Antifouling Coatings via Tethering of ... - ACS Publications

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Antifouling Coatings via Tethering of Hyperbranched Polyglycerols on Biomimetic Anchors Dicky Pranantyo, Li Qun Xu, Koon Gee Neoh, and En-Tang Kang* Department of Chemical & Biomolecular Engineering National University of Singapore, Kent Ridge, Singapore 119260

Serena Lay-Ming Teo* Tropical Marine Science Institute National University of Singapore, Kent Ridge, Singapore 119223 S Supporting Information *

ABSTRACT: Hyperbranched polyglycerols (HPG) bearing terminal thiol moieties (HPG-SH) were synthesized via anionicring-opening multibranching polymerization of glycidol from pentaerythritol and subsequent 1,1′-carbonyldiimidazole (CDI) coupling with cysteamine. Bioinspired (1) N-dopamine maleimide (DM), (2) tannic acid (TA), and (3) polydopamine (PDA) were employed to produce monolayer, multilayer, and polymeric anchors, respectively, on stainless-steel (SS) substrates. Postfunctionalization of the biomimetic anchor-modified SS surfaces was enacted by tethering of HPG-SH via Michael addition or thiol−ene “click” reaction to confer surface hydrophilicity. The thickness and grafting density of HPG coatings could be controlled by tuning the degree of thiolation. In comparison to the pristine SS surface, the HPG-modified surfaces exhibited substantially reduced initial adhesion and inhibition of the biofilm formation of Gram-negative Pseudomonas sp. and Grampositive Staphylococcus epidermidis. Qualitative and quantitative assays of settlement of the microalgae Amphora coffeaeformis further demonstrate the low fouling characteristics of the HPG-modified surfaces. Therefore, tethering of HPG coatings on biomimetic anchors provides an environmentally benign alternative to antifouling surfaces.

1. INTRODUCTION Despite the high efficacy in biofouling mitigation, coatings that release organometallic or organic biocides are exhausted overtime and can bring about detrimental effects to the environment.1 These limitations have intensified the search for environmentally benign means for surface functionalization of materials in biomedical devices, marine structures, water treatment systems, and chemical industries.1−5 With regard to environmental benignity, hydrophilic and amphiphilic polymer brushes have been developed as an alternative means to construct nondepleting coatings for antifouling surfaces.6−11 Bioinspired and “green” chemistry approaches to surface modification and functionalization have been of increasing interest.12,13 Thus, the development of simpler and “greener” processes for surface functionalization is in line with current interests and concerns. Mussel-inspired adhesive has emerged as a versatile platform in surface functionalization technology. Driven by the reactivity of ortho-dihydroxyphenyl binding sites toward independent substrates, dopamine as a mussel-protein mimic is capable of achieving bidentate metal complexes, hydrophobic−hydrophobic interactions, hydrogen bonds, or coupling-induced covalent bonds with organic and inorganic materials.14−16 Moreover, molecular combination of these catechol moieties with the representative biofunctional polymers, e.g., poly(sodium 4-vinylbenzenesulfonate), poly(sulfobetaine methacrylate), and poly(1-vinyl-2-pyrrolidone), has been reported to readily form self-cross-linked nanolayers for the design of versatile biointerfaces.17 Because of structural similarities to dopamine, plant polyphenolics commonly found in chocolate, © XXXX American Chemical Society

wine, and tea extract also exhibit material-independent adhesion. The trihydroxyphenyl residues in plant polyphenolics are highly reactive and capable of diverse binding mechanisms, viz., hydrogen bonds, charge-transfer, and charge-dipole interactions.18−21 These biomimetic adhesives constitute an ideal platform for “green” coating processes and environmentally benign materials.22 Hyperbranched polymers are 3D macromolecules with dendritic architecture that exhibit unique structures and properties such as abundant functional groups, intramolecular cavities, low viscosity, and high solubility.23 Theoretically, at equivalent grafting density, a branched polymer graft has higher efficiency in reducing protein interactions with the coated surface than that of its linear analogue.24 For the same functional polymers, globular-shaped graft polymers have also been reported to provide superior antifouling efficacy over that of their linear counterparts.25 These findings provide a good incentive for the investigation of antifouling surfaces based on hyperbranched polymer coatings. Unlike dendrimers, which require tedious multistep syntheses, hyperbranched polymers can be prepared in a one-pot synthesis at the expense of having an imperfect degree of branching. Among a few classes of these polymers, hyperbranched polyglycerols (HPG) can be synthesized in a controlled manner with predetermined molecular weights and narrow polydispersity.26,27 It has been Received: October 6, 2015 Revised: January 26, 2016 Accepted: February 1, 2016

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DOI: 10.1021/acs.iecr.5b03735 Ind. Eng. Chem. Res. XXXX, XXX, XXX−XXX

