Sodium alginate-assisted route to antimicrobial biopolymer film combined with aminoclay for enhanced mechanical behaviors

Industrial Crops & Products 135 (2019) 271–282

Contents lists available at ScienceDirect

Industrial Crops & Products journal homepage: www.elsevier.com/locate/indcrop

Sodium alginate-assisted route to antimicrobial biopolymer film combined with aminoclay for enhanced mechanical behaviors Shicun Jina,b,c, Kuang Lia,b,c, Changlei Xiad, Jianzhang Lia,b,c,

T

⁎

a

Key Laboratory of Wood Materials Science and Utilization (Beijing Forestry University), Ministry of Education, Beijing 100083, China Beijing Key Laboratory of Wood Science and Engineering, Beijing Forestry University, Beijing 100083, China c College of Materials Science and Technology, Beijing Forestry University, Beijing 100083, China d Department of Mechanical and Energy Engineering, University of North Texas, Denton, TX 76203, USA b

A R T I C LE I N FO

A B S T R A C T

Keywords: Sodium alginate Soy protein isolate Aminoclay Silver nanoparticle Antibacterial activity Toughness

Considerable attention has been paid to the utilization of eco-friendly biopolymer-based composites in such areas as bioscience, packaging, and tissue engineering. However, the drawbacks of biopolymers, for instance, low mechanical performance and high water absorption, present obvious challenges. In this study, we fabricated a better-performing bio-film from soy protein isolate (SPI) that was modified by oxidized sodium alginate and silver nanoparticles (OSA@AgNPs). Furthermore, synthetic platelike aminoclay (AC) was introduced to form an interpenetrating polymeric network structure in the matrix of the SPI-based films. The appearance and size distribution of the obtained AgNPs were confirmed by transmission electron microscopy (TEM) and dynamic light scattering (DLS). The results of mechanical tests showed that the tensile strength and toughness of the film were significantly increased by 230.3% (to 10.9 ± 0.4 MPa) and 148.1% (to 12.9 ± 0.3 MJ m−3), respectively, with the introduction of 8 wt% AC into the matrix. The antimicrobial properties of the SPI-based films were determined using the disc diffusion method, the results of which suggested that the films had favorable antibacterial activities against both Escherichia coli and Staphylococcus aureus. Furthermore, the SPI/OSA@AgNPs/ AC films displayed hydrophobic surfaces and dramatically enhanced water resistance. The effort made in this study for solving the drawbacks of SPI-based films might expand their applications.

1. Introduction

incomplete clay exfoliation, and weak clay–matrix adhesion (Bui et al., 2018). A highly dispersible clay that interacts well with the selected substrates is needed. The strategy of synthesizing tailored clays can address the above-mentioned hurdles. Aminoclay (AC) is a 3-aminopropyl functionalized magnesium phyllosilicate [R8Si8Mg6O16(OH)4, where R represents –CH2CH2NH2]. As a plate-like nanoclay, AC has been utilized in the applications of ion exchange, catalysis, and drug delivery (Liu et al., 2018). Moreover, the organic moieties in the clay provide greater flexibility for other inorganic fillers, thus improving the plasticity of the composite (Achari et al., 2013; Zheng et al., 2014). The unique properties of AC provide the possibility of constructing a crosslinked network composed of biopolymer and inorganic clay layers to achieve a stronger biopolymer–clay nanocomposite. In addition, the antibacterial properties of SPI-based films need to be improved to reduce the possibility of bacterial infections with the films and expand their applications. Silver nanoparticles (AgNPs) have been an important component in various antimicrobial products because of their effective antimicrobial activity towards multiple targets

The use of biopolymer-based composites as alternatives to petroleum feedstock and packaging plastics has risen exponentially (Echeverría et al., 2014). Among them, the plant-derived soy protein isolate (SPI) has been successfully developed for use in food packaging, adhesives and composites owing to its low cost, biodegradability, nontoxicity, and renewability (Li et al., 2016; Wang and Wang, 2017). However, soy protein-based composites typically exhibit inferior mechanical properties, poor water resistance, and no antibacterial property because of their natural attributes (Zhang and Zhang, 2013). To use soy protein-based films, it is a challenging but necessary work to solve these concerns. Previous studies proved that the exfoliation and dispersion of clay materials such as Montmorillonite (MMT) or saponite in a protein matrix could improve the mechanical properties of composites (Echeverría et al., 2014; Perez-Puyana et al., 2018). However, those studies often encountered several crucial issues such as poor miscibility,

⁎

Corresponding author at: Key Laboratory of Wood Materials Science and Utilization (Beijing Forestry University), Ministry of Education, Beijing 100083, China. E-mail address: [email protected] (J. Li).

https://doi.org/10.1016/j.indcrop.2019.04.052 Received 11 November 2018; Received in revised form 23 April 2019; Accepted 24 April 2019 Available online 02 May 2019 0926-6690/ © 2019 Elsevier B.V. All rights reserved.

