Development of Multimodal Antibacterial Surfaces Using Porous

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Applications of Polymer, Composite, and Coating Materials

Development of Multimodal Antibacterial Surfaces Using Porous Amine-Reactive Films Incorporating Lubricant and Silver Nanoparticles Jieun Lee, Jin Yoo, Joonwon Kim, Yeongseon Jang, Kwangsoo Shin, Eunsu Ha, Sangryeol Ryu, Byung-Gee Kim, Sanghyuk Wooh, and Kookheon Char ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b20092 • Publication Date (Web): 14 Jan 2019 Downloaded from http://pubs.acs.org on January 15, 2019

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ACS Applied Materials & Interfaces

Development of Multimodal Antibacterial Surfaces Using Porous Amine-Reactive Films Incorporating Lubricant and Silver Nanoparticles Jieun Lee,†,‡ Jin Yoo,†,‡ Joonwon Kim,§ Yeongseon Jang,# Kwangsoo Shin, ⊥ Eunsu Ha,ǁ Sangryeol Ryu,ǁ Byung-Gee Kim,§ Sanghyuk Wooh¶,* and Kookheon Char†,* †The

National Creative Research Initiative Center for Intelligent Hybrids, School of Chemical

and Biological Engineering, Seoul National University, Seoul 08826, Republic of Korea, §Institute

of Molecular Biology and Genetics, School of Chemical and Biological Engineering,

Seoul National University, Seoul 08826, Republic of Korea, #Department of Chemical Engineering, University of Florida, Gainesville, FL 32611, USA,

⊥ School

of Chemical and

Biological Engineering, Seoul National University, Seoul 08826, Republic of Korea, ǁDepartment

of Food and Animal Biotechnology, Department of Agricultural Biotechnology,

and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Republic of Korea, ¶School of Chemical Engineering & Materials Science, Chung-Ang University, Seoul, 06974, Republic of Korea ‡These

authors contributed equally to this work.

KEYWORDS poly(pentafluorophenyl acrylate) • anti-biofouling • bactericidal• silver nanoparticles • lubricant

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ABSTRACT

Anti-biofouling has been improved by passive or active ways. Passive antifouling strategies aim to prevent the initial adsorption of foulants, while active strategies aim to eliminate proliferative fouling by destruction of the chemical structure and inactivation of the cells. However, neither passive antifouling strategies nor active antifouling strategies can solely resist biofouling due to their inherent limitations. Herein, we successfully developed multimodal antibacterial surfaces for waterborne and airborne bacteria with the benefit of combination of anti-adhesion (passive) and bactericidal (active) properties of the surfaces. We elaborated multi-functionalizable porous amine-reactive (PAR) polymer films from poly(pentafluorophenyl acrylate) (PPFPA). Pentafluorophenyl ester groups in the PAR films facilitate to create multiple functionalities through a simple post-modification under mild condition, based on their high reactivity towards various primary amines. We introduced amine containing-polydimethylsiloxane (amine-PDMS) and dopamine into the PAR films, resulting in infusion of antifouling silicone oil lubricants and formation of bactericidal silver nanoparticles (AgNPs), respectively. As a result, the PAR film-based AgNPs incorporated lubricant infused surfaces demonstrate outstanding antibacterial effects toward both waterborne and airborne Escherichia coli (E. coli), suggesting a new door to develop an effective multimodal anti-biofouling surface.


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INTRODUCTION

Microbial fouling on surfaces causes numerous issues in our daily life and various fields of industry, e.g. infections from sink drain, food processing and medical implant, and high water resistance of water transportations.1 Biofouling, also called biocontamination, mostly originates from bacteria adhesion on surfaces. Bacteria primarily present on surface as robust community by colonization, known as biofilm, which is extremely difficult to eliminate from the surface due to high antibiotics resistance of the biofilm of bacteria.2 Mechanical removal of bacterial biofilms or sterilization techniques such as UV radiation, dry heat and autoclave can induce biofilm removal,3 however, they can may have strong impact or damage to the surfaces.4 Therefore, initial bacterial adhesion should be inhibited in order to protect surfaces from biofouling. For the last decades, various surfaces, such as superhydrophilic, zwitter-ionic, superhydrophobic, and lubricant infused surfaces, have been applied to reduce bacterial adhesion on surfaces.5, 6 Especially, surfaces infused with lubricant have gained attention for remarkable bacteria-repellent property attributing to low surface tension of slippery lubricant.710

According to the slippery Wenzel state, liquid droplets easily slide on the smooth dynamic

liquid layers of lubricant infused surfaces (LISs).11, 12 LISs exhibit excellent anti-biofouling performance due to the exceptionally low bacterial adhesion and biofilm formation prevention on their mobile lubricant surfaces.10 Biofouling can also be suppressed by damaging bacteria. This approach, named bactericidal method, has focused on killing bacteria via two different ways, contact-killing and/or biocide leaching. The contact-killing seeks to induce death of bacteria adhering to surfaces by biochemical way. The biocide leaching by cytotoxic compounds released from surfaces causes 3 ACS Paragon Plus Environment