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Industrial & Engineering Chemistry Research

taerythritol (408.45 mg, 3 mmol) was deprotonated with PTB (1346.52 mg, 12 mmol) in 10 mL of dioxane. The mixture was stirred and degassed with argon for 30 min at 25 °C, sealed, and transferred to an oil bath at 95 °C. Glycidol (12 mL, 160 mmol) was introduced dropwise under argon atmosphere and vigorous stirring for 12 h. The reaction was allowed to continue overnight. After polymerization, the mixture was cooled down and diluted with deionized water. The solution was neutralized by adding dilute HCl to obtain pH 7. The solution was dialyzed to remove bound monomers and reactants and then lyophilized to obtain ∼3.3 g of HPG. Thiolation of HPG was conducted via CDI chemistry. HPG (100 mg) was dissolved in 2 mL of dry DMSO and degassed with argon for 15 min. A predetermined amount of CDI was introduced and the mixture was sealed. The coupling reaction was allowed to proceed under stirring at 25 °C overnight. After reaction, the mixture was precipitated thrice in acetone and dried under reduced pressure to obtain imidazole-functionalized hyperbranched polyglycerol (HPG-Im). HPG-Im (100 mg) was dissolved in 2 mL of dry DMSO and degassed with argon for 15 min. A predetermined amount of cysteamine was introduced and the mixture was sealed. The thiolation reaction was allowed to proceed under stirring at 25 °C overnight. After the reaction, the mixture was dialyzed and lyophilized to obtain hyperbranched polyglycerol with various degrees of thiolation (HPG-SH1 to HPG-SH4, denoted collectively as HPG-SH). 2.3. Surface Functionalization of SS Substrates. The SS substrates were cut into 1 cm × 1 cm coupons and immersed in the piranha solution (H2SO4 (95−97%)/H2O2 (30%) = 3:1, v/ v) for 30 min to oxidize the organic residues. After oxidation, the SS coupons were subjected to sequential ultrasonic cleansing in deionized water, acetone, and ethanol for 10 min each. The clean SS coupons were dried under reduced pressure for further use. Three types of anchoring design were introduced on the SS substrates. For monolayer anchoring, 40 coupons of SS of 1 cm2 and 80 mg of DM were introduced into 40 mL of deionized water. For multilayer deposition anchoring, 40 coupons of SS of 1 cm2 and 80 mg of TA were introduced into 40 mL of NaCl buffered saline (0.6 M, pH 7.8). For polydopamine (PDA) anchoring, 40 coupons of SS of 1 cm2 and 80 mg of dopamine were introduced into 40 mL of TrisHCl (10 mM, pH 8.5). Each anchoring mixture was stirred thoroughly at 25 °C for 24 h. After immobilization, the substrates were rinsed with deionized water and ethanol prior to being dried under reduced pressure. According to the respective anchoring process, the obtained surfaces were denoted as SS-DM, SS-TA, or SS-PDA. Postmodification to impart antifouling property was enacted by tethering HPG-SH to the anchoring surfaces. HPG-SH (20 mg) was dissolved in 10 mL of deionized water, and 10 coupons of SS-DM were introduced into the solution. The mixture was stirred thoroughly at 25 °C for 24 h. The modified substrates were rinsed with ethanol and dried under reduced pressure to obtain the SS-DM-HPG surfaces. A similar procedure was applied to the SS-TA and SS-PDA surfaces to produce the SS-TA-HPG and SS-PDA-HPG surfaces, respectively. 2.4. Characterization. The chemical structures of HPG, HPG-Im, and HPG-SH were characterized by 1H NMR spectroscopy on a Bruker ARX 300 MHz spectrometer, using DMSO-d 6 as the deuterated solvent. Gel permeation chromatography (GPC) was performed on a Waters GPC

reported that linear polyglycerol and poly(methyl glycerol) coatings exhibit protein and cell-fouling resistances comparable to that of the poly(ethylene glycol) (PEG) coating.28 The compact, globular structure with multitude distribution of hydroxyl groups down to the cavity levels would make HPG a more potent antifouling graft coating than linear polyglycerols and PEG. Experimental results have shown that ultrathin coatings based on HPG can render gold and glass surfaces highly protein resistant.29−32 In addition, HPG exhibits higher stability against thermal and oxidative degradation than PEG.29 Recently there is a growing interest in the combination of polyglycerols and biomimetic anchors. Linear and hyperbranched polyglycerols have been grown from acetonideprotected catechol initiator, which could form a coating layer on metal oxide nanoparticles after the deprotection of acetonide.33 In another molecular combination, HPG has been conjugated with catechol and amino moieties to mimic the mussel foot proteins, which could readily form a coating on any type of material while also serving the surface antifouling function.34 The coating formation of HPG bearing catechol and amino groups could take place within 10 min by a simple dipcoating method, which is as fast as the formation of mussel byssal threads.35 In this work, we explored the functionality of a collective design set of biomimetic anchors: (1) a monolayer of dopamine maleimide (DM), (2) a multilayer coating of tannic acid (TA), and (3) a polymeric layer of polydopamine (PDA) coating on stainless steel. As the precursor of DM and monomer of PDA, dopamine is a strong neurotransmitter with a range of LD50 at 59−950 mg/kg in mouse, depending on the administering routes.36 In comparison, TA is generally recognized as safe (GRAS) by the U.S. Food and Drug Administration (FDA) and thus represents a “greener” surface-anchoring technique.37 Antifouling postmodification was achieved by tethering thiolterminated HPG to the surface hydroxyphenyl or maleimide rings via Michael addition or thiol−ene “click” chemistry. Performance of the HPG-modified surfaces in resisting bacterial adhesion, biofilm formation, and algae settlement were investigated.