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

2.4. Synthesis of aminoclay (AC)

(e.g. bacteria, fungi and viruses) (Lin et al., 2018). AgNPs were typically formed by reduction reactions that involved expensive chemicals such as dopamine. Furthermore, toxic reducing agents such as NaBH4 could adversely affect the environment and ecosystem (Ravula et al., 2015). Alternatively, sodium alginate, a linear natural polysaccharide derived from brown seaweed that has low toxicity, low cost, and good tissue compatibility, is tried to serve as a reducing agent (Wei et al., 2015). In addition, it can be oxidized by sodium periodate to reduce its viscosity and improve biodegradability, making it more suitable for use in biopolymer-based systems. Multiple functional aldehyde groups formed on the oxidized sodium alginate (OSA) are reducing agents and promote covalent cross-linking with the amino groups of protein or polypeptides (Ding et al., 2017a). This study aimed to prepare AgNPs using a green process and develop an SPI-based composite film with better mechanical properties, improved water resistance, and favorable antibacterial activity. To achieve these objectives, AgNPs were reduced from a silver salt solution using OSA. Then, the obtained OSA@AgNPs (OA) was in situ crosslinked with the SPI and ultrasonically exfoliated AC to prepare a betterperforming SPI-based composite film. The effects of OA and AC on the thermo-mechanical properties, water resistance and microstructure of the SPI-based films were investigated. The antibacterial properties of the films were also evaluated. To our knowledge, the prepared SPIbased films with simultaneous enhancement of mechanical, antibacterial, and water resistance properties have been rarely reported. It is well-accepted that protein and other biopolymers belong to promising green materials with tailored characteristics.

MgCl2·6H2O (7.24 mM) was added into 40 mL of anhydrous ethanol and the mixture was stirred until the MgCl2·6H2O was completely dissolved. Then 11.7 mM of APTES was added dropwise into the above MgCl2 ethanol solution, upon which the formation of a white gel like material was observed immediately. After stirring for 24 h at 25 °C, the white precipitate was collected and purified with anhydrous ethanol via centrifugation (8000 rpm, 15 min) for three times. The resultant AC was dried in a vacuum oven for 12 h at 40 °C, and then pulverized into a fine powder using a vertical planetary ball mill (XQM-0.4, Changsha, China) at 870 rpm. Finally, the AC was dispersed in 10 mL of deionized water, and the obtained AC dispersions were magnetically stirred for 10 min and sonicated in an ultrasonic cleaner (KQ-300DE, Kunshan, China) operating at 40 kHz and 270 W for 2 min (nanoparticle exfoliation) for later use. 2.5. Preparation of SPI-based composite films To prepare the SPI, 5 g of SPI and 2.5 g of glycerol were dissolved in 70 mL of deionized water and the mixture was magnetically stirred at 800 rpm for 30 min. Then, NaOH solution (10%, w/w) was added dropwise into the above solution to adjust the pH to approximately 9.0, the temperature was increased to 85 °C, and the solution was stirred for another 30 min to obtain a pristine SPI solution. To prepare the SPI/OA, the OA solution was added to the prepared SPI solution and the resulting solution was stirred at 40 °C for 3 h. SPI/OA/AC was produced by adding the OA solution and 10 mL of AC dispersion (5, 8, 11, and 14 wt% based on SPI content) into the prepared SPI solution and stirring the mixture at 40 °C for 3 h. Finally, the above SPI-based solutions were placed in an ultrasonic cleaner (KQ-300DE, Kunshan, China) operating at 40 kHz and 270 W for 20 min to form a homogeneous system. The degassed mixture was poured into a Teflon-coated mold and vacuum-dried at 45 °C for 20 h. The samples were stripped and then stored in a desiccator (50% relative humidity, 25 °C) before testing.