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death of either nearby or adhered bacteria.13, 14 Development of effective antibacterial surfaces using silver nanoparticles (AgNPs) has been received considerable interest due to their broadspectrum biocidal activity and simple strategy.15 The antibacterial mechanisms of AgNPs have been proposed as below: (i) altering the membrane properties of adhered bacteria on AgNPs (contact-killing) and (ii) releasing antibacterial Ag+ ions from AgNPs (biocide leaching).15-17 Though bactericidal surfaces prevent biofilm formation by living bacteria, the surface can be fouled by dead bacteria and debris following contacting biofluids. This fouling layer would block the surface-tethered bactericidal agents, thereby inactivating bactericidal functionality.18, 19

Therefore, a monofunctional bactericidal coating is insufficient for preventing biofilm

formation. In the other words, to achieve highly effective anti-biofouling surfaces, integration of bactericidal and bacteria-repellency is highly in demand.9, 20-21 Herein, we present a simple strategy for developing lubricant-infused surfaces containing AgNPs. We utilized poly(pentaflourophenyl acrylate) (PPFPA) to realize effective antibiofouling and antibacterial surfaces, which has aroused interests due to its high reactivity with amines under mild conditions and resistance towards hydrolysis.22-28 To retain lubricant in films, porous structures of PPFPA films were developed by vapor-induced phase separation (VIPS) of polystyrene (PS)/PPFPA mixture and selective removal of PS. Attributing to excellent amine-reactive property of PPFPA, porous amine-reactive (PAR) films enable imparting versatile physiochemical functionalities on surfaces via sequential postpolymerization modification. Amine-containing molecules (i.e., amine-polydimethylsiloxane (amine-PDMS) and dopamine) and AgNPs were introduced on PAR films in serial order, followed by silicone oil infusion into PAR films. We adopted silicone oil (trimethylsilyloxyterminated PDMS) as lubricant material since it shows good compatibility with PDMS tethered PAR films owing to the same chemical structure resulting in thermodynamically stable 4 ACS Paragon Plus Environment

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lubricant coating and outstanding liquid repellency.11 In addition, it is also known for more cost-effective than other commonly used lubricating oils (e.g., perfluoropolyethers). Antibacterial efficiency of the developed surfaces was assessed for both waterborne and airborne Escherichia coli (E. coli). We confirmed that lubricant-infused PAR films inhibit adhesion of not only waterborne bacteria but also airborne bacteria. To the best of our knowledge, this is the first study to utilize slippery surfaces as antibacterial surfaces for airborne bacteria. However, as previous studies have demonstrated that contact-killing strategy is necessary to minimize airborne bacterial adhesion,29, 30 the LISs were insufficient to prevent airborne bacteria adhesion thoroughly. On the contrary, the AgNPs incorporated lubricant infused surface showed nearly perfect antibacterial efficiency for airborne bacteria owing to bacterial resistance of AgNPs.31, 32 The aim of this work is to develop efficient and multimodal antibacterial surfaces toward both waterborne and airborne bacteria as the first proof of concept for application of PAR films with multi-functionalities by post-modification.

EXPERIMENTAL SECTION

Materials Poly(pentafluorophenyl acrylate) (PPFPA) with weight-average molecular weight (Mw) of ~47,000 g/mol was synthesized as previously described (Figure S1).28 Polystyrene (PS, Mw ~184,000 g/mol), Poly[dimethylsiloxane-co-(3-aminopropyl)methylsiloxane] (amine-PDMS, eq. wt. 4,400 Amine), crystal violet (CV), and silicone oil (viscosity: 100 cSt) were purchased from Sigma-Aldrich. 4’,6-diamidino-2-phenylindole dihydrochloride (DAPI) and propidium iodide (PI) were purchased from Thermo Fisher Scientific Inc. All the chemicals and solvents were used as received. Deionized (DI) water was used throughout the study. Fabrication of Porous Amine-Reactive (PAR) Films A mixture of PS and PPFPA (PS/PPFPA=70/30, w/w) was dissolved in tetrahydrofuran (THF) for 5 wt % solution. The 5 ACS Paragon Plus Environment


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silicon (Si) wafer or glass substrates were cleaned in piranha solution (a mixture of 70 vol % H2SO4 and 30 vol % H2O2) for 1 hr at room temperature (RT) before casting the solution onto substrates. The polymer solution was casted on Si substrates, and then spin-coated with a 1,000 rpm spinning rate for 25 s in the closed chamber under controlled relative humidity (RH).33-35 Then the blend films were exposed to cyclohexane at 40 °C for 1 hr allowing selectively removal of PS domains to obtain PAR films.36, 37 Multi-Component Modification of PAR Films Pentafluorophenyl (PFP) units of the PAR films were functionalized by dipping the prepared films in a 50 mg/mL aqueous solution of dopamine hydrochloride for 6 hrs, followed by immersing them in 10 vol % aminePDMS/hexane solution for overnight. The obtained dopamine and PDMS functionalized PAR (DP-PAR) films were placed in a freshly prepared AgNO3 (50 mM) aqueous solution. After 6 hrs, the resulted product, AgNPs-modified DP-PAR (Ag@DP-PAR) films, were achieved from the solution, then washed thoroughly with DI water and dried under a stream of nitrogen. All the functionalization steps were conducted under shaking. Subsequently, lubricant-infused (Linfused) Ag@DP-PAR films were obtained by spin-coating of silicone oil at 3,000 rpm for 30 s. The fabrication process of L-infused Ag@DP-PAR films are illustrated in Scheme 1. For biofilm coverage analysis, all samples were coated on both sides of slide glasses.

