Antibacterial Structural Color Hydrogels - ACS Applied Materials

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Antibacterial structural color hydrogel Zhuoyue Chen, Min Mo, Fanfan Fu, Luoran Shang, Huan Wang, Cihui Liu, and Yuanjin Zhao ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b11258 • Publication Date (Web): 13 Oct 2017 Downloaded from http://pubs.acs.org on October 15, 2017

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ACS Applied Materials & Interfaces

Antibacterial structural color hydrogel Zhuoyue Chen,†,§ Min Mo,‡,§ Fanfan Fu,† Luoran Shang,† Huan Wang,† Cihui Liu,† and Yuanjin Zhao†* †

State Key Laboratory of Bioelectronics, School of Biological Science and Medical

Engineering, Southeast University, Nanjing 210096, China ‡

Department of Critical Care Medicine, Zhong-Da Hospital, School of Medicine, Southeast

University, Nanjing, China.

Keywords: structural color; colloidal crystal; hydrogel; AgNPs; antibacterial

Abstract

Structural color hydrogels with lasting survivability are important for many areas, while their anti-biodegradation capability is still lacking. Thus, we herein present novel antibacterial structural color hydrogels by simply synthesizing AgNPs in situ within the hydrogel materials. As the integrated AgNPs possessed wide and excellent antibacterial abilities, the structural color hydrogels could prevent bacteria adhering, avoid hydrogel damage, and maintain their vivid

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structural colors during application and storage. It was demonstrated that the AgNPs-tagged PNIPAM structural color hydrogels could keep their original thermal-responsive color transition even when the AgNPs-free hydrogels were degraded by bacteria, and the AgNPs-integrated selfhealing structural color protein hydrogels could save their self-repairing property instead of being digested and in ruins by bacteria. These features indicated that the antibacterial structural color hydrogels could be amenable to a variety of practically biomedical applications.


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1. INTRODUCTION Structural colors refer to materials that derive colors from the interaction of their periodically photonic nanostructures with light.1,2 During the long-term evolution, some creatures in nature exhibit brilliant structural colors to adapt to the selection pressure of survival and reproduction, including communication, attraction, propagation, disguise and other biological functions.3 Due to their striking brilliancy, scientists have been fascinated and devoted themselves to fabricating a series of bio-inspired structural color materials for different applications.4-10 Among these materials, structural color hydrogels, the combinations of highly ordered colloidal crystal arrays and elastic hydrogels, show great potential in generating arbitrary color distribution for given materials.11-15 As stimulus-responsive swelling or shrinking of the hydrogels would lead to change in the photonic band gaps (PBGs) or structural colors of the materials, the structural color hydrogels have been widely applied in colorimetric sensors,16-18 detection devices,19,20 optical devices,21 switches,22 etc.23,24 However, because of the biocompatibility of the hydrogel materials, most of the structural color hydrogels are suffering from bacterial adhesion and proliferation on their surface, which could degrade the hydrogel network, disorganize the periodic nanostructures, and finally destroy the PBGs or structural colors of the materials. This restricted the structural color hydrogels for many practical applications where persistent running or long-term storage is needed. Thus, the creation of structural color hydrogels with increased survivability is still anticipated. In this paper, we present a novel structural color hydrogel with the desired survivability by simply integrating antibacterial nanoparticles into the hydrogel materials, as schemed in Figure 1. Antibacterial nanoparticles, such as silver nanoparticles (AgNPs), have gained great attention because of their wide and excellent antibacterial abilities.25-28 These antibacterial AgNPs are


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utilized frequently in our daily life in water disinfectants,29 wound treatment,30 anti-inflammatory agents,31 sterilization reagents,32 and so on.33-37 However, the potential value of the antibacterial nanoparticles for protecting structural color materials remains unexplored. Thus, we herein synthesized AgNPs in situ within the structural color hydrogels and investigated their effects on materials properties. As the composite materials have the capacity to release antibacterial factors slowly and steadily, the structural color hydrogels could sterilize bacteria adhering on their surface, and thus avoid hydrogel damage and color destruction during their application and storage. It was demonstrated that the AgNPs-tagged poly(N-isopropylacrylamide) (PNIPAM) structural color hydrogels could keep their original thermal-responsive volume change and color transition performances even when the AgNPs-free hydrogels were degraded by bacteria. Also, the integration of AgNPs in self-healing structural color protein hydrogels could save their selfrepairing property instead of being digested in ruins by bacteria. These results indicated many practically biomedical values of the anti-bacteria structural color hydrogels.


