Nature-Inspired and “Water-Skating” Paper and Polyester Substrates

Article Cite This: Biomacromolecules XXXX, XXX, XXX−XXX

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Nature-Inspired and “Water-Skating” Paper and Polyester Substrates Enabled by the Molecular Structure of Poly(γ-stearylα,L‑glutamate) Homopolypeptide Cornelia Rosu,*,†,§ Yeongseon Jang,†,⊥ Lu Jiang,†,‡ and Julie Champion† †

School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332, United States Renewable Bioproducts Institute, Georgia Institute of Technology, Atlanta, Georgia 30332, United States § Georgia Tech Polymer Network, GTPN, Georgia Institute of Technology, Atlanta, Georgia 30332, United States Downloaded via KAOHSIUNG MEDICAL UNIV on November 16, 2018 at 14:37:15 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

‡

S Supporting Information *

ABSTRACT: We demonstrate that the molecular structure of a synthetic homopolypeptide that resembles the leg architecture of water strider insects is effective to impart flexible polymeric surfaces with superhydrophobic behavior. Filter paper (FP) and polyester (PET) were modified with a coating consisting of low-molecular weight α-helical poly(γstearyl-α,L-glutamate) (PSLG, Mw = 4500 Da) homopolypeptide. PSLG-coated substrates displayed near to and superhydrophobic behavior (≥150°) as reflected by the contact angle values. Despite being physically adsorbed, the PSLG coating uniformly covered and was strongly adhered to the substrate surfaces. The thin coating layer displayed remarkable mechanical abrasion resistance and was insensitive to long-time exposure to ambient conditions. PLSG-coated textile fibers exhibited useful and interesting properties. Under an iron-containing load, PSLG-coated PET was able to float and “walk” on water when exposed to a magnet. The PSLG coating was able to reduce the adhesion of Escherichia coli, model Gram-negative bacteria. The results indicated that the molecular geometry of PSLG homopolypeptide, which possesses a α-helical backbone sprouting out of highly hydrophobic stearyl side chains, was the key feature responsible for the observed behaviors. This study is relevant for a broad range of potential applications: from crop and drinking water management in arid geographic areas to biomedical devices and implants.

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INTRODUCTION Materials with superhydrophobic properties are extremely important in a variety of applications such as anti-icing,1 anticorrosion,2,3 microfluidic4,5 and optical devices,6 sensors,2,7 and batteries.2,7 Recent work has been directed toward paper8 and textiles9−11 because imparting superhydrophobicity to these materials expands their range of potential applications. A superhydrophobic surface is characterized by an apparent water contact angle ≥150° and, in many cases, displays selfcleaning properties2 derived from a stable Cassie−Baxter state.12 These features are a consequence of dual-scale architecture of the material surface. A variety of methods have been used to achieve this prerequisite topology: simple modification of the substrate by plasma technology, electrochemical etching to increase roughness, use of inorganic and organic coatings, and combinations of these approaches.13−17 An appealing approach to achieving superhydrophobic behavior is to mimic natural structures.18 The most cited example of a natural superhydrophobic and self-cleaning surface is that of lotus leaves.19 They possess convex cell papilla coated with an epicuticular wax (lipid) layer. Many other plants have developed leaves with a hairy architecture.20 This topology is not only useful for generating the above© XXXX American Chemical Society

mentioned properties in plants but also crucial for survival of many animal species.21 One particular example is the Gerridae family of insects, also known as water striders.22 The legs of water striders have waxy and flexible grooved hairs that support the ability to capture air when they contact water surface.23 These hairy structures induce self-removal of water droplets, a prerequisite of self-cleaning, and, in general, protect from bacteria attachment.24 The ability of these insects to move easily while afloat has received tremendous interest to design biologically inspired mobile robots.25 Scaled to millimeter size, these robots lack the performance and elegance of natural water striders. Approaches designed to closely mimic the natural architecture of water striders use expensive tools. For example, Suzuki et al. employed femtosecond laser machining to fabricate spiral grooves on brass wires and subsequently deposited a fluorine agent.26 A robotic assembly reported by Ozcan et al. involved laser-cutting to generate circular footpads.27 Bai et al. have used a combination of electroReceived: August 30, 2018 Revised: October 31, 2018

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DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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the ability to mimic “walking on water” like water striders. PSLG coating was found to provide another feature required in nature, reduction of bacterial adhesion. Potential applications of PSLG coating include textiles able to collect water from fog and paper-made biomedical devices for health monitoring/ diagnosis kits as well as printed electronic devices.

spinning and template-selective removal by thermal degradation to obtain polyimide grooved fibers.28 These examples highlight that mimicry of water strider leg architecture in a simple, perhaps one-step process, still awaits development. Such approaches will require the use of smart coatings or, simply, materials similar in structure down to the molecular level with that of insect legs. In this regard, biopolymers may be viewed as an appealing solution to mimic these natural constructs. It is known that from the large family of biopolymers, natural peptides and polypeptides are able to display a variety of secondary conformations which are important in regulating many natural processes. Nonetheless, their synthetic homologues are interesting and useful because they allow processing from a broad spectrum of solvents.29,30 From the synthetic polypeptide family poly(γ-stearyl-α,L-glutamate) (PSLG) is unique. PSLG macromolecule has a helical backbone functionalized with stearyl side chains that spread out similarly to tree branches and, at the molecular level, is reminiscent of the structure of water strider legs.31,32 Despite the fact that physical behavior of PSLG was previously studied,32−34 to date, less is known about how to manipulate the molecular geometry of this homopolypeptide and design materials with useful and interesting properties. Previous studies have suggested that PSLG was able to induce certain behaviors. For example, PSLG linked by the growing f rom and grafting to approaches to spherical silica core particles35,36 and immersed in a PSLG cholesteric liquid crystal formed islets of remarkable stability whose organization could not be disturbed by an applied magnetic field.36,37 Upon changing the core shape to a dome-like appearance, PSLG− silica composite particles were observed to follow patterns associated with a cholesteric arrangement and also selforganized into stable crystalline structures of hexagonal and lamellar geometries.38 Interdigitation of waxy and branchy stearyl side chains within the above assemblies was suspected to generate the observed behaviors. In many regards, PSLG resembles the structure of lipid layers that form the outer cell membrane of many microorganisms.39 Grafted on both flat and curved solid surfaces, PSLG was found to promote adsorption of lipases from the Candida rugosa family, an enzyme used as a catalyst in biotechnology.37,40,41 Candida rugosa lipase requires a highly hydrophobic support to attach and fold into its active state.42 The observed high efficiency of PSLG−silica particles as a lipase carrier also suggested that the disposition of the PSLG macromolecule may play a key role.37 Because of its molecular structure that resembles the architecture of water strider legs, it was hypothesized that coating PSLG on flexible polymeric substrates may impart them with highly water repellent behavior. In this study, mixtures of the PSLG homopolypeptide in dodecane (DD) were used to modify the surfaces of filter paper (FP) and polyester (PET). The water repellent behavior of the PSLG-coated substrates was evaluated by goniometry. The contact angle values (≥150°) indicated that PSLG was able to impart superhydrophobic behavior of the surfaces. Tests under conditions that mimic rain and peeling, folding and exfoliation were performed to investigate PSLG adhesion to the surface and its resistance to mechanical abrasion. Aging tests were performed by exposure to the ambient conditions for more than two months. Different protocols of wicking tests were used to evaluate whether the PSLG-coated substrates had