Scheme 1. Schematic illustration of fabrication process of the lubricant-infused dopamine, PDMS functionalized porous amine-reactive films decorated with AgNPs (L-infused Ag@DPPAR films).


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Characterization The surface morphologies of initial and post-functionalized PAR films were characterized by tapping-mode atomic force microscopy (AFM, Innova, Veeco, USA) and scanning electron microscopy (SEM, JSM-6701F, JEOL, Japan) following Pt coating using a sputter coater. The pore size and porosity of the porous film was analyzed using an image processing software, Image J (National Institutes of Mental Health, USA), based on previous studies.34, 35 AFM images were adjusted to black/white binary phase, and the portion of black area to the total area was considered as the porosity of membrane. We assumed the pores in the membrane were in circular shape, thus the pore diameters were calculated from the value of the area of each circle. To determine the thickness of films, we scratched the film with a scalpel blade and measured the depth of the scratch using AFM. Tapping-mode silicon probes of nominal spring constant of 40 N/m and resonant frequency of 330 kHz was used for tapping mode scans. For recording the topography of surface, scan rate was set to 1.0 Hz, while the tip was engaged at a low scan rate of 0.2 Hz when carry out a large-scale scan to measure thickness. The chemical composition of the film was analyzed by Fourier transform infrared spectroscopy (FT-IR, Tensor27, Bruker, Germany), energy-dispersive X-ray spectroscopy (EDS, X-MaxN, Oxford Instruments, England), and X-ray photoelectron spectroscopy (XPS, Sigma Probe, VG, UK). The XPS spectra were acquired using XPS system equipped with a 275 mm mean diameter spherical sector analyzer and a micro-focused monochromatic Al energy source (1486.6 eV). The take-off angle was set at 53 °. The pressure in the analysis chamber was below 5 × 10-9 mbar. Acquired data were fitted by Thermo Avantage software. Water and ethanol contact angle measurements were performed on a contact angle meter (Phoenix 150, SEO, Korea) with a 5 μL droplet. Absorbance intensity for biofilm coverage analysis was obtained from UV-Vis absorbance spectra (Lambda 35, PerkinElmer, USA). Fluorescence analysis was performed with confocal laser scanning microscope (CLSM, LSM 780, Carl Zeiss, Germany). For the assessment of silver release profile, silver ion concentration from the 7 ACS Paragon Plus Environment


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Ag@DP-PAR and L-infused Ag@DP-PAR films were detected using inductively coupled plasma-mass spectrometry (ICP-MS, Varian 820-MS, Varian, Australia). The modified surfaces were immersed in 1 mL of DI water at RT without stirring in darkness. The solution was extracted after 6, 24 and 48 hrs. Biofilm Coverage Analysis Tests against biofilm formation were performed by immersing the bare, Ag@DP-PAR and L-infused Ag@DP-PAR glasses in Escherichia coli (E. coli) DH5α stock solution with a density of 3 × 109 CFU (colony forming unit)/mL at 37 °C for 6, 24 and 48 hrs. Afterwards, the incubated substrates were removed and immediately dipped into a 0.1 % (w/v) aqueous CV solution for 10 min. Each sample was gently rinsed with DI water to remove excess dye. The quantification of biofilm coverage was performed by adding same amount of ethanol on each stained film to extract CV completely followed by absorbance measurement at 590 nm of the dissolved CV solution. Bactericidal Test The bactericidal activity of the films for waterborne bacteria was investigated by following four methods. To analyze antibacterial activity on waterborne bacteria by surface contact, E. coli, Bacillus cereus (B. cereus), and Staphylococcus aureus (S. aureus) cells were washed twice with pH 7.4 Phosphate Buffered Saline (PBS buffer) and diluted to 3 × 107 CFU/mL for E. coli and 1 × 107 CFU/mL for B. cereus and S. aureus. 100 μL of cell suspension was added onto each surface and incubated at 30 °C for 6 hrs. PDMS ring was placed on modified surfaces to prevent leakage of bacterial suspension. The incubated cell suspensions were harvested, sequentially diluted, and spread onto Lysogency broth (LB) agar plates for E. coli to count the number of viable colonies. For B. cereus and S. aureus, the incubated cell suspensions were harvested, sequentially diluted, and spread onto BHI (Brain Heart Infusion) and TSB (Tryptic Soy Broth) agar plates to count the number of viable colonies, respectively. The whole set of experiments were performed in triplicate. In case of CLSM analysis for viability of cells attached to surfaces, the substrates were incubated at 37 °C in the 8 ACS Paragon Plus Environment