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Figure 1. Schematic of the AgNPs-free structural color hydrogel and AgNPs-tagged structural color hydrogel after long time placement. The former would lose the structural color due to bacteria proliferation and destruction, while the latter could keep vivid structural color without bacteria adhesion.

2. EXPERIMENTAL SECTION 2.1. Materials. Monodisperse charged silica nanoparticles with size of 135 nm, non-charged silica nanoparticles with size of 230 and 300 nm were purchased from Nanjing Nanorainbow Biotechnolodgy Co., Ltd. Acrylamide (AAm), N,N’-Methylene-bisacrylamide (BIS), poly(Nisopropylacrylamide)

(PNIPAM),

2-hydroxy-2-methyl-1-phenyl-1-propanone

(HMPP),

phosphate buffer saline (PBS) and FITC Concanavalin A (ConA) were purchased from Sigma Aldrich (St. Louis, MO). Silver nitrate (AgNO3), Trisodium citrate dihydrate, and glycerol were derived from Aladdin (Shanghai, China). Methacrylated gelatin (GelMA) was self-prepared. Gelatin (from porcine skin), Bovine serum albumin (BSA), glucose oxidase (GOX), and catalase (CAT) were acquired from Sigma Aldrich (St. Louis, MO).Water used in all experiments was purified using a Milli-Q Plus 185 water purification system (Millipore, Bedford, MA) with resistivity higher than 18 MΩ•cm. 2.2. Preparation of AgNPs-tagged structural color hydrogels. The pregel solution was prepared firstly. Monodisperse charged silica nanoparticles were purified via centrifugation. Monomer AAm and cross-linker BIS were mixed at a mass ratio of 29:1 to prepare the 10 wt% pre-gel solution (deionized water). Then, the purified colloidal nanoparticles were dispersed in pregel solution, which composed of pre-gel solution (99%, v/v) and HMPP (1%, v/v). An excess


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of ion-exchange resin was added to the pregel solution to complete the ion exchange process. The purpose of adding ion-exchange resin was to purify the charge of the silica nanoparticles solution. After extensive mixing, the color-formed colloidal crystal array solution was extracted into another centrifuge tube to get rid of ion-exchange resin. A mode was prepared with two flat glass slides separated by two bar shape spacer (1 cm in length and 250 µm in diameter). The pregel solution was introduced into the mold, and then exposed to UV light for 30s. After the colloidal crystal array hydrogel solidified, the mold was removed to obtain the structural color hydrogel. In addition, the color of the colloidal crystal hydrogels could be adjusted by using different concentrations of silica nanoparticles. For further thermal-responsive structural color hydrogel experiments, PNIPAM (10%, v/v) was used instead of AAm in pregel solution. A butterfly-patterned mask was covered on the upper glass slide of the mold during UV light exposure to gain the specific pattern. Two methods of AgNPs integration were carried out, the silver staining and reduction in situ. In staining method, silver sol was firstly synthesized according to the literature.38 Briefly, a 50 mL mixture of glycerol (40%, v/v) and deionized water (60%, v/v) was stirred and heated up to 95 °C. Then, 9 mg silver nitrate was added into the solution. After 1 minute, 1 mL 3 wt% sodium citrated solution was added. The above mixture was kept stirring for 1 h at 95 °C. The structural color hydrogels were immersed into the silver sol when its temperature fell back to room temperature for 24 h. In reduction in situ method, AgNO3 solution was prepared for Ag ions infiltration. After immersion in AgNO3 solution, structural color hydrogels were exposed to an UV light for photo-reduction of Ag+. In a typical experiment, 4 groups of the hydrogel were immersed in different concentrations of AgNO3 solution (1 mM, 10 mM, 100 mM, and 1000 mM) for 24 h and experienced a 3 minutes UV radiation, respectively.