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EXPERIMENTAL SECTION

Materials. L-Glutamic acid (99%), stearyl alcohol (octadecanol) (99%), tert-butanol, (99.5%), 1-butanol (99.8%), triethylamine (99.5%), anhydrous ethanol (200PRF), sulfuric acid (99.999%), methanol, anhydrous hexane, ethyl acetate, anhydrous tetrahydrofuran (THF), sodium carbonate (anhydrous powder, 99.999%), hexamethyldisilazane (reagent grade, ≥99%), Celite S, Whatman filter paper (55 mm circles), anhydrous dichloromethane (DCM), acetone and dodecane (DD, ReagentPlus, ≥99%) were purchased from Sigma-Aldrich and used as received. Triphosgene was obtained from TCI America. Poly(γ-benzyl-α,L-glutamate (PBLG, Mw = 22 000 Da, Đ = Mw/Mn = 1.04 ± 0.005) was procured from Polysciences, Inc.). Glass Petri dishes (60 × 15 mm) were procured from VWR. Polyester (polyethylene terephthalate (PET), Anticon 100 Heavyweight Series Cleanroom Wipes, 9 × 9 in., Contec brand) were obtained from VWR. Wipes contain 100% continuous filament polyester double-knit interlock fabric. One-sided Scotch Magic Tape (3M) was used for peeling tests. Six well tissue cell culture plates and 50 mL tubes for bacterial cell culture and release were obtained from VWR. Preparation of Poly(γ-stearyl-α,L-glutamate) Polypeptide, PSLG. γ-Stearyl-α,L-Glutamate Amino Acid (SLG). SLG was prepared following the procedure reported by Wasserman et al.43 Details are available in the report by Rosu et al.36 γ-Stearyl-α,L-Glutamate N-Carboxyanhydride (SLG-NCA). The SLG-NCA monomer was prepared by the ring closure of the γ-stearylL-glutamate amino acid in the presence of triphosgene, as reported by Daly and Poche.44 Details are available in the report by Rosu et al.36 Poly(γ-stearyl-α,L-glutamate) Homopolypeptide (PSLG). The synthesis of PSLG followed the report by Daly and Poche.36,44 Briefly, SLG-NCA monomer (1 g, 2.3 × 10−3 mol) was dissolved in 50 mL of dry DCM. After the solution became clear upon swirling, 1.28 mL of a 2% v/v solution of triethylamine in DCM ([M]/[I] = 10) was added under continuous magnetic stirring. The flask was connected to a nitrogen bubbler and the reaction continued for 3 days at 30 °C. The mixture was then precipitated in acetone (100 mL). The white precipitate was collected by suction filtration and dried in vacuo. Preparation of PSLG/Dodecane Mixtures. Solutions of 0.5, 1, 1.5, 2 and 3% (w/w) were prepared in 20 mL scintillation vials by dissolution of PSLG polymer in dodecane (DD). The mixture was heated to 60 °C for 20 min until it became clear and subsequently was allowed to cool at room temperature. All steps are illustrated in Scheme 1. Preparation of PSLG-Coated Paper and Polyester Substrates. Squares (1.5 in. ×1.5 in.) of filter paper and polyester were immersed in the PSLG/dodecane solutions preheated at 60 °C. Then they were allowed to soak for 3 min in the cooling mixture. After soaking, the samples were placed in glass Petri dishes and dried in vacuo overnight at 45 °C. The PSLG-coated substrates are abbreviated as follows: filter paper (PSLG0.5/FP, PSLG1/FP, PSLG1.5/FP, PSLG2/FP) and polyester (PSLG0.5/PET, PSLG1/PET, PSLG1.5/ PET, PSLG2/PET). Bacteria Cultures and Characterization. Gram-negative E. coli (BL21) was used in this study as model microorganism for bacterial adhesion assays. The samples (squares of 1 cm × 1 cm) were transferred into 6-well cell culture plates and incubated with 5 mL of bacterial solution with optical density (O.D.) 0.3 (≈5 × 107 cells/ mL) in lysogency broth (LB) media. E. coli cells were cultured on the samples for 24 h in a static incubator (37 °C). To quantify the number of E. coli attached to each surface, the colony forming units (CFUs) of cells detached from the surfaces were counted using the B

DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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then multiplying by the initial volume of cell suspension (5 mL). In order to visualize bacterial adhesion on the surface using SEM, the samples were prepared and incubated in bacterial solution with same procedure described above. After the incubation, the samples were gently washed with PBS three times and fixed with 2.5% glutaraldehyde solution for 1 h. Subsequently, they were dehydrated using a series of ethanol concentrations in distilled water (i.e., 50%, 70%, 90% and 100% ethanol for 20 min, respectively). The dehydrated samples were dried by hexamethyldisilazane treatment overnight. Gel Permeation Chromatography, GPC. The molecular weight of PSLG was measured by gel permeation chromatography with multiangle light scattering, (GPC-MALS). An instrument equipped with an Agilent 1100 solvent degasser, Agilent 1100 pump and Agilent 1100 autosampler was used for separation. The column set was a 10 μm, 50 mm × 7.8 mm guard column and two Phenogel 300 mm × 7.8 mm columns from Phenomenex, Torrance, CA: (1) 10 μm, 105 Å (10 kDa-1000 kDa) and (2) 10 μm, MXM, (100 Da−10 000 kDa). A Wyatt Dawn DSP-F multiangle-light scattering detector used a He− Ne laser. A Hitachi L-7490 differential index detector (32 × 10−5, refractive index full scale) served as concentration detector. An injection volume of 100 μL was used for separation. The mobile carrier was THF (1 mL·min−1) stabilized with 250 ppm butylated hydroxytoluene. The specific refractive index increment of PSLG was taken as 0.080 ± 0.002 mL·g−1.32 Fourier-Transform Infrared Spectroscopy, FTIR. A Thermo Scientific iS50 FTIR spectrometer was used to identify the characteristic adsorption bands of coated fabrics, plain PET and MTMS-based coating mixture alone. The instrument is equipped with a long lifetime Polaris infrared source, a fixed DLaTGS detector with KBr window, and a Ge or KBr beamsplitter. Spectra were an average of 32 individual scans collected at 8 data point resolution. Spectra were also background (32 scans) and baseline corrected. X-ray Photoelectron Spectroscopy, XPS. The chemical composition of the PSLG-coated filter paper and PET fabrics was determined with a Thermo K-Alpha XPS (Thermo Fisher Scientific, West Palm Beach, FL) equipped with a monochromatic Al Kα X-ray source (hυ = 1486.6 eV), with a 400 μm diameter beam operating at a vacuum below 10−7 Pa. High-resolution and survey spectra of individual elements were recorded for each sample. The number of scans was varied between 4 and 20. Peak locations were calibrated against that of C 1s which occurred at 284 eV. Peak fitting of the highresolution spectra was performed with Thermo Avantage 5.934 software. Prior to analyses, samples were degassed in vacuo overnight. Contact Angle Goniometry, CA. Contact angles were measured with a Ramé-Hart CA goniometer (Model 290, Succasunna, NJ) equipped with a camera for image capture. Samples were affixed to the instrument stage with double-sided tape (3M). The volume of the