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cell suspension with a density of 3 × 107 CFU/mL. After 16 hrs contact, all samples were washed twice with PBS buffer and stained using DAPI (15 μg/mL) and PI (5 μg/mL) in dark for 15 min. The stained bacterial cells were observed under CLSM. To obtain SEM images of bacteria, each substrate was immersed in E. coli suspension (3 × 108 CFU/mL) for 18 hrs, and after that the attached bacteria were fixed. Samples were dipped into 2.5 % (v/v) glutaraldehyde for 30 min, washed and dehydrated by soaking in ethanol-water solution for each 20 min in series (for each step, ethanol concentration were made of 20 %, 50 %, 70 %, 90 % and 100 %). Lubricant was carefully removed using hexane followed by SEM observation. For inhibition zone assay, LB agar plates to test growth inhibition were prepared by streaking into 3 × 108 CFU of E.coli cells using swabs to test growth inhibition. The samples for the assay were placed on the LB agar plates and incubated at 37 °C for 24 hrs. For airborne tests, E. coli cells were resuspended in water with 108 CFU/mL of concentration. The bacterial suspension was sprayed onto samples using chromatography sprayer. Following spraying a fine mist of the cell suspension onto surfaces, samples were then placed on empty petri dishes and air-dried for 5 min. Then, the samples were covered with autoclaved LB agars that had been allowed to cool to approximately 40 °C. After the agar had solidified, the samples were incubated at 37 °C for 48 hrs. All the experiments were performed on a clean bench to avoid introduction of other bacteria. For the assessment of AgNPs release profile from the Ag@DP-PAR and L-infused Ag@DP-PAR films, silver ion concentration was detected by ICP-MS. Each film-coated Si wafers were immersed in 1 mL of DI water at RT without stirring in darkness. DI water containing released silver ions was collected after 6 hrs, 24 hrs, and 48 hrs.



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RESULTS AND DISCUSSION Fabrication of Lubricant Infused AgNPs Incorporated Porous Amine-Reactive Films In this study, we fabricated porous amine-reactive (PAR) films as a platform of anti-biofouling materials. A variety of functional groups can easily be incorporated into the porous structures through

facile

post-polymerization

modification

of

reactive

polymer

matrix.

Poly(pentafluorophenyl acrylate) (PPFPA) as well-known amine-reactive polymer was applied since the activated ester groups present along its polymer chain shows excellent reactivity towards primary and secondary amines even under mild conditions, e.g., at room temperature, with high yields.28 We successfully obtained PPFPA porous amine-reactive (PAR) films by vapor-induced phase separation (VIPS) of polystyrene (PS)/PPFPA blends followed by selective removal of PS moiety. For preparation of the PAR films, a simple spin-coating technique was adopted which was done in 25 s. The VIPS process is widely used to fabricate porous membrane in polymeric system. In particular, previous studies published from our group have reported development of porous and ultrathin membranes with different polymers via VIPS process.33-35 Due to the strong hydrophobic nature of PPFPA, casting PPFPA solely was insufficient to induce formation of pores in films (Figure S2). PS/PPFPA blends instead have been successfully developed porous structures on film surfaces. By addition of PS, a less hydrophobic polymer compared to PPFPA, the water vapor could be drawn onto the casting solution, resulting in production of micro- and nano-sized pores in thin films by VIPS.38 Subsequently, the PS domains were extracted from the blend films with cyclohexane, a PS selective solvent, without deteriorating the remained PPFPA structures. Figure 1 shows the surface morphology of PS/PPFPA films (prepared at different relative humidity (RH)) before and after etching PS with cyclohexane. For as spincast PS/PPFPA blend films, porous surfaces were achieved at a high RH (> 90 %) condition 10 ACS Paragon Plus Environment

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while no pores were observed at a low RH (< 30 %) condition. With selective dissolution of PS in cyclohexane, the different surface morphologies of films have been obtained depending on initial spin-coating condition. After PS removal, PPFPA films formed under high RH showed continuous networks of PPFPA having pores and island-like domains, while that formed under low RH exhibited the isolated islands surface morphology composed of PPFPA only with no pores. The pores formed on polymer blend films during the VIPS process determine the final structure of the PPFPA films and the corresponding surface properties, such as hydrophobicity measured by contact angle (Table S1). The porous films fabricated at high RH have an average pore size of 590nm with 36% porosity (Figure S3). To the best of our knowledge, this is the first study to develop porous PPFPA films showing amine-reactivity with simple fabrication method. Notably, phase separation was induced in present system not only by water vapor but also by polymer blends. Most polymer blends of high molecular weight polymers are intrinsically immiscible, and therefore phase separation occurs due to vanishing entropy of mixing.39 Thus, by controlling the weight ratio of PS/PPFPA polymer blends, the surface morphology of the thin films can be effectively tuned.40 The pore size and film thickness decrease along with the decrease of PPFPA fraction in the blends while the uniformity of pore size distribution increased (Figure S4 and S5). According to previous studies, lubricant-infused liquid repellent films require rough surfaces with adequate thickness to retain lubricant inside.41, 42 Also, if lubricant forms a uniform layer on film surfaces, the effect of the surface structure on the wettability could be marginal.43 Aside from this, the lubricant retention ability of films is rather significant. Collectively, for antifouling and antibacterial applications, the films with 7:3 weight ratio of PS/PPFPA blends were prepared at high RH as this condition allows the formation of well-defined porous structures with thick enough film.