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2.3. Antibacterial contrast test between AgNPs-free and AgNPs-tagged structural color hydrogels. Prepared AgNPs-free structural color hydrogel and AgNPs-tagged structural color hydrogel were kept in open petri dishes under a humid environment at about 30 °C. Some water without sterilization was sprinkled termly to avoid hydrogels’ structure destruction by dehydration. The surface feature and structure color changes of both hydrogels were observed and recorded by digital camera. Both hydrogel materials (1 cm × 1 cm) were immersed in ConA (2 µg/mL, dissolved by PBS) for 20 min at room temperature, followed by rinsed twice with PBS buffer. The stained hydrogels materials were observed by a laser scanning confocal microscope. 2.4. Preparation of AgNPs-integrated self-healing structural color hydrogels. The inverse opal scaffold was firstly prepared by a sacrificial templated method. The colloidal crystal templates were obtained by a deposition method at constant temperature. Briefly, silica nanoparticles with sizes of 230 and 300 nm were dispersed in 20 wt% ethyl alcohol, and selfassembled on glass slides (about 0.5 mm in thickness) at 4 °C for 3 hours. Then the glass was calcined at 450 °C for 5 hours to strengthen the colloidal templates. The GelMA pregel solution (0.2 g/mL) was infiltrated into the interstices between silica nanoparticles, and the pregel solution was then solidified by UV radiation (patterned mask in UV light exposure could help fabricate specific-patterned hydrogel). Finally, the whole film was immersed in HF solution (4 wt%) for etching silica nanoparticles to obtain the inverse opal scaffolds. Different structural color were controlled by the sizes of silica nanoparticles. Then the glutaraldehyde (0.5 wt%) cross-linked BSA (12.5 wt%) hydrogel with GOX (0.2 wt%) and CAT (0.8 wt%) was infused into the inverse opal scaffold. The pH value of the mixed solution was adjusted around 7.0. Then, the inverse opal scaffold was dehydrated at 35 °C for 2 hours, and quickly fulfilled by the mixed solution in vacuum for 20 minutes. The structural color hydrogel film was transferred into


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a stable and closed environment at 4 °C for 3 hours for polymerization of the mixed solution in the pores of the inverse opal scaffold. In self-healing protein hydrogel, AgNPs were first mixed into the glutaraldehyde cross-linked BSA hydrogel, and then the hydrogel mixture was infused into GelMA inverse opal scaffolds and formed an AgNPs integrated structure color self-healing hydrogel. 2.5. The construction process of AgNPs-integrated self-healing structural color hydrogels. The self-healing property of AgNPs-integrated self-healing structural color hydrogels was observed by cutting the patterned hydrogels (with two colors) into two segment, which were placed in a high humidity condition for a few days, respectively. Then, two different color segments were brought together, contacted tightly and stimulated with external glucose (0.1 mg) under a closed condition at 4 °C for 3 hours. Finally, the self-healed structural color hydrogel was prepared. As a control, the surface of AgNPs-free self-healing structural color hydrogel was also observed. 2.6. Characterization. SEM images of samples were taken by a scanning electron microscopy (SEM, Hitachi S-3000N). Reflection spectra were measured by an optical spectrometer (Ocean Optics, USB 2000) and a tungsten halogen source (Ocean Optics, LS-1). Microscope optical images of the samples were obtained by a stereoscopic microscope (NOVEL NTB-3A, Ningbo Yongxin Optics Co., Ltd) equipped with a CCD camera (Media Cybernetics Evolution MP5.0). Photographs of samples were taken by a digital camera (Canon EOS 5D Mark II). Fluorescence photographs of cross-section of the helical microfibers were snapped by a Laser Scanning Confocal Microscope (Carl Zeiss, LSM510).