Scheme 1. Schematic Illustration of Coating Filter Paper (FP) and Polyester (PET) Substrates with PSLG Homopolypeptidea

a

The blue-framed inset shows the chemical structure of PSLG and the cartoon illustrates PSLG α-helical structure with stearyl side chains sprouting out like tree branches from the backbone. spread plate method. At the end of incubation, samples were rinsed three times with phosphate-buffered saline (PBS) and transferred into a 50 mL tube with 5 mL of fresh PBS. Each sample was sonicated for 10 min and vortexed for 30 s to release bacteria remaining on the sample surface into the solution. The initial dilution was made by transferring 25 μL of the resuspended cell solution into 225 μL of fresh PBS (10−1 dilution). Subsequently a series of diluted solutions (10−1−10−8) in PBS were prepared in 96 well plates. Then, 0.1 mL of each diluted solution of E. coli was spread onto LB agar plates. Bacterial colonies, between 30 and 300 colonies on each plate, were counted after 24 h of incubation at 37 °C. The number of viable bacteria expressed as colony-forming unit (CFU) per sample was calculated by dividing the number of colonies by the dilution factor multiplied by the amount of cell suspension plated to agar (0.1 mL),

Figure 1. Comparative FTIR spectra of FP, PSLG, PSLG2-coated FP (A, black, red, blue) and PET, PSLG, PSLG2-coated PET (B, black, red, blue). Spectra were offset by 20 transmittance units for better clarity. C

DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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Biomacromolecules Table 1. Number-Average and Weight-Average Molecular Weights (Mn, Mw), Polydispersity Index (Đ), Degree of Polymerization (DP), Chain Length (L) and Number of Helical Turns peak

Mn (kDa)

Mw (kDa)

Đ

mass recovery (%)

DP

L (Å)a

helical turnsb

P1 P2

234 ± 14.6 3.85 ± 0.3

360 ± 13.5 4.5 ± 0.3

1.55 ± 0.05 1.17 ± 0.09

2.4 ± 0.15 94 ± 1

− 11

− 60

− 3

a Based on Mw: L = (Mw/M0) × 1.5, M0 = 381 g mol−1 (the monomer unit mass), 1.5 Å is the projection of the helix turn. bCalculation formula: (Mn/3.6 × M0), one single turn of the helix requires 3.6 monomer units

Figure 2. Comparative XPS survey scans of FP (A), PSLG2/FP (B), PET (C) and PSLG2/PET (D).

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sessile drop was 4 μL. The reported contact angle values represent the average of at least five measurements at different locations on each sample. In the case of PSLG-coated samples, diverse conditions were used for recording CA values. Static contact angle (SCA) was determined by landing the water droplet normally onto the surface while for impact contact angle (ICA) the droplet was dispensed from 5 cm height. The latter setup mimics rain conditions. Contact angle in static and impact mode were also measured after the sample was subjected to abrasion by peeling (PSCA, PICA). Single-sided 3M tape was pressed against the sample by thumb and detached using tweezers. The aged (2 months) PSLG-coated filter paper substrates were folded several times by hand and SCA was evaluated in the folded area. Scanning Electron Microscopy, SEM. The morphology of the control and coated paper and fabric surfaces was inspected with a Hitachi SU8230 cold field-emission scanning electron microscope (Hitachi High Technologies Co., Japan). The instrument was operated at an acceleration voltage of 1 keV and a current of 10 μA. Samples were affixed/grounded to stainless steel stubs (D = 12 mm, Electron Microscopy Sciences) by double-sided conductive tape (Electron Microscopy Sciences). Before imaging they were sputtercoated for 4 min with Ag/Pd to mitigate charging effects during exposure to the electron beam. Statistical Analysis. All experiments for bacterial cell studies were performed in triplicate and were repeated twice. Mean values with the standard error of the mean (mean ± Standard Error of Mean in caption of Figure 8) were calculated, and the statistical significance was assessed by t-test with p-values less than 0.05 considered being statistically significant.

RESULTS AND DISCUSSION PSLG preparation involves amine-initiated ring opening polymerization of its γ-stearyl-α,L-glutamate N-carboxyanhydride monomer.44 Synthesis of PSLG homopolypeptide was confirmed by Fourier-Transform infrared spectroscopy (FTIR, Figure 1). The red traces in Figure 1A,B show the specific vibration bands of amide I (1655 cm−1) and amide II (1545 cm−1) associated with the α-helical secondary conformation of PSLG.32,35−38 Contribution from asymmetric and symmetric stretching of stearyl side chains was detected in the range of 3000−2800 cm−1 wavenumbers. The signal associated with chain terminal amino group was centered at ∼3200 cm−1 and that of ester at ∼1750 cm−1. The polymer structure was also evidenced by 1H NMR (Figure S1). PSLG was further characterized by gel-permeation chromatography coupled to multiangle light scattering detection (Table 1, Figure S2). Two Gaussian peaks were detected: P1 (Mw = 360 ± 30.5 kDa, Đ = Mw/Mn = 1.55 ± 0.05) and P2 (Mw = 4.5 ± 0.3 kDa, Đ = 1.17 ± 0.09). The mass recovery percentage (∼2 wt %) indicated that P1 was in small trace and was likely associated with aggregation behavior. Therefore, the absolute molecular weight of the polymer was assigned to P2 (DP = 11). Wellknown is the ability of rodlike polypeptide chains to form aggregates by end-to-end assembly.33,45 PSLG consisted mainly of short helical chains of about 3 turns. Once the preparation of α-helical PSLG was confirmed by GPC and FTIR, PSLG/DD mixtures were used to coat filter paper (FP) and polyester (PET) as shown in Scheme 1. Upon D

DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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those found in PSLG2/FP (Figure 2B) were identified in PSLG2/PET (Figure 2D). The similar appearance of these two survey scan profiles confirms the presence of PSLG at the surface of both FP and PET. Furthermore, a common trend was observed: significant decrease in O 1s signal concomitantly with increased C 1s intensity. In support, Table 2 shows that

unassisted cooling at ambient temperature the PSLG/ dodecane solutions (0.5−2 wt %) displayed a turbid appearance. Sequential heating and cooling demonstrated the thermoreversible behavior of the mixtures, as they turned clear (thin liquid) and turbid (thick liquid) again. None of the four mixtures presented the properties of a free-standing gel (inversion vial test). A 3 wt % mixture formed a true gel and was not considered further for coating. Immersion of FP and PET substrates in PSLG/DD mixtures preheated at 60 °C, soaking for 3 min under unassisted cooling to ambient temperature and in vacuo drying (45 °C) yielded PSLG-coated surfaces. The PSLG-coated substrates are abbreviated as follows: filter paper (PSLG0.5/FP, PSLG1/FP, PSLG1.5/FP, PSLG2/FP) and polyester (PSLG0.5/PET, PSLG1/PET, PSLG1.5/PET, PSLG2/PET). FTIR was used to investigate whether PSLG was present at the substrate surface and, most importantly, if α-helical conformation was preserved after solvent evaporation. The FTIR trace of PSLG-coated FP (Figure 1A, blue trace) clearly reflects the amide I and amide II signals indicative of α-helical structure (1655 and 1547 cm−1). They were identified at the same wavenumbers as in pristine PSLG (Figure 1A, red trace). In addition, all vibration peaks of cellulose from paper were present in the spectrum. Specifically, a broad vibration band assigned to glucose’ −COC− and ring stretching was centered at ∼1000 cm−1 (Figure 1A, black trace). The bending vibrations of −COH and −CHCH2− overlapped under a broad peak centered at ∼1400 cm−1. Interestingly, the signal associated with hydroxyl (OH) groups (∼3300−3600 cm−1) was very weak (Figure S3). This fact suggested the presence of trace additives used in paper manufacturing. Presumably, vibration bands originating from these compounds were overlapping with and possibly screening those of cellulose. Although attenuated in intensity, the specific vibration peak characteristic to PSLG amide I (1658 cm−1) and amide II (1548 cm−1) were also identified in the coated PET (Figure 1B, blue trace), confirming the trends observed in FP coating. The presence of PSLG at the surface of PET was also supported by the strong absorption bands associated with stearyl side chains centered at 2920 cm−1 (CH2) and 2850 cm−1 (CH3) and also the signal at 3292 cm−1 (NH2). Pristine polyester (PET) presented the specific −CH (718 cm−1), −OCO− (1089 cm−1), −CCO− (1242 cm−1) and −CO (1713 cm−1) strong absorption bands (Figure 1B, black trace). In addition, aromatic and aliphatic CH2 stretching bands were identified at (∼3000 cm−1) and (2915 cm−1), respectively. Successful coating of FP and PET substrates with PSLG was also evidenced by XPS (Figure 2). Figure 2A shows the specific elemental fingerprint detected for neat FP at 530.5 eV (O 1s) and 283.5 eV (C 1s). XPS confirmed that trace elements, likely due to paper manufacturing, were present in the paper and were identified at 1071.7 eV (Na 1s), 780.5 eV (Ba 1s), 153 eV (Si 2s) and 104 eV (Si 2p), respectively. Two additional small peaks centered at ∼800 and 500 eV were unknown. The presence of the PSLG coat at the surface of FP was clearly evidenced by the occurrence of the N 1s peak (498 eV) (Figure 2B). The peaks of trace elements all disappeared except those of Si 2s and Si 2p but were substantially diminished. The second substrate, PET, followed the same trend as its FP homologue. In the survey scan of uncoated PET, O 1s and C 1s signals occurred at 532.5 and 285.5 eV, respectively (Figure 2C). Identical elemental signatures to

Table 2. Sample Name and Surface Elemental Composition Percentage from XPS Investigation Elemental Composition (%) Sample

Si

C

N

O

Na

FP PSLG2/FP PET PSLG2/PET

25.61 8.62 − −

15.96 65.11 74.72 83.76

− 3.99 − 2.77

55.29 22.28 25.28 13.47

3.13 − − −

the oxygen content decreased with approximately 23% and 12% in PSLG2/FP and PSLG2/PET while the carbon composition increased with 50% (PSLG2/FP) and 9% (PSLG2/FP). Presumably, this variation is due to the carbon-rich stearyl side chains linked to the PSLG backbone. Most probably, they screen oxygen from cellulose and polyester skeletons. The survey data demonstrate that PSLG uniformly covered the FP and PET substrates. Additional evidence on successful PSLG coating was provided by deconvolution of the high-resolution XPS spectra of carbon (Figure 3). The C 1s signal for FP was resolved into three distinct peaks (Figure 3A) reflecting the local environment of the carbon atoms. Carbon bonded to other carbon atoms (CC) had a binding energy of 284 eV. The large number of carbon− oxygen bonds (CO) of cellulose constituent gave an ample signal centered at 285 eV. The OCO bond of α-Dglucopyranose units was also detected at 287 eV. A distinct molecular environment of carbon was identified in PSLG2/FP (Figure 3B). The peak assigned to CC bonds was markedly increased in intensity and slightly shifted to 285 eV, indicating an increase in the aliphatic carbon content at the surface, also supported by the disappearance of CO and OCO signals seen in FP. The specific homopolypeptide amide linkages OCNH and CNH were found at 286 and 287 eV, respectively. The carbon environment in PET was dominated by CCC bonds of aromatic ring centered at 285 eV. The binding energies of CO and CO bonds were identified at 286.5 and 289 eV, respectively. The π−π* aromatic satellite peak was observed at ∼292 eV. As expected, the carbon chemical surroundings were markedly different after PSLG coating. In PSLG2/PET the C 1s signal was deconvoluted in three well-defined peaks. The most dominant was that associated with CC bonds (285 eV). The peaks originating from CNH and OCNH were identified at 286.5 and 289 eV, respectively. These values were identical with those recorded for PSLG2/FP. Altogether, FTIR and XPS data demonstrated the uniform coverage of FP and PET substrates with α-helical PSLG chains. Additional confirmation of uniform coverage and PSLG coating morphology was provided by SEM (Figure 4). Uncoated FP consisted of polydisperse cylindrical, long and entangled fibers, as discerned from Figure 4A. The inset image shows that the surface of the fibers seemed infrequently populated by debris. After coating (Figure 4B), the fibers were E

DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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Figure 3. XPS high-resolution scans of FP (A), PSLG2/FP (B), PET (C) and PSLG2/PET (D).