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Figure 1. Surface morphology of blend films after vapor-induced phase-separation (VIPS) and selective removal of PS with cyclohexane. (a) FE-SEM images and (b) AFM topography of the blend films. (scale bars = 4 μm) As shown in Figure 2a, pentafluorophenyl (PFP) units of PAR films were multi-functionalized by sequential reactions with two amine-containing molecules; dopamine and amine-PDMS to create dopamine and PDMS functionalized porous amine-reactive (DP-PAR) films. It has been reported that catechol functional group facilitates formation of silver nanoparticle (AgNP)s,44 therefore, we chose dopamine to introduce catechol moieties on PAR films for further AgNP incorporation. Due to the presence of amine groups in dopamine, dopamine can be grafted to 12 ACS Paragon Plus Environment

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PPFPA through substitution reaction. The PAR films were immersed in dopamine solution first allowing partial modification of PFP units. Subsequently, the dopamine substituted PAR films were placed in amine-PDMS solution overnight for the remaining PPFPA residues to react enough to increase film hydrophobicity. This strategy to convert physiochemical property of film surfaces from PPFPA into PDMS improves compatibility between polymer matrix and silicone oil lubricant by minimized interface energy. Successful grafting of both dopamine and amine-PDMS to PPFPA proved that the post-modification of PAR films facilitates endowing more than two different chemical functionalities simultaneously on PAR films via serial substitutions. Surface chemical composition of films for each treatment step were confirmed by Fourier transform infrared spectroscopy (FT-IR) spectra in ATR (attenuated total reflectance) mode (Figure 2c). Differing from PS/PPFPA blends, the IR spectrum of PAR film indicated that PPFPA is the only component remained after treated in cyclohexane. After subsequent reactions with dopamine and amine-PDMS, the DP-PAR film presented strong absorption band of amide at 1638 cm-1 while the characteristic PFPA C=O ester stretch at 1782 cm-1 and C-C aromatic stretch at 1520 cm-1 were decreased. In order to prepare AgNPs incorporated porous amine-reactive (Ag@DP-PAR) films, the DPPAR films were exposed to AgNO3 solution. The catechol group of dopamine spontaneously reduced Ag+ ions to Ag0 allowing in-situ AgNPs synthesis onto film surfaces without introduction of any additional reducing agents or UV/VIS light irradiation.45-47 Although, PDMS was functionalized on PAR film after dopamine substitution, the catechol groups of dopamine successfully reduced Ag+ into Ag NPs. The surface morphology of the Ag@DPPAR films was verified by SEM images (Figure 2c) and the surface chemical composition including Ag contents on the film surfaces was examined by EDS (Figure S7). As shown in SEM images, the initial porous structures of PAR films were preserved even after PPFPA 13 ACS Paragon Plus Environment


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modification with dopamine and PDMS. Moreover, well-defined AgNPs (67.5 ± 13.5 nm on average) have decorated on the surfaces of the functionalized PAR films in high density, as was verified by EDS spectra. The wide XPS spectra for surface characterization are shown in Figure 2d. The characteristic Ag(0) 3d peaks of Ag@DP-PAR film were detected in XPS wide scan, and furthermore, the high resolution Ag 3d spectrum could be fitted into two peaks, 373.96 (Ag 3d3) and 367.89 eV (Ag 3d5) confirming that the in-situ formed AgNPs were successfully anchored on the film surfaces.44, 48 In addition, the high resolution C 1s spectrum was deconvoluted into three bonds, C-C, C-N, and C=O bonds at 284.46, 285.55 and 287.86 eV,49 respectively, indicating amide bond formation as a result of the reaction of PPFPA with amines. In the wide XPS spectra of DP-PAR and Ag@DP-PAR films compared with PAR film, the N 1s peak arose after substitution while the F 1s peak disappeared. Also, the changes observed in high resolution O 1s spectrum supports the post-modification of PAR films with amine-PDMS (Figure S6). The characteristic O 1s peaks of PAR films were deconvoluted into carbonyl O and methoxy O peaks due to pentafluorophenyl acrylate moiety. After functionalization, the DP-PAR and Ag@DP-PAR films had dominant Si-O-Si arising from PDMS moiety.


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Figure 2. Characterization of multi-functionalized PAR films. (a) Schematic showing the fabrication of dopamine and amine-PDMS functionalized PAR (DP-PAR) films and AgNPsincorporated DP-PAR (Ag@DP-PAR) films. (b) FT-IR (ATR) spectra of PS/PPFPA blends, PAR and DP-PAR films. (c) Surface morphology of Ag@DP-PAR films characterized by SEM. The marked yellow circle indicates synthesized Ag NPs with an average size of 67.5 nm. (scale bar = 5 μm; inset scale bar = 1 μm). (d) XPS wide scan of PAR, DP-PAR and Ag@DPPAR films; (i, ii) high-resolution XPS Ag 3d and C 1s spectra for Ag@DP-PAR films. (iii) relative atomic concentration of C, N, O, F and Ag elements. Recent studies have shown that infusion of lubricant into porous polymer films creates slippery surfaces for effective reduction in biofouling.7-10 Applying lubricant infused surfaces (LISs) to 15 ACS Paragon Plus Environment