2. EXPERIMENTAL SECTION 2.1. Materials. Stainless-steel (SS) foils (AISI type 304, 0.05 mm thick) were purchased from Goodfellow, Ltd., Cambridge, UK. Tannic acid (TA), pentaerythritol (98%), potassium tert-butoxide (PTB, 98%), (±)-glycidol (96%), 1,1′carbonyldiimidazole (CDI), cysteamine, and 1,4-dioxane (anhydrous, 99.8%) were purchased from Sigma-Aldrich Co., St. Louis, MO. Dopamine hydrochloride (99%) and 1,4-dithioDL-threitol (99%) were purchased from Alfa Aesar Co., Ward Hill, MA, USA. Pseudomonas sp. (NCIMB 2021) was obtained from the National Collection of Industrial Marine Bacteria, Sussex, UK. Staphylococcus epidermidis (ATCC 12228) was obtained from American Type Culture Collection, Manassas, VA, USA. The LIVE/DEAD BacLight Bacterial Viability Kit L131152 was purchased from Molecular Probes Inc., Eugene, OR, USA. Acetone (analytical-grade) was used as received. Dimethyl sulfoxide (DMSO, analytical-grade) was dehydrated with oven-dried molecular sieves (4 Å). N-Dopamine maleimide (DM) was synthesized according to the method reported in the literature.38 2.2. Synthesis of Thiolated Hyperbranched Polyglycerols. Hyperbranched polyglycerol (HPG) was synthesized via anionic-ring-opening multibranching polymerization. PenB


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Industrial & Engineering Chemistry Research Scheme 1. Preparation of the Thiolated Hyperbranched Polyglycreols

system, equipped with a Waters 1515 isocratic HPLC pump, a Waters 717 Plus autosampler injector, a Waters 2414 refractive index detector, and an Agilent PLgel 5 μm MIXED-D column (P/N: 79911GP-MXD), using DMF as the eluent at a flow rate of 1.0 mL/min at 35 °C. The calibration curve was generated using poly(ethylene glycol) molecular weight standards. Surface compositions of the modified SS substrates were determined by X-ray photoelectron spectroscopy (XPS) on a Kratos AXIS Ultra DLD spectrometer. Analyses were performed with a monochromatized Al Kα X-ray source of 1486.71 eV photons, at a constant dwelling time of 100 ms and pass energy of 40 eV. A photoelectron takeoff angle (α) of 90°, with respect to the sample surface, was chosen to obtain the core-level signals. The XPSPEAK version 4.1 software was used in peak analysis, using the C 1s hydrocarbon peak at 284.6 eV as a reference for all binding energies (BEs). In peak synthesis, the full width at half-maximum (fwhm) for the Gaussian peaks

was maintained as constant for all components in a particular spectrum. Surface elemental stoichiometries were determined from the peak-area ratios. Static water contact angles of the pristine and surface-functionalized SS substrates were measured at 25 °C using the sessile drop method with 2 μL water droplets on a telescopic goniometer (Model 100−00-(230), Rame-Hart Inc., Mountain Lake, NJ, USA) with a magnification power of 23× and a protactor of 1° graduation. Each static water contact angle reported was the mean value from three substrates, with the value of each substrate obtained by averaging the contact angles from at least three surface locations. The topography of the HPG-modified surfaces was investigated using glass substrates by atomic force microscopy (AFM) on a Bruker’s Dimension Icon System (Santa Barbara, CA, USA), equipped with a NanoScope V Controller. The root-mean-square surface roughness (Rs) was calculated from the image profile determined by AFM. To measure the C