Figure 4. SEM images of FP (A), PSLG2/FP (B), PET (C) and PSLG2/PET (D). Scale bars: 100 μm. Insets show the specimen at high magnification. Scale bars: 5 μm (A, C) and 10 μm (B, D). F

DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX

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Biomacromolecules interconnected by porous coating film but their surface had a smooth appearance (inset). Plain PET fibers had a twisted, edgy appearance (Figure 4C) and, like FP, marked by some impurities (inset). After coating (Figure 4D), the fiber surface was very smooth and sparsely interconnected by a PSLG film (inset). It was not possible to quantitatively determine the thickness of the PSLG coat from high magnification SEM images because the difference between uncoated and coated fibers was very small. The investigation further focused on wetting behavior of PSLG/FP and PSLG/PET. Table 3 summarizes static contact Table 3. PSLG Concentration in Dodecane, and Static Contact Angle Values SCA/degrees (deg) PSLG concentration in dodecane (wt %) 0.5 1.0 1.5 2.0

FP 135.0 131.0 140.0 141.5

± ± ± ±

Figure 5. Contact angle values measured for 2 wt % PSLG-coated FP freshly made and aged for 2 months. The aged sample was subjected to six folding procedures and SCA was evaluated in the folded region. A layer of the coated paper was exfoliated and SCA was measured at the surface of the remaining coated sample.

PET 2.0 7.5 9.0 8.0

140.0 134.5 151.0 156.0

± ± ± ±

3.4 4.0 6.0 6.5

(∼500 μm) of the aged and six-times folded PSLG-coated paper was carefully removed by using tweezers. The SCA value measured at the surface of the remaining sample was centered at 143° ± 2°. This result confirmed the presence of PSLG in the depth of the paper. The control experiment performed on uncoated and exfoliated FP showed instant wicking upon contact with the water droplet similarly to that shown in Figure 6A. The elevation in hydrophobicity when compared to that recorded after the sixth folding was assigned to additional dual morphology created at the surface during exfoliation. Removal of paper layers likely causes breakage of some entangled fibers that in concert with the PSLG coating promotes the formation of air pockets that ultimately stabilize a Cassie−Baxter wetting state. This behavior was previously observed for roughly abraded polyester fabrics.11 Altogether, these tests demonstrated that a PSLG coating was able to impart paper substrates with remarkable wetting properties, due to its mechanical robustness and long-time durability. Rough mechanical abrasion and liquid adhesion testing were performed on two months-aged surface of PSLG2/PET by tape peeling and water droplet impact. The results, summarized in Table 4, showed that similarly to FP substrates,

angle (SCA) values recorded for the two substrates coated with PSLG/DD mixtures. For FP, SCA did not significantly depend on the PSLG/DD concentration and reflected a highly hydrophobic surface. Yet, as expected, higher content in PSLG (1.5 and 2.0 wt %) seemed to result in slightly higher SCA values (140.0° ± 9.0°, 141.5° ± 8.0°). SCA for all samples were close to the accepted limit for superhydrophobic behavior (150°). SCA values for PET were higher than those recorded for FP but followed the same trend with respect to the PSLG/ DD concentration. The most concentrated samples exceeded the agreed limit of superhydrophobic behavior (≥150°) and were centered at 151.0° ± 6.0° (1.5 wt %) and 156.0° ± 6.5° (2 wt %), respectively. The roll-off angles (RA) of a 4 μL water drop were ∼30° and ∼20°, respectively. The practical use of these substrates, especially paper, for example as packaging materials oftentimes require folding. In addition, the coated material is desired to have long-time shelf life without losing its properties such as hydrophobicity. In line with this idea, PSLG2/FP was allowed to age for 2 months at ambient conditions, as shown in Figure 5. Aging did not impact SCA value, 142° ± 3°, when compared to the freshly coated FP (141.5° ± 8°). The PSLG2/FP sample was further subjected to sequential folding (90°). After the first operation, the measured SCA value in the folded area increased to 154° ± 3°. A water droplet (4 μL) was able to roll off at about ∼30°. The limit required for superhydrophobicity (150°) was also reached after the second folding 150° ± 2°, but the RA was higher ∼50°. Apparently, at low tilt angle, the small droplet seemed pinned at the surface but once the surface inclination increased the droplet easily rolled off. In general, superhydrophobic surfaces are either “sticky” or “slippy”.46 PSLG coating showed an interesting transition between the two behaviors, property useful for applications requiring water collection from air and fog. Note that RA depends on droplet size.11 After the third folding, SCA started to slightly decline (147° ± 4°) and leveled at around 135° (folding 5 and 6). Folding of PSLG2/FP did not reveal a failure mode in coating hydrophobicity. Another test was then applied to gain insight about whether PSLG was able to penetrate thorough the depth of the entangled paper fibers network (Figure 4A). An upper layer

Table 4. Test Type and Contact Angle Values Recorded for Aged (2 Months) PSLG2/PET Fabrica test SCA ICA PSCA PICA

contact angle value/degrees 152 140 143 143

± ± ± ±

5 4 2 3

a

ICA, impact contact angle; PSCA, static contact angle after peeling; PICA, impact contact angle after peeling.

PSLG coat was able to effectively protect PET. Under impact, the contact angle value indeed decreased slightly (140° ± 4°) when compared to static conditions (152° ± 5°) but it was still close to the limit of superhydrophobicity (150°). This fact demonstrated that liquid was not able to penetrate through the depth of the fiber bundles. Rough peeling did not remove the PSLG layer, as the PSCA value (143° ± 2°) was, within experimental error, close to SCA value. Impact after peeling G

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Biomacromolecules PICA was 143° ± 3°, identical to PSCA. PICA confirmed that essentially PSLG covered uniformly and was strongly adhered to the surface of the fibers. These results also indicate that physical adhesion of PSLG coating may be stabilized by Hbonding between the polymer amide and substrate OH groups as well as by Van der Walls interactions between the hydrophobic parts of the polymer and substrate. Additional insight into the PSLG coating ability to effectively repel water, especially after aging, was acquired from the wicking test: uncoated and coated fabrics were placed on an air−water interface as illustrated in Figure 6.