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3. RESULTS AND DISCUSSION 3.1. Preparation of AgNPs-tagged structural color hydrogels. In a typical experiment, the structural color hydrogels were fabricated by polymerizing non-close-packed colloidal crystal arrays. During this process, the monodisperse silica nanoparticles were well dispersed in a pregel solution composed of polymer monomers, cross-linking agents and photoinitiator in a certain ratio. After a strict ion exchange treatment to the pregel solution, ionic impurities were reduced and interparticle repulsion occurred at the average interparticle spacing, making silica nanoparticles self-assembled into ordered non-close-packed colloidal crystal array structures in the solution. The highly ordered nanoparticles imparted the pregel solution with brilliant structure colors which could be adjusted by using different concentrations of silica nanoparticles (Figure S1). Finally, the non-close-packed colloidal crystal films with orderly arranged nanostructure (Figure 2) were fabricated by infusing the nanoparticle suspension into a mold and photo-polymerizing with UV irradiation. From scanning electron microscopy (SEM) characterization, it could be observed that the monodisperse silica nanoparticles formed a predominantly hexagonal symmetry structure (Figure 2a) on the hydrogel surface, and also in the cross-section (Figure 2b), indicating the orderly arranged structure of the whole hydrogel films. As the charged colloidal nanoparticles dispersed in the highly purified nonionic polymerizable monomers solution, significant interparticle repulsion occurs and the minimum energy configuration makes the colloidal nanoparticles self-assemble into non-close-packed colloidal crystal array structure. The array is locked in polymerized hydrogel matrix. Because of the periodic arrangement of the orderly arranged nanoparticles, the hydrogel films were imparted with PBGs property. This structure could prohibit certain wavelengths from propagating and lead


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to their reflection from the films. Thus, the hydrogel films were imparted with specific characteristic reflection peaks and corresponding vivid structural colors. Under normal incidence, the main reflection peak position λ of the structural color hydrogel film could be estimated by Bragg’s equation: λ = 2d111naverage, where d111 is the interplanar distance of the (111) diffracting planes and naverage is the average refractive index of the materials. By using different concentration of silica nanoparticles for the colloidal crystal array, the d111-relevant scaffold could be regulated. Thus, a series of structure color hydrogels with different diffraction peaks and structure colors could be obtained as well.

Figure 2. (a, b) SEM images of structural color hydrogel: silica colloidal crystal array on the surface (a) and in the cross-section (b) of the AgNPs-free hydrogel. (c) Magnified surface of the AgNPs-free hydrogel. (d) Magnified surface of AgNPs-tagged structural color hydrogel.


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Integrated AgNPs were labelled by yellow circles. Due to the resolution ratio of SEM, the AgNPs were synthesized to about 40 nm for the observation. For the antibacterial experiments, 10 nm of AgNPs were employed. The bars are 1 µm in (a, b) and 250 nm in (c, d), respectively. In order to impart the structural color hydrogels with antibacterial function, the achieved films were further integrated with AgNPs. As the scaffold was primarily composed of hydrogel polymers, the films possessed unique loose and porous structure, which was suitable for AgNPs staining or reduction in situ. For the sliver staining procedure, the as-prepared films were dried and immersed into AgNPs solution for the nanoparticles absorption. While in the reduction method, the structural color hydrogels were immersed with silver nitrated solution throughout their cross-linked networks, and were then exposed to an UV light for in situ reduction. Although the staining method was much simpler, the in situ reduction process provided a better way for controlling the size of the AgNPs by employing different concentrations of silver nitrated solution, and intensity and duration of UV radiation. Generally, with the increase of these parameters, the size of the AgNPs increased correspondingly. However, the oversized AgNPs would destroy the ordered nanostructures of the structural color hydrogels. Therefore, an optimized AgNPs size of about 10 nm was applied in the structural color hydrogels for the following antibacterial experiments. Compared to the AgNPs-free structure colors hydrogels (Figure 2c), the AgNPs showed an even distribution in the composite structural color hydrogels (Figure 2d). The energy dispersive X-ray spectroscopy (EDS) analysis was also implemented for confirming the existence evidence of the Ag elements (Figure S2). 3.2. Optical characterization of the AgNPs-tagged structural color hydrogels. The effects of integrated AgNPs on the PBGs shift of the structural color hydrogels were investigated by using different concentrations of silver nitrate solution for the in situ photo-synthesizing. It was


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found that the reflection peak red-shifted when the concentration of silver nitrate solution was increased (Figure 3a). This should be ascribed to the increasing of the effective refractive index of the structural color hydrogels due to the formation of the AgNPs inside the hydrogel networks. The relationship between the change of structural color hydrogel spectra wavelength and the concentration of the silver nitrate solution which structural color hydrogel immersed in was described in a curve (Figure S3). As AgNPs integrated into structural color hydrogel, the naverage was increased and the wavelength was correspondingly increased based on Bragg’s equation. The shift value of the structural color hydrogels was about 30 nm with the formation of 10 nm AgNPs, and each shifted reflection wavelength maintained a good waveform with a narrow half width of the peak. Although with the PBGs shifting, the structural colors of the hydrogel films remained vivid during the nanoparticles growth. This process was also confirmed in different hydrogel systems with various structural colors. The results indicated that the reflection peaks of those hydrogels all red-shifted in a similar shift range during the AgNPs formation (Figure 3b), and these hydrogels could all keep their vivid structural colors.