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Industrial & Engineering Chemistry Research thickness of HPG coatings by step profiling, the surfaces were scratched with a razor blade.39 2.5. Bacterial Adhesion and Biofilm Formation Assays. Pseudomonas sp. was cultured in nutrient-rich simulated seawater according to the method described previously.40 S. epidermidis was cultured in aqueous nutrient broth according to the ATCC procedure. After incubation, each bacterial suspension was centrifuged at 2700 rpm for 10 min to remove the supernatant. Pseudomonas sp. and S. epidermidis sediments were washed twice with simulated seawater and phosphatebuffered saline (PBS), respectively, and resuspended at a concentration of 107 cells/mL. Each sample substrate was placed in a 24-well plate (Nalge, Nunc Int., Rochester, NY, USA) and immersed in 1 mL of the bacterial suspension under static condition at 37 °C for 4 h. After washing thrice with ultrapure water to remove the nonadhered bacteria, each sample substrate was stained with LIVE/DEAD BacLight solution for 15 min. The viable (appearing green) and dead (appearing red) bacterial cells adhered on the sample surfaces were distinguishable under a Nikon ECLIPSE Ti-U fluorescence microscope (Tokyo, Japan), equipped with a green filter (excitation/emission: 450−490 nm/500−550 nm) and a red filter (excitation/emission: 510−560 nm/605−685 nm). For the biofilm formation assay, Pseudomonas sp. and S. epidermidis sediments were resuspended in nutrient-rich simulated seawater and PBS containing nutrient broth, respectively, at a concentration of 106 cells/mL. Each sample substrate was immersed in 1 mL of the bacterial suspension at 37 °C for 24 h to allow the growth of biofilm, before being washed thrice with ultrapure water to remove the loosely adhered bacteria. The bacterial layer was fixed by immersing each sample substrate in 3% of aqueous glutaraldehyde at 4 °C overnight, followed by serial dehydration in 20, 40, 60, 80 and 100% of ethanol for 5 min each. After being dried under reduced pressure and sputter-coated with a thin platinum layer, each sample substrate was observed under a scanning electron microscope (SEM, Model JSM-5600LV, JEOL Co., Tokyo, Japan). 2.6. Amphora coffeaeformis Settlement Assay. The culturing procedure of A. coffeaeformis (UTEX B2080, ∼16 μm in diameter), as well as the microalgal settlement assays under microscopic observation and quantification techniques, were carried out according to the methods described in previous literature.41,42

Figure 1. Molar-feed ratio dependence of the theoretical (left axis) and calculated (right axis) degree of HPG thiolation. The [S]/[C] component ratios were obtained from XPS peak area integration.

Site activation was first carried out by coupling with 1,1′carbonyldiimidazole (CDI) to produce HPG-Im with reactive imidazole carbamates. Hydrolysis of these imidazole carbamates has been reported to be very slow, which provides a good opportunity for postfunctionalization.44 The imidazole terminals of HPG-Im were substituted with the amino moiety of cysteamine to form stable carbamate linkages, resulting in the thiolated hyperbranched polyglycerol (HPG-SH, Scheme 1). In the 1H NMR spectra (Figure S2), the chemical shifts at about 3.0−4.0 and 4.3−5.0 ppm represent the hydrocarbon and hydroxyl protons of HPG, respectively.27 Upon activation with CDI, new signals characteristic of imidazole species appear at 6.98 and 7.61 ppm, attributable to the cyclic methine protons. After thiolation, these imidazole signals completely disappear, and in return, a new chemical shift characteristic of the thiol proton appears at 2.06 ppm.45 This chemical shift indicates successful substitution of imidazole ring with cysteamine. In comparison to HPG, the Mn of HPG-SH exhibits a fivefold increase to 125 200 g/mol (Figure S1). This increase has resulted from molecular cross-linking between the thiol moieties to form disulfides. Upon addition of 1,4-dithio-DLthreitol to the HPG-SH solution, the GPC spectrum shows peak broadening and shifts to higher elution time, indicating the cleavage of disulfide bonds. In the multibranching polymerization of glycidol, a new hydroxyl group is annexed to the polymer molecule for every addition of monomer. The number of hydroxyl moieties in one molecule of HPG can be calculated from

3. RESULTS AND DISCUSSION 3.1. Synthesis of Thiolated Hyperbranched Polyglycerols. Hyperbranched polyglycerol (HPG) was synthesized via anionic-ring-opening multibranching polymerization of glycidol, a reactive oxirane monomer with latent AB2 structure (Scheme 1).26 Slow monomer addition to the deprotonated tetrafunctional core initiator facilitated simultaneous growth of the secondary alkoxides and primary alcohols, which controlled the chain propagation to form a hyperbranched structure in a rapid cation exchange equilibrium among the hydroxyls.43 From GPC measurement, the number-average molecular weight (Mn) of the HPG reaches 25 300 g/mol (Figure S1). The use of dioxane as an emulsifying agent of low polarity helps to moderate the viscosity increase during polymerization and to sustain a favorable condition for ion exchange, producing a high-molecular-weight HPG with narrow polydispersity.27 The randomly distributed hydroxyl moieties of HPG represent abundant derivatizable sites for molecular design.

[OH]p = [OH]i +

[M n]p − [M n]i [M n]m

where subscript i, m, and p denote, respectively, the initiator (pentaerythritol), monomer (glycidol), and polymer (HPG). Therefore, one molecule of HPG with a Mn of 25 300 g/mol contains about 344 hydroxyl terminal groups. In the preparation of HPG-SH, the molar feed ratio of [CDI]/ [HPG] or [cysteamine]/[HPG] was controlled to produce four combinations with various degrees of thiolation, denoted as HPG-SH1 to HPG-SH4 (Figure 1). Theoretical degree of thiolation was calculated by accounting the hydroxyl groups reacted with CDI/cysteamine over the total hydroxyl groups of HPG, assuming CDI/cysteamine as the limiting reactants in each molar feed ratio. The [S]/[C] molar ratio of the HPG-SH was derived from the elemental stoichiometry in X-ray photoelectron spectroscopy (XPS) analysis (Table S1). The D