water by using a metal washer for 30 min (Figure S4B). After releasing the weight, the PSLG2/FP sample was able to rise to the air−water interface and float again (Figure S4C). Three consecutive cycles were performed in the same manner and each time the sample displayed floating abilities. Interestingly, PSLG2/FP seemed to retain a thin film of water atop upon rising to air−water interface. Once the water was removed by shaking and equilibration at ambient conditions for 10 min, the SCA value was similar to that recorded after aging 143° ± 2° (Figure 5). This test showed that PSLG-coated substrate was able to preserve its near superhydrophobic properties in extreme water exposure conditions likely due to robust and uniform PSLG coverage. The remarkable dewetting observed during the wicking test also suggested that PSLG2/FP and PSLG2/PET may display other properties similar to water striders. To verify whether the coated samples are able to “walk” on water, PSLG2/PET loaded with a heavy load (metal washer) was set on an air− water interface (Figure S4A). Note that the weight of the metal washer was at least 1 order of magnitude higher than that of PSLG2/PET. The added mass mimics the weight of the insect body that is supported by its legs. Because of iron content of the washer, the sample was easily manipulated by a magnet (Movie 1, Supporting Information). Friction with water surface did not cause wicking. Air bubbles were visible at the metal− water−textile interface confirming the fabric’s hydrophobic nature. A dimple around the sample was also observed and it was caused by the balance between water buoyancy, fibercoated surface tension and the weight of the floating object. The test confirmed that PSLG2/PET has wetting properties similar to water striders. Again, this investigation provided clear evidence that the presence of PSLG coat induces fast dewetting that is supported by strong adherence of PSLG at the substrates surface. From a mechanistic standpoint, it is intriguing how a thin coating layer of short PSLG rodlike chains of about 34 Å in diameter32 were so efficient to impart the two polymeric surfaces with superhydrophobic behavior. The key feature of the observed substrate properties points to the molecular structure of PSLG. Additional control experiments performed by soaking the substrates in dodecane without PSLG and in poly(γ-benzyl-α, L -glutamate) (PBLG)/toluene mixtures strongly support this assumption (see Supporting Information, Control Experiments Section). The α-helical backbone of the polymer is stabilized by the NH···OC hydrogen bonds that, in general, restrain the segmental motion of the chain. On the other hand, the presence of side chains along the backbone influence its flexibility. Jeon et al. showed that in poly(γ-alkyl-Lglutamates) carrying different side groups (methyl, hexamethyl and stearyl) the hydrogen-bond strength decreased with increased side chain length.31 The simulation data performed on polymer chains of 11 repeat amino acid units, identical to the DP of the polymer used in this study, predicted that the geometrical structure of PSLG consists of a α-helical backbone flanked by stearyl side chains that sprout out like the tree branches.31 This structure also resembles closely the architecture of the water strider legs decorated with hairy nanopillars.22 It is also an unique molecular geometry when compared to other sister synthetic homopolypeptides whose side chain functional groups rather “hug” the backbone.47 Taking in account these structural particularities of PSLG, it is reasonable to assume that the oily stearyl chains prevent interaction of water with the less hydrophobic polymer

Figure 6. Images showing the wetting behavior of uncoated and coated FP (A) and PET (B) during the wicking test. Red-dyed water droplets were set in the static mode whereas the blue-dyed droplets were impinged from 5 cm height. The uncoated FP and PET wicked rapidly and settled at the beaker bottom.

Because of its hydrophilic nature, uncoated FP (Figure 6A) was rapidly wetted and sunk to the bottom of the flask. The weak hydrophobic nature of plain PET was not enough to prevent wicking and caused sample submersion (Figure 6B). Distinctly different behavior was observed for PSLG-coated samples. Regardless of the substrate nature, PSLG2/FP (Figure 6A) and PSLG2/PET (Figure 6B) were able to float at the water−air interface. Water droplets (20 μL) were placed onto substrate surface both in static (blue) and impact (red) conditions. The two samples remained afloat while carrying the droplets weight and floating persisted after flipping samples on the back side. This easy test demonstrated that dewetting occurs very fast because of the PSLG coat. The water droplets cannot penetrate through the fiber network and bridge with the water underneath. The wicking test proved that PSLG did not allow water penetration but it was reasonable to wonder about the effect of long-time exposure to water on these samples. In order to investigate this aspect, PSLG2/FP was forcibly immersed into H

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Figure 7. SEM images of E. coli adsorbed onto FP (A), PSLG/FP (B), PET (C) and PSLG/PET (D). White arrows point to bacterial cells.

backbone. Moreover, entanglement of PSLG helices due to solvent evaporation leads to side chain interdigitation, thus increasing the hydrophobic regions at the coating surface. Water droplets cannot penetrate through the coating; likely, they are cushioned by the air bubbles trapped between the fiber networks and prevent water from pinning. The inability of water droplets to anchor to the oily PSLG-coated induces roll off behaviors, feature characteristic to self-cleaning materials and many living organisms. In order to determine whether PSLG has an impact on bacterial adhesion, the two substrates, PSLG2/FP and PSLG2/ PET, and uncoated FP and PET were exposed to Gramnegative bacteria, E. coli (BL21). Gram-negative bacteria accounts for more antibiotic resistance due to a unique outer membrane surrounding the peptidoglycan layer of the cell wall.48 Therefore, it is important to prevent their adhesion onto surfaces. Figure 7 shows SEM images of PSLG-free and PSLG-coated substrates after exposure to E. coli cells for 24 h. SEM clearly showed that both homopolypeptide-coated surfaces PSLG2/FP and PSLG2/PET (Figure 7B,D) have a much lower number of attached E. coli bacteria than uncoated substrates FP and PET (Figure 7A,C), respectively. Counting of E. coli in the images confirmed these observations (Table S1). Furthermore, the presence of PSLG seemed to also interfere with the ability of E. coli to multiply and form colonies. In Figure 7A,C, long microbial rods containing 7−12 cells were observed across the paper and polyester fibers. In contrast, at the surface of coated substrates Figure 7B (PSLG2/FP) and Figure 7D (PSLG2/PET) the bacterial rodlike assemblies contained maximum three cells. While qualitatively SEM provided strong evidence that the waxy

PSLG reduced considerably the bacterial adhesion, it was also important to have quantitative insight. Evaluation of the colony forming units (CFU) is a typical quantitative measurement to evaluate the number of adherent bacteria on surfaces. Thus, CFU of detached bacterial cells was determined for PSLG-coated FP and PET surfaces as compared to PSLG-free surfaces after 24 h culture incubation (Figure 8). As a result, it is clear that the adhesion of E. coli was effectively inhibited on the PSLG-PET surfaces as compared to uncoated PET surfaces (p < 0.05). However, PSLG-FP surfaces did not show a significant statistical difference with uncoated FP surfaces (p > 0.05). We can interpret these results