Figure 3. Reflection spectra of the structural color hydrogels before and after AgNPs composition: (a) the reflection peaks were red-shifted with the increase of AgNO3 and AgNPs


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concentrations; (b) the reflection peaks of three structural color hydrogels were all red-shifted during the AgNPs formation. 3.3. Antibacterial contrast test between AgNPs-free and AgNPs-tagged structural color hydrogels. To investigate the antibacterial performance of the AgNPs-tagged materials, a contrast test was employed to the AgNPs-free structural color hydrogel film and the AgNPstagged structural color hydrogel film, both of which were kept in open petri dishes under a bacteria multiplication environment for 20 days. Due to the biocompatibility of the hydrogel materials, bacteria could adhere and proliferate on the hydrogel films, which degraded the polymer hydrogel network, disorganized the well-arranged silica particles array, and finally destroyed the PBGs or structural colors of the hydrogel films, as shown in Figure 4. It could be observed that both the AgNPs-free and AgNPs-tagged hydrogel films had bright structural color, smooth surface and clear border at the beginning (Figure 4a, d). As time went on, the surface of the AgNPs-free hydrogel films became rough, and their structural colors were fade out gradually (Figure 4a-c). Finally, the AgNPs-free hydrogel films were badly weakened and their colors almost disappeared (Figure 4c). The process of the hydrogel’s bacterial infection was further confirmed by using a laser confocal microscopy to observe the FITC-concanavalin A stained bacteria. It was found that the bacteria not only existed on the surface, but also invaded into inner section of the hydrogel film (Figure S4). In contrast, the AgNPs-tagged structural color hydrogel films could maintain their vivid structural color during long-term experiments (Figure 4d-f). This should be ascribed to the constant release the silver irons from the tagged AgNPs nanoparticles, which prevented the bacteria adhesion and hydrogel destruction. Therefore, a new strategy for the construction of antibacterial structural color materials was developed, which could improve the survivability of the structural color hydrogels.


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Figure 4. (a-c) The destruction process of AgNPs-free structural color hydrogel films during 20 days storage. (d-f) The AgNPs-tagged structural color hydrogel films maintained vivid colors during 20 days storage. The bar is 500 mm. 3.4. Temperature responsive property of AgNPs-tagged PNIPAM structural color hydrogels. The functions of the AgNPs-tagged antibacterial structural color hydrogels after long-time storage were also investigated. To test the sensing performance, temperature responsive PNIPAM structural color hydrogels, which can shrink and swell under different thermal triggers, were constructed and tagged with AgNPs. Generally, the volumes of the PNIPAM hydrogels decrease with the surrounding temperature increasing. This could cause a gradual decrease of the interplanar distance of the (111) diffracting planes (d111), and result in the blue-shift of both the structural color and reflection peaks of the PNIPAM hydrogel both blue shifting. However, due to the adhesion and proliferation of bacteria on the film, the hydrogel system was degraded, which led to the temperature-responsive functional impairment of the materials (Figure S5). But with the presence of AgNPs in the systems, these bacteria-caused


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damages could be avoided. Thus, the improved PNIPAM structural color hydrogels could keep their original properties of thermal-responsive volume change and structural color transition (Figure 5), even though they were exposed in a bacteria-rich environment and deposited for several months. These results indicated that the AgNPs-tagged structural color hydrogel could keep their sensing performance for different long-time applications.