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Scheme 2. Various Anchoring Strategies on Stainless-Steel Surfaces and Immobilization of the Thiolated Hyperbranched Polyglycerols

SH thiol group, based on the total hydroxyl groups, was determined by direct titration of the thiol content with iodine and starch as colorimetric indicator (Table S2). In agreement with the XPS results, the thiol fraction determined by direct titration also showed progressive increase with the increasing molar feed of CDI/cycteamine. Thus, a predetermined degree of thiolation can be achieved by controlling the molar feed ratio during the reaction. 3.2. Surface Functionalization of the SS Substrates. DM was used as a small-molecule anchor to produce monolayer functionality on the SS surface (Scheme 2). The catechol group of DM constitutes a strong chelating agent, capable of producing a bidentate complex with the metal center.15 In contrast to the dopamine precursor, maleimide protection of the DM molecule forms a tertiary amine, which presumably negates self-polymerization. In the XPS wide-scan spectrum of DM-anchored SS surface (SS-DM, Figure 2a), the distinct signals characteristic of metals, such as Cr 2p3/2, Fe 2p3/2, and Ni 2p3/2 core-level components with respective binding energies (BEs) at 577, 711, and 860 eV, suggest a monolayer thickness below the 8 nm probing depth of XPS technique in organic matrices.46 The XPS C 1s core-level spectrum of the SS-DM surface (Figure 2b) can be curve-fitted into four peak components with BEs at 284.6, 285.6, 286.2, and 287.9 eV, attributable to the C−H, C−N, C−Om and N−C O species, respectively.15 TA spontaneously forms coatings on SS surfaces. The TAanchored SS surface (SS-TA) consists of tridentate coordination complexes. The characteristic signals of metallic elements are not discernible in the XPS wide-scan spectrum of the SS-TA surface (Figure 2c), indicative of a coating thickness greater than the XPS probing depth. It has been reported that the thickness of TA coatings on a TiO2 surface can reach ∼70 nm after 12 h of immersion in 2 mg/mL of TA solution.18 Multilayer surface deposition presumably was achieved through

Figure 2. XPS wide-scan and C 1s core-level spectra of (a and b) SSDM, (c and d) SS-TA, and (e and f) SS-PDA surfaces.

[S]/[C] molar ratio increases proportionally with the [CDI]/ [HPG] or [cysteamine]/[HPG] molar feed ratio. The fact that the rate of increase in [S]/[C] molar ratio is in good agreement with that of the theoretical degree of thiolation implies a high reaction efficiency. In addition, the actual percentage of HPGE


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a combination of inherent affinity of phenolics toward independent substrates (including self-affinity) and compact, noncovalent oligomerization, e.g., hydrogen bonding. The curve-fitted XPS C 1s core-level spectrum of the SS-TA surface (Figure 2d) comprises of three peak components with BEs at 284.6, 286.2, and 288.4 for the respective C−H, C−O, and O− CO species.47 Dopamine has been considered an essential building block in adhesive that mimics the marine mussel protein. In the absence of amine protection, it undergoes self-polymerization into polydopamine (PDA), which involves oxidation of catechol to quinine and subsequent rearrangement into dihydroxyindole.14 Herein, dopamine was beneficially employed to form a stable polymeric anchor on the SS surfaces (SS-PDA). The dense and thick coverage of PDA coatings on the SS substrates resulted in signal eclipse of the underlying metallic elements in the XPS wide-scan spectrum (Figure 2e). The C 1s core-level spectrum of the SS-PDA surface (Figure 2f) can be curve-fitted into five peak components with BEs at 284.6, 285.6, 286.2, 287.6, and 288.6 eV, associated with the respective C−H, C−N, C−O, CO, and O−CO species.46 Postmodification with HPG renders the surfaces highly hydrophilic for inhibition of biofouling. The SS-DM, SS-TA and SS-PDA surfaces provide abundant di- or trihydroxyphenyl sites, which can react readily with the thiol moieties of the HPG-SH through Michael addition.14,18 In addition, HPG-SH can form covalent bond with the electron-deficient maleimide olefin via the modular thiol−ene “click” chemistry.48 The presence of HPG-SH molecules tethered on the SS surface anchors was confirmed by XPS analysis. The C 1s core-level spectrum of the SS-PDA-HPG (Figure 3a,c,e,g) can be curvefitted into five peak components for the C−H, C−N/C−S, C− O, CO and O−CO species, with respective BEs at 284.6, 285.6, 286.2, 287.5, and 288.6 eV.46,49 The predominance of C−O peak intensity is attributable to the presence of abundant ether repeat units in the HPG domain. In comparison to the C−H reference peak, the C−O peak area of the SS-PDA-HPG surface shows a progressive increase with the increase in degree of HPG thiolation. This correlation has resulted from the presence of disulfide cross-linking, which gives rise to the thickness and surface coverage of HPG-SH layers and enhanced ether signal intensity within the XPS sampling depth. The intensity of XPS S 2p core-level spectra of the SS-PDA-HPG surfaces (Figure 3b,d,f,h) becomes more prominent with the increase in degree of thiolation, as is also indicated by the

Figure 3. XPS C 1s and S 2p core-level spectra of (a and b) SS-PDAHPG1, (c and d) SS- PDA-HPG2, (e and f) SS-PDA-HPG3, (g and h) SS-PDA-HPG4, (i) SS-TA-HPG4, and (j) SS-DM-HPG4 surfaces.