Figure 8. Number of E. coli colony forming units on filter paper and PET fabric without or with PSLG coatings after 24 h of incubation (mean ± Standard Error of Mean, N = 4). Surface unit represents 1 cm2. I

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interactions that decrease the adhesion events to the surfaces of PSLG-coated FP and PET. There may also be a contribution from steric hindrance of the PSLG chains.

under the consideration of experimental protocols and the nature of FP surface properties. SEM images showed that E. coli cells were able to penetrate through the highly porous and networked structure of uncoated FP, which likely provided an efficient environment for cell thriving, multiplication and growth. The SEM images also showed that coated FP had very little E. coli attachment atop, suggesting that the bacteria contributing to the CFU counts may not have been attached but sterically trapped in between fibers. Conceivably, fiber entanglement could prevent a portion of bacteria cells to detach from the surface during sonication, thus explaining the large variation between samples. It is rather difficult to establish a standard reliable protocol for substrates like paper whose construction is made of layers, each containing highly entangled cellulose fibers. The overall results revealed that the use of PSLG as a bioinspired coating yielded multifunctional surfaces able to display a variety of properties: superhydrophobicity, self-cleaning, mechanical abrasion resistance, robustness and low bacterial adhesion. It is rather difficult to accurately describe the observed effect of PSLG on lowering bacterial adhesion mainly because, to date, the bacteria attachment mechanism to various surfaces is not fully elucidated. Many factors affect this extremely complex process.49,50 The environment (e.g., temperature, time of exposure, associated flow conditions, bacterial concentration), the material surface characteristics (morphology-roughness, physicochemical properties) are only a few.51 A handful of reports have pointed out that charge, chemical composition and topology of surfaces seem to influence how each type of bacteria invades a certain surface.51−54 If van der Waals forces or long-range electrostatic interactions between the substrate and microbial cell are attractive, likely the bacteria will adhere.55 A rough architecture of the substrate was found to promote bacterial adhesion when compared to a smooth surface.55 Unless treated with antimicrobial coatings,56 it was also demonstrated that bacteria had a high preference toward porous materials like FP because, due to their irregularities, they provide an increased surface area for cell growth.49 FP is a hydrophilic substrate due to the presence of cellulose OH groups. Owing to its chemical structure PET has a significantly lower density of OH groups at the fiber surface making it less hydrophilic. Therefore, negatively charged microbial cells should prefer PET because the repulsive electric double layer formed at the interface is markedly weaker than that in FP. Yet, the fact that statistically PET and FP were similarly populated by bacteria suggests that, in the case of FP, porosity was the dominating factor over long-range repulsive interactions. The PSLG homopolypeptide carry fatty acid-like side chains that resemble the character of the lipids from the outer membrane wall and from proteinaceous appendages (pili)57 of E. coli. It would be expected that interactions between these apparently compatible constituents would lead to physical binding of E. coli to PSLG coatings, but the data did not agree. It is known that extremely hydrophobic surfaces show antimicrobial abilities due to their dual-scale topology and surface chemistry.58,59 As discerned from the SEM images, PSLG coating has smoothed the appearance of both FP and PET. Therefore, it is reasonable to assume that the molecular structure of PSLG was the governing factor. The charge-free stearyl moieties of helical PSLG may induce perturbations at the interface that particularly prevent microbial cell adhesion. Likely mismatching between the structure of the polypeptide and bacteria appendages (or cell wall) may trigger unfavorable

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CONCLUSION Filter paper (FP) and polyester (PET) polymeric surfaces were coated with α-helical poly(γ-stearyl-L-glutamate) (PSLG), a synthetic homopolypeptide of Mn = 3.85 kDa. The coating process was simple, involving soaking of substrates in various mixtures of PSLG and dodecane (0.5−2 wt %) upon cooling from 60 °C. The PSLG coating covered uniformly the surface of FP and PET fibers while creating a thin layer, as shown by FTIR, SEM and XPS analyses. Static contact angle measurements demonstrated that the freshly coated samples displayed near superhydrophobic and superhydrophobic behaviors. Particularly, PET presented self-cleaning abilities because a 4 μL water droplet was able to roll off from the surface. A series of tests were performed on PSLG-coated samples to assess coating robustness, adhesion to surface and long-time exposure to ambient conditions. Peeling and impact testing demonstrated the remarkable mechanical robustness of PSLG coating due to the homopolypeptide strong adherence to the fiber surface. Aging did not show any change in substrate wetting as revealed by the contact angle values. Additional tests performed on aged PSLG2/FP such as folding and exfoliation showed a transition from near to superhydrophobic behavior and confirmed that homopolypeptide chains were able to penetrate into the depth of FP fiber layers. Loaded with a metal weight and placed onto water surface, PSLG2/PE was able to “walk” easily while afloat encouraged by an external magnetic field provided by a magnet. Supplemental wicking tests confirmed the superhydrophobic behavior of FP and PET and underlined that dewetting occurred very fast due to the presence of PSLG coating. Proof-of-concept experiments on bacterial adhesion performed by using E. coli, the model Gram-negative bacteria showed that PSLG was able to reduce microbial cell attachment to the surface of the fibers. The reduction in adhesion of E. coli suggested that likely the molecular structure of PSLG consisting of a α-helical backbone sprouting out oily stearyl side chains was the most predominant factor leading to the observed substrate behaviors. The results presented here offer new opportunities to harness homopolypeptides as effective tools to design flexible polymeric materials that mimic natural organisms and their properties. The simple technology involving PSLG−dodecane mixtures is easy transferable to various substrates. The use of bioderived and biocompatible homopolypeptide coating offers prospects for development of textiles able to collect water from fog, a potential solution to addressing the water scarcity in dry and underdeveloped geographic area. PSLG-coated paper and textile substrates examined here also provide a foundation for using these nature-inspired materials in implant devices, biomedical utensils and other devices whose performance depends on exposure to moisture and pathogenic bacteria.