Figure 5. (a-e) The microscope images of AgNPs-tagged PNIPAM structural color hydrogel under different temperatures. From (a) to (e), the temperature of the hydrogel was increased from 25°C to 40°C. (f) Reflection spectra of AgNPs-tagged structural color hydrogel during temperature growth. The bar is 500 mm. 3.5. Self-healing property of AgNPs-integrated structural color protein hydrogels. Besides the sensing ability, the self-healing performance of the AgNPs-tagged antibacterial structural color hydrogels was also investigated. For this purpose, the structural color hydrogels with self-healing ability were prepared by filling a glucose oxidase (GOX) and catalase (CAT) enzymes-added glutaraldehyde cross-linked Bovine serum albumin (BSA) hydrogel into


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methacrylated gelatin (GelMA) inverse opal scaffolds. The BSA hydrogel filler imparted the composite hydrogel materials with self-healing capability through reversible covalent attachment of the glutaraldehyde to lysine residues of BSA and the enzyme additives. Due to high proteins content, such self-healing structural color hydrogels were susceptible to losing their selfrepairing properties and vivid structural colors as a result of bacterial proliferation, which greatly limited their further applications. To overcome this drawback, AgNPs-tagged BSA hydrogel was used for the GelMA inverse opal filler. It was found that the improved protein structural color hydrogels were endowed with unobvious bacteria adhesion during their long-time placement in the environment suitable for bacterial proliferation, as shown in Figure 6. More importantly, the AgNPs-tagged structural color protein hydrogels maintained excellent self-healing capability, with two tightly adhered hydrogels form an integrated one under glucose addition (Figure 6b, 6c and Figure S6).The extended storage and strengthened resistance of these self-healing structural color hydrogels make them superiorly available for different applications.


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Figure 6. (a) AgNPs-tagged self-healing structural color hydrogel after a long-time placement. (b) Optical image of the self-healed AgNPs-tagged structural color hydrogel which could be picked up as an integrated one. (c) Optical images of a butterfly pattern assembled by the AgNPs-tagged self-healing structural color hydrogel. 4. CONCLUSION In conclusion, we have developed an antibacterial structural color hydrogels with superior survivability and improved stability by simply integrating AgNPs into the hydrogel materials. The composite hydrogels have the capacity to release antibacterial silver ions slowly and steadily, and thus the materials could prevent bacteria adhering, avoid hydrogel damage, and maintain their vivid structural colors during storage. Based on this stratagem, we have demonstrated that the AgNPs-tagged PNIPAM structural color hydrogels could keep good thermal-responsive volume change and structural color transition capabilities, and the AgNPsintegrated self-healing structural color protein hydrogels could save their self-repairing property and be assembled into vivid patterns instead of being digested by bacteria. These features of the AgNPs-tagged antibacterial structural color hydrogels indicated their versatile values in different areas. ASSOCIATED CONTENT Supporting Information Different structural colors of non-close-packed colloidal crystal arrays; EDS analysis of AgNPstagged structural color hydrogels; Confocal laser scanning microscope image of AgNPs-free and AgNPs-tagged structural color hydrogels; Reflection spectra of AgNPs-free and AgNPs-tagged


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structural color hydrogels; The destruction process of AgNPs-free PNIPAM structural color hydrogel films. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author (*Yuanjin Zhao) Email: [email protected] Author Contributions §

Z. C. and M. M. contributed equally to this work.

Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This work was supported by the National Science Foundation of China (Grant Nos. 21473029 and 51522302), the NSAF Foundation of China (Grant No.U1530260), the National Science Foundation of Jiangsu (Grant No.BK20140028), the Scientific Research Foundation of Southeast University, and the Scientific Research Foundation of Graduate School of Southeast University (Grant No.YBJJ1671). REFERENCES (1) Zhao, Y. J.; Xie, Z. Y.; Gu, H. C.; Zhu, C.; Gu, Z. Z. Bio-Inspired Variable Structural Color Materials. Chem. Soc. Rev. 2012, 41, 3297-3317. (2) Kim, S. H.; Lee, S. Y.; Yang, S. M.; Yi, G. R. Self-Assembled Colloidal Structures for Photonics. NPG Asia Mater. 2011, 3, 25-33. (3) Shang, L. R.; Gu, Z. Z.; Zhao, Y. J. Structural Color Materials in Evolution. Mater. Today 2016, 19, 420-421.


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Antibacterial Structural Color Hydrogels - ACS Applied Materials

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