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a substrate requires a porous structure with proper surface chemical functionalization in order that a liquid lubricant with lower surface energy can completely wet the substrate.50 We prepared lubricant-infused Ag@DP-PAR (L-infused Ag@DP-PAR) films by spin-casting silicone oil onto Ag@DP-PAR films. Since the hydrophobic PDMS matrix and silicone oil lubricant have the same chemical structures, the interface energy of lubricant and substrate is minimized (nearly zero) that results in highly stable lubricant coating. Figure 3a shows digital image of various PAR derivative films. PAR, DP-PAR and Ag@DP-PAR films were opaque when observed with the naked eye, compared to the bare glass. However, L-infused Ag@DPPAR films turned nearly transparent after lubricant infusion. Optical transmittance measurements also showed enhanced optical transmittance in lubricant-infused film (Figure S8). In addition, these digital images exhibit the stability of films without detachment of films from surface after several steps of functionalization. To evaluate liquid sliding behavior, water droplets were placed on top of the bare and L-infused Ag@DP-PAR film-coated glasses initially standing horizontal and later tilted (Figure 3b). Purple dye was added to the water droplets to aid visualization here. On the bare glass, the water droplet spread widely leaving a long trail behind once it slid. In contrast, water slid down readily without any trail of liquid on the surface of L-infused Ag@DP-PAR films, no remaining trail or stain along the sliding path of water droplet was observed after sliding. However, on the surface of the bare glass, the purple staining was still present even after washing the glass. Furthermore, for L-infused Ag@DP-PAR film-coated glass, a tilt angle of 10 ° was sufficient for water droplet to slide down the surface. The time-lapse images of sliding motions of water and ethanol droplets on tilted L-infused Ag@DP-PAR film surfaces were observed as shown in Figure 3c. In order to further investigate sliding behavior on various surfaces, we measured sliding angles, i.e., the lowest angle substrate needs to be tilted allowing liquid droplets slide 16 ACS Paragon Plus Environment

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off (Table 1). Droplets of water pinned to both bare glass and non-infused Ag@DP-PAR film surfaces even at vertical inclination. On the other hand, ethanol which has much lower surface tension than water spreads on those surfaces, indicating wetting behavior. However, on the lubricant-infused surfaces, both water and ethanol were able to slide off when substrates were tilted less than 10 °. Sliding angles of water and ethanol droplets on the L-infused Ag@DPPAR film surfaces were 8.7 ° and 8.0 °, respectively. This outstanding liquid repellency of the L-infused Ag@DP-PAR films showed the potential of biofouling resistant behavior, which is discussed below.



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Figure 3. Liquid sliding behavior of Ag@DP-PAR films compared with bare glass. (a) Digital photographs of PAR derivative films before and after lubricant infusion compared with bare glass. (b) Photographs of a droplet of water (purple dye added to aid visualization) placed on the bare glass and L-infused Ag@DP-PAR films before and after tilting from horizontal to the angles indicated. (c) Time-sequence photographs showing the dynamic mobility of water (left) and ethanol (right) droplets (5 μL) on the L-infused Ag@DP-PAR films at tilting angle ~ 10 ° (scale bar = 5 mm). 18 ACS Paragon Plus Environment

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Table 1. Sliding behavior of water and ethanol on dry and L-infused Ag@DP-PAR films compared to bare glass. Sliding angles (°) of water and ethanol droplets (5 μL) on bare glass, Ag@DP-PAR, and L-infused Ag@DP-PAR films. Water

Ethanol

Sample

Bare glass

Ag@DP-PAR

L-Infused Ag@DP-PAR

Bare glass

Ag@DP-PAR

L-Infused Ag@DP-PAR

Sliding Angle (°)

pinned

pinned

8.7 ± 1.3

wetting

wetting

8.0 ± 0.8

Bacteria Repellency by Lubricant Layer To demonstrate bacteria repellency of our lubricant infused multi-functionalized films, the adhesion behavior of E. coli on L-infused Ag@DP-PAR film surfaces under static culture condition was evaluated. Bare glass and non-infused Ag@DP-PAR films were used as control samples to demonstrate biofilm formation. After sufficient time of incubation in E. coli medium, bacterial biofilm was formed on substrates. Both bare glass and non-infused Ag@DP-PAR films failed to resist biofilm attachment resulting in purple color over entire substrates by CV staining, as shown in Figure 4a. In contrast, little or no CV stains were observed on L-infused Ag@DP-PAR films. For the quantitative analysis of biofilm adhesion, we compared the amounts of CV dye bound to each film sample by UV/VIS spectroscopy. CV was extracted from stained films, then the absorption intensity of each CV solution was measured at 590 nm, its maximum absorption wavelength (Figure 4b and Figure S9). The absorption intensities were normalized by the 24 hrs E. coli medium-immersed bare glass sample. With 6 hrs of immersion in bacteria medium, bare and Ag@DP-PAR film-coated glasses showed average normalized absorbance of 1.05 and 1.34, while the L-infused Ag@DP-PAR film-coated glass exhibited 0.62, indicating that the effects on preventing biofilm formation are apparent. Compared to visual inspection of the stained substrates (Figure 4a), however, the quantified amounts of CV on L-infused Ag@DP-PAR films showed higher value due to the attached bacteria at the uncoated edge of substrates. The incomplete surface coating led to biofilm formation on the uncoated edges, leaving some 19 ACS Paragon Plus Environment


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residual staining. As the immersion time increased to 48 hrs, E. coli attachment significantly increased, resulting in average normalized absorption intensity of 3.17 and 5.82 for the bare and Ag@DP-PAR film-coated glasses, respectively. In the case of L-infused Ag@DP-PAR film, the average intensity was about 2.40 corresponding to approximately 75 % reduced staining relative to the non-infused control samples. The slippery L-infused Ag@DP-PAR film surfaces were effective in resistance against bacterial attachment and colonization compared bare glass and non-infused control samples.

