic amide groups of

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p(MPC-co-AEMA) and the anionic carboxyl groups on the RO membrane. The MPC groups of p(MPC-

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co-AEMA) were oriented towards the outside of the RO membrane because the surface potential of the

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RO membrane immersed into the p(MPC-co-AEMA) solution did not have the positive value of amino

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groups but rather the neutral value of phosphorylcholine groups.

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Figure 4 shows the XPS spectra for the RO membranes immersed into the p(MPC-co-AEMA)

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solution. The spectrum of the p(MPC-co-AEMA)-coated membrane shows a strong peak of phosphorus

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at 134 eV. This result also indicates the immobilization of p(MPC-co-AEMA) onto the RO membrane.

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Intensity [a.u.]

P 2p

Coated membrane

Raw membrane 134

140

1 2

135 130 Binding Enery [eV]

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Fig. 4

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3.2. QCM-D measurement

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At first, we characterized the prepared quartz sensors. The water contact angles of the bare quartz

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sensor, aminated quartz sensor, and polyamide-coated quartz sensor were 69.8 (S.D. 1.4), 44.0 (1.3),

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and 50.0 (1.7), respectively. The surface of the quartz sensor was hydrophilized by amination with

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cysteamine, and the hydrophilic surface maintained through the polyamide coating. The XPS spectrum

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of the polyamide-coated quartz sensor shows a peak shift for nitrogen from 400.1 to 399.8 eV (Fig. S2,

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Supplementary data). This peak shift was also observed in a previous study [36]. These results show that

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a polyamide layer was successfully formed on the quartz sensor.

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The QCM-D experiments were carried out using the prepared polyamide-coated quartz sensor. Figure

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5 shows the time course of the mass adsorbed on the polyamide-coated quartz sensor. The mass change

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of the quartz sensor became stable immediately after the injection of the p(MPC-co-AEMA) aqueous

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solution and remained constant for 15 min. This indicates that the cationic p(MPC-co-AEMA)

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immediately adsorbed onto the anionic surface of the polyamide membrane via electrostatic interaction,

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and non-specific adsorption or aggregation between p(MPC-co-AEMA) hardly occurred. The mass of

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the adsorbed p(MPC-co-AEMA) was quantified as about 0.67 g/cm2 from the mass change after 1 h of

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the Milli-Q water injection following the p(MPC-co-AEMA) injection. The immobilized polymer-chain

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density of p(MPC-co-AEMA) was calculated as about 0.023 chains/nm2 from the quantified adsorbed

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mass and the weight-average molecular weight measured by GPC. This value is considered reasonable

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because it is comparable to previously reported values [40].

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To evaluate coating stability under high ionic strength conditions, 3.5 wt% NaCl aqueous solution,

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roughly equivalent to the salt concentration of sea water, was injected onto the p(MPC-co-AEMA)-

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adsorbed sensor for 24 h. The mass adsorbed onto the quartz sensor hardly changed for 24 h, and the

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mass of the adsorbed p(MPC-co-AEMA) was 0.50 g/cm2. A difference of 0.17 g/cm2 before and after

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the introduction of salt solution was certainly physical adsorption. This result indicates that once

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p(MPC-co-AEMA) had adsorbed onto the membrane surface via electrostatic interaction, it was not

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easily desorbed, even under high ionic strength conditions. The amino groups of one molecule of

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p(MPC-co-AEMA) were strongly adsorbed via multiple-point electrostatic interactions with the

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carboxyl groups on the surface of the polyamide RO membrane. These results also show that the QCM-

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D measurements presented in this study are potentially useful for investigating adsorption behaviors on

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the surface of polyamide RO membranes for various research fields such as surface modification or

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membrane fouling.

Adsorbed mass [g/cm2]

0.8 0.7 0.6 0.5

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Detachment mass

0.4 0.3 0.2 3.5 wt% NaCl

0.1 0

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Adsorbed mass

0

1

2

3

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23 24 25 26 27 Time [h]

Fig. 5 11

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3.3. Membrane performance of p(MPC-co-AEMA)-coated membranes

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The effect of p(MPC-co-AEMA) coating on membrane performance was evaluated (Table 2). The

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water permeability of the p(MPC-co-AEMA)-coated membranes decreased by about 20% compared

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with bare RO membranes, although salt rejection was maintained at a high value of over 95%, which is

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comparable with commercial membranes. The coated polymer was responsible for the resistance to

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permeation of water molecules. The decrease in water permeability by zwitterionic polymer coating in

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this study was lower than that observed after covalent grafting in previous studies [20, 41, 42]. The

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present method could immobilize zwitterionic polymers while maintaining membrane performance.