Table 1. Surface Composition and Static Water Contact Angle of the Pristine and Surface-Functionalized Stainless-Steel Substratesa sample pristine SS SS-DM SS-TA SS-PDA SS-DM-HPG4 SS-TA-HPG4 SS-PDA-HPG1 SS-PDA-HPG2 SS-PDA-HPG3 SS-PDA-HPG4

surface composition (molar ratio)b [C]/[O]/[N] [C]/[O] [C]/[O]/[N] [C]/[O]/[N]/[S] [C]/[O]/[N]/[S] [C]/[O]/[N]/[S] [C]/[O]/[N]/[S] [C]/[O]/[N]/[S] [C]/[O]/[N]/[S]

= = = = = = = = =

13.4:7.4:1.0 1.3:1.0 9.5:3.6:1.0 38.9:24.5: 2.1:1.0 41.4:26.1: 1.0:1.0 279.3:112.6:23.8:1.0 134.4: 62.9:10.1:1.0 37.9:21.1: 2.2:1.0 24.7:21.1: 2.5:1.0

static water contact angle (mean ± SD)c 77 70 56 59 27 23 39 32 21 15

± ± ± ± ± ± ± ± ± ±

4° 2° 2° 2° 3° 2° 3° 3° 2° 2°

a

Each contact angle measurement indicates a mean value with standard deviation obtained from three replicates. bSurface composition was derived from the peak area integration of XPS spectra. cSD denotes standard deviation obtained from three replicates. F


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increases, the HPG coatings appear to become denser, and the surface roughness (Rs) decreases from 3.3 to 2.6 nm. The thickness of HPG coatings (h) with different thiolation degrees was determined over the scratched surfaces. The change in phase signals between the scratched and unscratched areas indicates two regions with different composition; thus, the scratches have reached the substratum base.3 For the AFM measurement, to avoid uncontrollable thickness of the anchors produced by TA or PDA, the monolayer anchor of DM was exploited as an initial platform for the postmodification with HPG-SH. The coating thickness over an observation area of 50 × 50 μm2 increases gradually from 35 to 86 nm with the increase in degree of thiolation. This result is in good agreement with the proclivity of HPG-SH molecules to form intra- and intermolecular cross-linking on the surface, which is also responsible for the increasing thickness, density, and complexity of the coatings. The grafting density of HPG-SH coatings on the DManchored surfaces was estimated from the calculation of polymer density, molecular weight, and coating thickness (Table S3). The HPG-SH with higher degree of thiolation exhibited higher molecular grafting density, in agreement with the AFM observation results of the Glass-DM-HPG surfaces. From the AFM images, the surface coatings obtained from three biomimetic anchors showed morphological difference (Figure S3). In comparison to TA and PDA, the DM anchor layer exhibited the lowest magnitude of roughness and thickness. Similar to that of the Glass-DM-HPG surfaces, the roughness of Glass-TA-HPG and Glass-PDA-HPG surfaces generally decreased with the increasing degree of HPG thiolation, as a result of the increase in grafting density (Figure S4). Therefore, upon postmodification with HPG-SH, the three biomimetic anchor layers resulted in comparable grafting density of the polymer coatings because of the predominant formation of disulfide bond. To confirm the presence of disulfide bonds, the SS-DM-HPG4, SS-TA-HPG4, and SSPDA-HPG4 surfaces were immersed in excess DTT solution and rinsed with deionized water. After the immersion treatment, the underlying metallic elements appeared in the XPS wide-scan spectra of the SS-DM-HPG4 and SS-TA-HPG4 (Figure S5). In the C 1s core-level spectra, the intensity and peak area of C−O signals also became lower than that of the C−H signals because of the reduction cleavage of the intermolecular disulfide bond of HPG-SH by DTT. 3.3. Bacterial Adhesion and Biofilm Formation Assays. Marine Gram-negative Pseudomonas sp. was used to challenge the antiadhesion properties of the HPG-modified substrates. After immersion in the Pseudomonas sp. suspension for 4 h, a mass of viable bacterial cells (appearing green) adhered and occupied almost the entire area of the pristine SS, SS-DM, SSTA, and SS-PDA surfaces (Figure S6a−d). In contrast, only a few viable cells are observable on the SS-PDA-HPG surfaces (Figure S6e−h), suggesting that the HPG-modified surfaces exhibit antifouling properties. The number of adhered bacterial cells decreases with the increase in degree of thiolation on the SS-PDA-HPG surfaces. This correlation implies that an increase in coating density and surface hydrophilicity results in higher antibacterial adhesion efficacy. All the sample surfaces show only a small number of dead cells (appearing red), implying that the low fouling property of the HPG coatings is not due to the bactericidal effect. The immense hydration capacity of the hyperbranched polyether of globular polyglycerols is responsible for inhibiting bacterial adhesion on the modified surfaces.