Figure 4. Bacteria-repellent activity of the bare glass, Ag@DP-PAR and L-infused Ag@DPPAR films. (a) Photographs and (b) normalized absorbance intensity (measured at 590 nm) of CV eluted solution from bare glass, Ag@DP-PAR, and L-infused Ag@DP-PAR films. Each film was previously stained with CV after exposure to the E. coli solution for 6, 24 and 48 hrs, and then dye was extracted with ethanol for further analysis. Waterborne Bactericidal Tests The bactericidal activity of AgNPs-incorporated PAR films was investigated by streaking bacteria on agar plates (Figure 5a). E. coli suspension was seeded on the bare Si wafer, L-infused DP-PAR, and L-infused Ag@DP-PAR film surfaces and cultured in contact for 6 hrs. To secure bacterial suspension against leakage on surfaces, PDMS 20 ACS Paragon Plus Environment

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ring was used as shown in Figure 5a. Then, the bacterial suspension was extracted and diluted in series for the measurement of colony forming unit number (CFU) by plate counting method. For the bare Si wafer and L-infused DP-PAR film-coated substrates, high number of bacterial colonies were displayed on the agar plates. On the contrary, after the incorporation of AgNPs into the film surfaces, no viable bacterial colonies remained for L-infused Ag@DP-PAR films indicating that E. coli was perfectly killed. Additionally, besides E. coli (Gram-negative) cells, we confirmed bactericidal activity of the modified surfaces toward Gram-positive bacteria (B. cereus and S. aureus). It was observed that all of the B. cereus and large amount of S. aureus were killed through contact with bacteria solution and AgNPs-conjugated surfaces (Figure S10). The modified surfaces showed high efficacy of bactericidal properties toward both Grampositive and Gram-negative bacteria cells. For further confirmation of the contact bactericidal property, the physiological condition of bacteria grown on the various substrate surfaces was characterized by confocal laser scanning microscope (CLSM) (Figure 5b). The bare, DP-PAR, L-infused DP-PAR, Ag@DP-PAR, and L-infused Ag@DP-PAR film-coated glass substrates were incubated overnight with E. coli suspension. Bacterial cells on the surfaces were stained either in blue (live and dead cells) or red (dead cells) by two nucleic acid stains, DAPI and PI. The fluorescence excitation of the DAPI (blue dye) and PI (red dye) were detected in two separate channels of blue and red, which appeared as the left and middle columns of Figure 5b, respectively. The two captured blue and red channel images were later overlaid, showed as the right column of Figure 5b. The pink colored bacteria in Figure 5b represented overlaid images of DAPI stained (blue) and PI stained (red) bacteria. DAPI is able to cross the cell membrane regardless of cell viability, however, PI can only intercalate DNA chains when the membrane has been damaged.51, 52 Therefore, both DAPI and PI stained (pink) bacteria represent the dead bacteria. A large number of live cells were seen on the bare glass and DP-PAR film surfaces, while almost no live cells were present on the Ag@DP-PAR film surfaces. Due to the strong 21 ACS Paragon Plus Environment


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bactericidal activity of AgNPs, numerous cells adhered to the AgNPs-incorporated films were clearly damaged. Notably, only a few live or dead bacterial cells were observed on lubricant infused films proving their excellent antifouling behavior. In other words, the L-infused Ag@DP-PAR films successfully exhibited dual-antibacterial functionality by combining the advantages of both bactericidal and bacteria-repellent properties. In accordance with confocal images, the antibacterial activities of AgNP incorporated surfaces towards E. coli were also investigated by SEM analysis. A large number of live cells were observed on the bare Si wafer and the DP-PAR films. However, E. coli on Ag@DP-PAR film and L-infused Ag@DP-PAR film showed morphological alteration (Figure S11). The control cells had intact morphologies and smooth surfaces, while most of the E. coli adhered on AgNPs-conjugated surfaces had structural alterations of the outer membrane such as disruption caused cytoplasmic leakage with shrunk morphology. Moreover, only a few bacterial cells were observed on L-infused Ag@DP-PAR films, proving successful bacterial repellency of lubricant. In addition, the antibacterial effect was assessed by observing bacterial inhibition zones (Figure S12). Substrates were placed on LB agar plates spread with E. coli. In the absence of AgNPs, bacterial growth was observed, while L-infused Ag@DP-PAR film-coated substrates inhibited bacterial growth on surfaces. These results clearly demonstrated that the AgNPs-loaded PAR films possess good antibacterial performance. By comparison of lubricant-infused and noninfused AgNPs-incorporated films, we verified effects of lubricant on antibacterial activity. The L-infused Ag@DP-PAR films showed much smaller inhibition zones than non-infused films, proving the antibacterial activity of L-infused Ag@DP-PAR films originated from contact-killing mechanism (Figure S13). Besides, silver release profiles also support that lubricant prevents dissolution of AgNPs, emphasizing the contact-killing mechanism as a major antibacterial activity (Figure S14). The main advantage of non-leaching systems, such as contact-killing surfaces, is in the confinement of the cytotoxic effect to the surfaces, resulting 22 ACS Paragon Plus Environment

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in minimizing the potentially harmful interactions between the agent and host tissues. Additionally, the bactericidal effect can be sustained without depletion of antibacterial agent, dissolution of AgNPs, over time.5, 53 The lubricant which seems to protect consumption of AgNPs has potent to lead long-lasting antibacterial activity.54

Figure 5. Waterborne antibacterial activity of L-infused Ag@DP-PAR films in comparison with control samples. (a) Schematic illustration of bactericidal test by surface contact. Photographs and CFU counts of E. coli colonies grew on the surfaces of bare Si wafer, Linfused DP-PAR, and L-infused Ag@DP-PAR films for 6 hrs. (b) Representative CLSM images of E. coli on bare glass, DP-PAR L-infused DP-PAR, Ag@DP-PAR, and L-infused Ag@DP-PAR film surfaces. DAPI stained both live and dead cells (blue). PI stained dead bacterial cells (red). The images in the rightmost column display overlaps of DAPI and PI (all scale bars = 10 μm).