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3.4. Bacterial adhesion test

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Figure 6 shows the results of the bacterial adhesion test. After 2 h immersion into the bacterial

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suspension as an initial bacterial adhesion test, bacteria were clearly observed on the raw membrane

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(Fig. 6A), but hardly observed on the p(MPC-co-AEMA)-coated membrane (Fig. 6D). After 24 h, the

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surface of the raw membrane was significantly covered by bacteria (Fig. 6B and C), with a bacteria

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coverage of 41.4% (Table 3). It was concluded that bacteria easily adhered to the surface of the raw

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membrane, grew, and then formed biofilms. However, the surface of the p(MPC-co-AEMA)-coated

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membrane remained clean (Fig. 6E and F), and the bacteria coverage was only 1.0% after 24 h

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immersion. The mass of the adhered bacteria on the p(MPC-co-AEMA)-coated membrane was lower

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than 2% of that on the raw membrane. In the both condition, dead bacteria were not observed (Fig. 6C

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and F). The p(MPC-co-AEMA) immobilized by the coating method successfully prevented initial

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bacterial adhesion and bacterial growth on the membrane surface, similar to a previously reported

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grafting method [27]. This result also indicates that the MPC groups of p(MPC-co-AEMA) were

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oriented towards the outside of the RO membrane, because if the cationic amino groups were oriented

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towards the outside of the RO membrane, dead bacteria or bacterial adhesion would be observed due to

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electrostatic interaction between the cationic groups of p(MPC-co-AEMA) and anionic bacterial

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membranes [26]. The results of the QCM-D measurement and bacterial adhesion test showed the coated

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p(MPC-co-AEMA) was stably adsorbed not only in high ionic strength condition but also bacterial

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broth containing various organic substances and electrolytes.

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Fig. 6

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Conclusions

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We developed a simple coating method for RO membranes using cationic phosphorylcholine

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polymers via electrostatic interaction to prevent bacterial adhesion. By immersing RO membranes into

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an aqueous solution of cationic phosphorylcholine polymer, p(MPC-co-AEMA), the surfaces were

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readily coated by a phosphorylcholine polymer via electrostatic interaction between the cationic amino

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groups of AEMA and the anionic carboxylic groups on the polyamide RO membrane. The surface of the

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p(MPC-co-AEMA)-coated membrane was hydrophilic, and the surface potential was neutral, specific

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for zwitterionic polymers. A QCM-D measurement showed that the mass of p(MPC-co-AEMA)

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adsorbed onto the RO membrane was 0.67 g/cm2, and 0.50 g/cm2 of p(MPC-co-AEMA) was stably

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adsorbed over 24 h under high ionic strength conditions equivalent to sea water. The p(MPC-co13

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AEMA)-coated membrane showed a high anti-adhesive property against a model strain of Gram-

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negative bacteria, Sphingomonas paucimobilis, while maintaining membrane performance. The methods

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described herein are expected to be useful for long-term operation of RO membranes.

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FIGURE CAPTIONS

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Fig. 1. Chemical structure of p(MPC-co-AEMA). m : n = 9 : 1.

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Fig. 2. Scheme for the preparation of the polyamide-coated quartz sensor for QCM-D measurement.

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Fig. 3. FE-SEM images of the surface of a raw RO membrane (A) and p(MPC-co-AEMA)-coated RO

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membranes (B). Bars indicate 1 m.

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Fig. 4. XPS P 2p spectra for p(MPC-co-AEMA)-coated polyamide RO membranes.

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Fig. 5. Time course for the mass adsorbed on the polyamide-coated quartz sensor by QCM-D

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measurement. An aqueous solution of 0.1 wt% p(MPC-co-AEMA) was supplied for 15 min at 50

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L/min, and Milli-Q water was supplied for 1 h. Consequently, an aqueous solution of 3.5 wt% NaCl

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was supplied for 24 h, and Milli-Q water was again supplied for 1 h.

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Fig. 6. Microscopic images of bacteria on the p(MPC-co-AEMA)-coated membranes after the bacterial

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adhesion test, analyzed using COMSTAT software. In the CLSM images (C and F), the living and dead

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bacteria were indicated by green and red color, respectively.

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TABLES

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Table 1. Surface properties of RO membranes immersed into various polymer solutions. Raw membrane

MPC homopolymer- p(MPC-co-AEMA)coated membrane coated membrane

Water contact angle [°]

36.0 (1.9)

30.0 (2.2)

18.6 (2.1)

Zeta potential* [mV]

-15.36 (0.94)

no data

-0.50 (1.72)

Numbers in parentheses indicate standard deviations. *Zeta potentials were measured in 10 mmol/L NaCl aqueous solution at pH 7.0. 6 7

Table 2. Performance of the RO membranes. Raw membrane

p(MPC-co-AEMA)-coated membrane

Water permeability [m3/m2 day]

0.997 (0.058)

0.755 (0.090)

NaCl rejection [%]

94.7 (0.7)

96.9 (0.4)

Numbers in parentheses indicate standard deviations. 8 9

Table 3. Quantification of biofilms on the membranes after the bacterial adhesion test. Raw membrane

p(MPC-co-AEMA)-coated membrane

Incubation time

2h

24 h

2h

24 h

Adhered bacteria [m3/m2]

0.58

3.78

0.05

0.05

Substratum coverage [%]

13.8

41.4

2.2

1.0

Maximum thickness (m)

10.60

17.10

6.49

8.26

10 11 12 15

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GRAPHICAL ABSTRACT

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