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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.biomac.8b01312. Movie 1 (AVI) J

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1 H NMR spectrum of PSLG in THF-d8, GPC trace of the synthesized PSLG, FTIR spectrum of OH region for FP, images showing a wicking test setup for FP, table with E. coli count from SEM images using the ImageJ software, Control Experiments Section (PDF)

(6) Vullers, F.; Gomard, G.; Preinfalk, J. B.; Klampaftis, E.; Worgull, M.; Richards, B.; Holscher, H.; Kavalenka, M. N. Bioinspired Superhydrophobic Highly Transmissive Films for Optical Applications. Small 2016, 12 (44), 6144−6152. (7) Shawat, E.; Perelshtein, I.; Westover, A.; Pint, C. L.; Nessim, G. D. Ultra High-Yield One-Step Synthesis of Conductive and Superhydrophobic Three-Dimensional Mats of Carbon Nanofibers via Full Catalysis of Unconstrained Thin Films. J. Mater. Chem. A 2014, 2 (36), 15118−15123. (8) Khanjani, P.; King, A. W. T.; Partl, G. J.; Johansson, L.-S.; Kostiainen, M. A.; Ras, R. H. A. Superhydrophobic Paper from Nanostructured Fluorinated Cellulose Esters. ACS Appl. Mater. Interfaces 2018, 10 (13), 11280−11288. (9) Zimmermann, J.; Reifler, F. A.; Fortunato, G.; Gerhardt, L.-C.; Seeger, S. A Simple, One-Step Approach to Durable and Robust Superhydrophobic Textiles. Adv. Funct. Mater. 2008, 18 (22), 3662− 3669. (10) Wu, M.; Ma, B.; Pan, T.; Chen, S.; Sun, J. Silver-NanoparticleColored Cotton Fabrics with Tunable Colors and Durable Antibacterial and Self-Healing Superhydrophobic Properties. Adv. Funct. Mater. 2016, 26 (4), 569−576. (11) Rosu, C.; Lin, H.; Jiang, L.; Breedveld, V.; Hess, D. W. Sustainable and Long-Time ’Rejuvenation’ of Biomimetic WaterRepellent Silica Coating on Polyester Fabrics Induced by Rough Mechanical Abrasion. J. Colloid Interface Sci. 2018, 516, 202−214. (12) Cassie, A. B. D.; Baxter, S. Wettability of Porous Surfaces. Trans. Faraday Soc. 1944, 40 (0), 546−551. (13) Bigan, M.; Mutel, B. Cold remote plasma modification of wood: Optimization Process Using Experimental Design. Appl. Surf. Sci. 2018, 453, 423−435. (14) Balan, C. M.; Vlandas, A.; Senez, V. Tunable Contact Angle Hysteresis for Component Placement on Stretchable Superhydrophobic Surfaces. Adv. Mater. Interfaces 2018, 5 (12), 1701353− 1701360. (15) Tserepi, A.; Gogolides, E.; Bourkoula, A.; Kanioura, A.; Kokkoris, G.; Petrou, P. S.; Kakabakos, S. E. Plasma Nanotextured Polymeric Surfaces for Controlling Cell Attachment and Proliferation: A Short Review. Plasma Chem. Plasma Process. 2016, 36 (1), 107− 120. (16) Zhang, X.; Shi, F.; Niu, J.; Jiang, Y.; Wang, Z. Superhydrophobic Surfaces: From Structural Control to Functional Application. J. Mater. Chem. 2008, 18 (6), 621−633. (17) Jang, Y.; Choi, W. T.; Johnson, C. T.; García, A. J.; Singh, P. M.; Breedveld, V.; Hess, D. W.; Champion, J. A. Inhibition of Bacterial Adhesion on Nanotextured Stainless Steel 316L by Electrochemical Etching. ACS Biomater. Sci. Eng. 2018, 4 (1), 90−97. (18) Liu, M.; Wang, S.; Jiang, L. Nature-Inspired Superwettability Systems. Nat. Rev. Mater. 2017, 2, 17036. (19) Sun, T.; Feng, L.; Gao, X.; Jiang, L. Bioinspired Surfaces with Special Wettability. Acc. Chem. Res. 2005, 38 (8), 644−652. (20) Guo, Z.; Liu, W. Biomimic from the Superhydrophobic Plant Leaves in Nature: Binary Structure and Unitary Structure. Plant Sci. 2007, 172 (6), 1103−1112. (21) Mouterde, T.; Lehoucq, G.; Xavier, S.; Checco, A.; Black, C. T.; Rahman, A.; Midavaine, T.; Clanet, C.; Quéré, D. Antifogging Abilities of Model Nanotextures. Nat. Mater. 2017, 16, 658−663. (22) Bush, J. W. M.; Hu, D. L. Walking on Water: Biolocomotion at the Interface. Annu. Rev. Fluid Mech. 2006, 38 (1), 339−369. (23) Hu, D. L.; Bush, J. W. M. The Hydrodynamics of WaterWalking Arthropods. J. Fluid Mech. 2010, 644, 5−33. (24) Watson, G. S.; Watson, J. A.; Cribb, B. W. Diversity of Cuticular Micro- and Nanostructures on Insects: Properties, Functions, and Potential Applications. Annu. Rev. Entomol. 2017, 62 (1), 185−205. (25) Zhang, X.; Zhao, J.; Zhu, Q.; Chen, N.; Zhang, M.; Pan, Q. Bioinspired Aquatic Microrobot Capable of Walking on Water Surface Like a Water Strider. ACS Appl. Mater. Interfaces 2011, 3 (7), 2630− 2636.

AUTHOR INFORMATION

Corresponding Author

*C. Rosu. E-mail: [email protected]. ORCID

Cornelia Rosu: 0000-0001-8687-7003 Julie Champion: 0000-0002-0260-9392 Present Address ⊥

Department of Chemical Engineering, University of Florida, Gainesville, FL 32611

Author Contributions

C.R. conceived the project. C.R. performed experiments on polypeptide coating preparation, characterization and water repellent behavior. L.J. conducted XPS and SEM data acquisition. Y.S. performed the bacteria adhesion experiments and with help from J.C. interpreted the results. C.R. wrote the paper with input from all authors. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS C.R. appreciates support from Grants DMR 1306262 from National Science Foundation. Y.J. acknowledges funding from M.T. Campagna. L.J. is grateful to Renewable Bioproduct Institute (Georgia Institute of Technology) for her fellowship. C.R. thanks Prof. Paul S. Russo (School of Materials Science and Engineering, Georgia Institute of Technology) and Prof. Dennis Hess (School of Chemical and Biomolecular Engineering, Georgia Institute of Technology) for access to laboratory facilities, Dr. Rafael Cueto (Louisiana State University, Chemistry Department) for help with GPC-MALS measurements and Mr. Paul Balding (School of Chemistry and Biochemistry, Georgia Institute of Technology) for help with control IR and 1H NMR experiments. The authors acknowledge the Institute of Electronics and Nanotechnology (Georgia Institute of Technology), a member of the National Nanotechnology Coordinated Infrastructure supported by the National Science Foundation (Grant ECCS-1542174), for access to characterization facilities.

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REFERENCES

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DOI: 10.1021/acs.biomac.8b01312 Biomacromolecules XXXX, XXX, XXX−XXX