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Airborne Bactericidal Tests The antibacterial activity of developed films was also determined by using airborne bacterial testing. Glass slides were coated and modified as stated above. E. coli suspension was sprayed as fine mist size on surfaces of various PAR derivative film-coated glasses, and allowed to grow and form colony of bacteria on LB agar at 37 °C (Figure 6a). After two nights of incubation for observation (Figure 6b), enormous numbers of colonies were visualized on substrates. Both bare glasses and various DP-PAR film-based substrates were fully covered with bacterial colonies. In the meantime, less bacterial colonies were seen on the L-infused DP-PAR film-coated substrates attributing to slippery features of lubricant with excellent water repellency,55 which prevents adhesion of bacteria in coarse-sized droplets. For airborne bacteria, bactericidal effects can only be activated by contact-killing strategy since no medium for diffusion of antibacterial material exists.29,

30

Therefore, Ag@DP-PAR film

surfaces achieved almost 100 % of bactericidal efficiency. In case of the L-infused Ag@DPPAR film, a few colonies grew on the surfaces though this film exhibits good bacteria repellency and bactericidal activity. This phenomenon occurred because while bacteria were readily in contact with AgNPs on Ag@DP-PAR film surfaces, the lubricant layer existing within the L-infused Ag@DP-PAR films decrease the possibility of direct contact between them. These results indicate that AgNPs are necessary for killing airborne bacteria as shown in previous studies,31, 32 although lubricant-infused surfaces show suppression effects on adhesion of airborne bacteria.


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Figure 6. Airborne antibacterial activity of L-infused Ag@DP-PAR films in comparison with control samples. (a) Schematic illustration of airborne bactericidal test. (b) Photographs of bare glass, L-infused DP-PAR, and L-infused Ag@DP-PAR film onto which E. coli suspensions were sprayed in fine droplets, air dried and incubated under 0.7 % agar for 48 hrs. CONCLUSION Functional surfaces displaying bactericidal properties and/or preventing bacterial adhesion have been actively developed to overcome the infectious problems from microbial fouling in many medical devices and food processing equipment. Surface functionalization provide efficient strategy to significantly improve material surfaces to avoid bacterial contamination. Using VIPS process of PS/PPFPA blends combined with selective PS removal, we developed porous amine-reactive films by simple process under ambient conditions. By virtue of the facile and highly reactive nature of activated PFP ester chemistry, two different primary aminecontaining molecules, dopamine and amine-PDMS, were successfully introduced to the PAR 25 ACS Paragon Plus Environment


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films in sequential manner without altering porous structures. The catechol moiety containing DP-PAR films could further induce formation of AgNPs on the surfaces and finally, silicone oil lubricant was infused within PDMS-functionalized films to construct slippery surfaces. This approach enables multi-functionalization of porous films after fabrication that can be used as dual-functional surfaces, i.e., preventing biofilm formation and showing bactericidal activity. The prepared L-infused Ag@DP-PAR film surfaces exhibited good bacteria-repellent property resulting in significant inhibition of biofilm formation, which was confirmed by static bacteria culture tests. Furthermore, antibacterial assays indicated that L-infused Ag@DP-PAR showed notable bactericidal activity toward waterborne and airborne E. coli. The L-infused Ag@DPPAR possessing contact-killing activity has potential to be sustained longer than biocideleaching system and to have lower toxicity. In summary, this efficient post-modification of PPFPA derived PAR films could easily introduce multiple functionalities onto the surfaces, which facilitate tuning of versatile properties. Thus, platforms presented in this study provide the possibility to introduce wide range of functionalities such as biomolecular immobilization and sensing since they possess amine-reactive functionality with high surface area attributing to the porous structures.


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ASSOCIATED CONTENT Supporting Information. Supporting Information is available free of charge on the ACS Publication website at http://pubs.acs.org. NMR data of PPFPA, Information of PAR films including SEM, EDS data and thickness value, Transmittance of films, and photographs of inhibition zone test (PDF).

AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] * E-mail: [email protected] Author Contributions ‡These

authors contributed equally to this work. The manuscript was written through

contributions of all authors. All authors have given approval to the final version of the manuscript. Notes Any additional relevant notes should be placed here. ACKNOWLEDGMENT This work was financially supported by the National Creative Research Initiative Program for “Intelligent Hybrids Research Center” (No. 2010-0018290) funded by the National Research Foundation of Korea (NRF), and the BK21 Plus Program funded by the Ministry of Education, Science, and Technology (MEST) of Korea. S.Wooh thanks to the National Research Foundation of Korea (NRF-2017R1C1B5076184) for financial support. 27 ACS Paragon Plus Environment


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Development of Multimodal Antibacterial Surfaces Using Porous Amine-Reactive Films Incorporating Lubricant and Silver Nanoparticles


Development of Multimodal Antibacterial Surfaces Using Porous

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