Figure 4. AFM images of (a) Glass-DM-HPG1, (b) Glass-DM-HPG2, (c) Glass-DM-HPG3, and (d) Glass-DM-HPG4 surfaces.

increase in [S]/[C] molar ratio (Table 1). The S 2p core-level spectrum of the SS-PDA-HPG4 surface (Figure 3h), with a spin−orbit split doublet (S 2p3/2 and S 2p1/2) with respective BEs at 163.1 and 164.3 eV and a spectral component area ratio of 2:1, is attributable to the covalently bonded sulfur species.50 For the SS-PDA-HPG1 to SS-PDA-HPG3 surfaces (Figure 3b,d,f, respectively), another S 2p doublet at the BEs of 167.2 and 168.4 eV have emerged from the sulfonate species because of partial self-oxidation.50 The C 1s core-level line shapes of the SS-TA-HPG4 and SS-DM-HPG4 surfaces (Figure 3i,j, respectively) are similar and resemble that of the SS-PDAHPG surface, suggesting the successful immobilization of HPGSH molecules. Surface morphology of the HPG-modified substrates was observed under an atomic force microscope (AFM) over an area of 5 × 5 μm2 (Figure 4). As the degree of thiolation G


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Figure 5. SEM images of the biofilm formation for Pseudomonas sp. on the (a and b) pristine SS, (c) SS-DM, (d) SS-DM-HPG4, (e) SS-TA, (f) SSTA-HPG4, (g) SS-PDA, and (h) SS-PDA-HPG4 surfaces after 24 h of immersion in the bacterial culture at 37 °C. Scale bars are (a and c−h) 10 μm and (b) 5 μm.

surface tethering51 or surface-initiated polymerization52,53 are effective in reducing fouling by E. coli, Pseudomonas aeruginosa, and Acinetobacter baylyi. Adherent bacteria are capable of forming biofilm on sample surfaces over an extended incubation time. During the incubation period, Pseudomonas sp. assembled in colonies to occupy a large portion of the pristine SS, SS-DM, SS-TA, and SS-PDA surfaces (Figure 5a,b,c,e,g). Without antifouling protection, the substrates are susceptible to biofilm formation. This mature stage of microfouling is responsible for subsequent establishment of macrofouling growth and eventually leads to failure of the material surface.54 In comparison, the HPGmodifed surfaces have a substantially reduced amount of

In addition, viable cells adhered sparsely on the SS-DM-HPG4 and SS-TA-HPG4 surfaces (Figure S6i,j), indicating comparable reliability of these bioinspired anchors in providing a functional platform postmodification. The adhesion assay results of the waterborne Gram-negative Staphylococcus epidermidis (Figure S7) also exhibit a trend similar to that of Pseudomonas sp., illustrating the antiadhesion properties of HPG coatings against different types of bacteria. On the basis of the bacterial cells count from the fluorescence micrographs, the HPG-functionalized surfaces exhibited a 10-fold reduction against initial adhesion in comparison to that of the pristine SS surface (Figure S8). This result is in agreement with the previous studies that report that HPG coatings constructed by H


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Figure 6. SEM images of the biofilm formation for S. epidermidis on (a and b) pristine SS, (c) SS-DM, (d) SS-DM-HPG4, (e) SS-TA, (f) SS-TAHPG4, (g) SS-PDA, and (h) SS-PDA-HPG4 surfaces after 24 h of immersion in the bacterial culture at 37 °C. Scale bars are (a and c−h) 10 μm and (b) 5 μm.

biofilm formation in comparison to that of the pristine SS surface (Figure S9). 3.4. Amphora coffeaeformis Settlement Assay. The benthic microalgae A. coffeaeformis is one of the most commonly encountered raphid diatoms integrated in the biofilms of submerged surfaces. As such, they are often employed in antifouling assays.41,42,55 During the 24 h settlement period, a large amount of diatoms clumped in small clusters and fouled the pristine SS, SS-DM, SS-TA, and SS-PDA surfaces (Figure 7a−d). The fact that cluster formation is preferred during A. coffeaeformis fouling implicates high susceptibility of the substrates. In comparison, only a few algal cells settled and distributed individually on the HPG-modified

adhered cells, which are sparsely distributed (Figure 5d,f,h). The inhibition of bacterial adhesion endured the extended incubation period and eventually prevented the formation of biofilm on the HPG-modified surfaces. The surface hydration layer of the HPG coatings effectively maintains a continuous dilution state in aquatic or plasmic media and thereby assumes a self-cleaning effect against microfouling. Similar results are observed for the biofilm formation assay of S. epidermidis (Figure 6), demonstrating the prevalence of antifouling properties provided by the HPG coatings. On the basis of the bacterial cell count from the SEM images, the HPGfunctionalized surfaces exhibited a 10-fold reduction against I


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Figure 8. Amount of A. coffeaeformis settled on the pristine, biomimetic-anchored, and HPG-modified SS surfaces after 24 h of immersion in the algal suspension at 25 °C. Error bars denote the standard deviation from three replicates.

surface to the suspension. Under an excitation wavelength (λex) of 440 nm, the chlorophyll of A. coffeaeformis cells exhibits autofluorescence with a major emission peak centered at ∼690 nm (Figure S11). Hence, fluorescence intensity of the planktonic algal suspension can be used to measure the cell density, as shown by the calibration curve of Figure S12. In addition, fluorescence intensity of the algal suspension increases slightly (∼18%) with the extended time of ultrasonic treatment and reaches a constant after ∼6 min (Figure S13), implying that ultrasonic treatment has no diminishing effect on the algal autofluorescence capacity. The slight enhancement in fluorescence intensity has probably resulted from a more uniform dispersion of the microalgae upon ultrasonic treatment. Therefore, the quantification method using the peel-off technique is reliable and can account for the overall fouling intensity of a surface. In an algal suspension containing 105 cells/mL, the degree of fouling on the pristine SS surface reaches 14 600 cells/cm2 (Figure 8). The SS-DM, SS-TA, and SS-PDA surfaces also suffer from heavy fouling of 13 800, 13 100, and 13 300 cells/ cm2, respectively. In comparison, the HPG-modified surfaces exhibit a low fouling effect in the algal suspension. With the increasing degree of thiolation on the SS-PDA-HPG1 to SSPDA-HPG4 surfaces, the number of settled algae decreases from 5200 to 1500 cells/mL (Figure S14). An increase in reactive thiol functionals has resulted in a correspondingly higher grafting density and surface coverage of the HPG-SH coatings. In addition, the SS-DM-HPG4 and SS-TA-HPG4 surfaces also show low algal settlement at 3300 and 2600 cells/ cm2, respectively, indicating comparable functionalities of the surface anchors from monolayer DM, multilayer TA and polymeric PDA.

Figure 7. Fluorescence micrographs of A. coffeaeformis settled on (a) pristine SS, (b) SS-DM, (c) SS-TA, (d) SS-PDA, (e) SS-PDA-HPG1, (f) SS-PDA-HPG2, (g) SS-PDA-HPG3, (h) SS-PDA-HPG4, (i) SSDM-HPG4, and (j) SS-TA-HPG4 surfaces after 24 h of immersion in the algal suspension at 25 °C. Scale bars are 50 μm.

surfaces (Figure 7e−j). The flexibility and high mobility of the HPG coatings in water probably have weakened the adhesion of microalgae on the surface. In this work, a quantitative assay of A. coffeaeformis settlement was developed using a “peel-off” technique to validate the low fouling efficacy of the HPG coatings. The settled algal cells were exfoliated from the fouled surface of 1 cm2 size by cleaning in an ultrasonic water bath. After a cleaning period of 10 min, no fluorescence spots were discernible on the previously fouled surface (Figure S10), indicating complete detachment of the algal cells from the

4. CONCLUSIONS In a collective design of surface functionalization, the formation of monolayer, multilayer, and polymeric layer anchors on stainless steel (SS) substrates has been achieved respectively by deposition of the biomimetic N-dopamine maleimide (DM), tannic acid (TA), and polydopamine (PDA). Highly hydrophilic hyperbranched polyglycerol (HPG) with thiol moieties J


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(HPG-SH) was synthesized for subsequent tethering on the SS surfaces with biomimetic anchors via Michael addition or thiol−ene “click” reaction to impart antifouling property. The grafting density of HPG-SH can be controlled by tuning the degree of thiolation. In comparison to the pristine and biomimetic-anchors-functionalized SS surfaces, the HPGmodified surfaces substantially reduced the adhesion of Gram-negative Pseudomonas sp. and Gram-positive S. epidermidis and further inhibited the biofilm formation of these bacteria. Furthermore, the HPG-modified surfaces also exhibit antifouling effect against A. coffeaeformis settlement. The surface modification strategy inspired by nature was achieved in a simple manner to produce environmentally benign antifouling coatings.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.iecr.5b03735. GPC spectra, XPS elemental ratio, 1H NMR spectra and actual thiol fraction of HPG-SH, grafting density of HPG-SH coatings, AFM images of surface coatings by different anchors, fluorescence micrographs and quantitative counts of bacterial fouling on sample surfaces, emission wavelength of microalgae, calibration curve of microalgal density, and amount of microalgal fouling on the sample surfaces. (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected] (E.T.K.). *E-mail: [email protected] (S.L.M.T.). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We acknowledge the financial support of this study from the Singapore Millennium Foundation Grant (NUS WBS No. R279-000-428-592).

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REFERENCES

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