2. Experimental section 2.1. Materials SPI (95% protein) as a biopolymer was supplied by Yuwang Ecological Food Industry Co., Ltd. (Shandong, China). SPI contains a maximum of 0.8% fat and 3% ash, and its isoelectric point is 4.6. Sodium periodate, sodium alginate (20–40 kDa), silver nitrate (AgNO3) (99.9% purity), 3-aminopropyltriethoxysilane (APTES), magnesium chloride hexahydrate (MgCl2·6H2O), and glycerol (99% purity) were received from Beijing Chemical Reagents Co., Ltd. (Beijing, China). All other reagents were analytical grade and used as received.

2.6. Characterization 2.6.1. Transmission electron microscopy (TEM) TEM images were obtained using a JEM-2100 F (JEOL, Tokyo, Japan) at 200 kV. The specimen solution was deposited on a carboncoated copper grid that was then dried at 25 °C before testing. 2.6.2. Dynamic light scattering (DLS) The Z-average hydrodynamic diameter and polydispersity index of the AgNPs were obtained using DLS measurement. Experiments were performed using a Zetasizer Nano ZS90 (Malvern Panalytical, Malvern, UK). The results were recorded in triplicate at 25 °C.

2.2. Preparation of oxidized sodium alginate (OSA) OSA was prepared using a sodium periodate oxidizing method (Sarker et al., 2014). Briefly, sodium alginate (10.0 g) was added into 650 mL of deionized water, and the mixture was mechanically stirred (400 rpm) at 25 °C for 2 h. Then, 50 mL of sodium periodate (0.93 mol/ L) was added dropwise into the above mixture and stirred for another 24 h in the dark at 25 °C. Finally, the reaction was terminated by adding 3.5 mL of ethylene glycol and continuously stirring the mixture for another 30 min. The product was dialyzed (Mw = 14,000) against deionized water for 3 days, and then freeze-dried. The degree of oxidation OSA was determined to be 69.7% according to a previous method that used hydroxylamine hydrochloride/sodium hydroxide (Balakrishnan et al., 2014).

2.6.3. Opacity analysis Ultraviolet–visible (UV–vis) absorption spectra were recorded using a TU-1901 spectrophotometer (Purkinje General Company, Beijing, China). A drop of test specimen (3 μL) was dispersed into 4 mL of deionized water, and quartz cuvettes were used for all measurements. The scanning range was 200–800 nm. 2.6.4. Fourier transform infrared (FTIR) spectroscopy FTIR spectra were acquired via attenuated total reflectance using a Nicolet 6700 spectrometer (Thermo Fisher Scientific, Waltham, MA, USA). The test specimens were analyzed over the range of 650–4000 cm−1 with 32 scans.

2.3. Preparation of OSA@AgNPs (OA) OSA (0.5 g) was dissolved in 10 mL of deionized water and the mixture was stirred vigorously at 1000 rpm for 15 min. Subsequently, 5 mL of 0.07 mol/L aqueous AgNO3 solution was introduced and the obtained OA mixture was magnetically stirred for 2 h at 25 °C in the dark.

2.6.5. X-ray diffraction (XRD) XRD was performed using a D8 Advance X-ray diffraction analyzer (Bruker AXS, Karlsruhe, Germany) equipped with a Cu Ka radiation source (λ = 0.154 nm). The test specimens were scanned from 5° to 80° 272

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 1. (a) Schematic illustration of the reaction process of oxidized sodium alginate (OSA). (b) Fourier transform infrared (FTIR) spectra and (c) 1H nuclear magnetic resonance (1H NMR) spectra of the original sodium alginate and OSA.

at a rate of 2° min−1.

using a universal mechanical tester (INSTRON 3365, Norwood, MA, USA) equipped with a 100-N load cell at a constant stretching rate of 20 mm min−1. The static tensile tests, including elongation at break (EB) and tensile strength (TS), were performed on rectangular specimens (80 mm × 10 mm). Six specimens for each group were measured to obtain the standard deviation. Toughness (W) was evaluated based on the integral area under the stress-strain curve. Dynamic mechanical analysis (DMA) of the SPI-based films was carried out using a DMA Q800 (TA Instruments) in tension mode with a fixed frequency of 1 Hz and a temperature range from 30 to 170 °C (heating rate = 5 °C min−1). The test specimens were tailored into a 50mm × 6-mm rectangle. Storage moduli (E′), loss moduli (E″), and loss factor (tan δ = E″/E′) as functions of temperature were recorded.

2.6.6. 1H nuclear magnetic resonance (1H NMR) For 1H NMR analysis, sodium alginate or OSA was dissolved in D2O, and liquid-state 1H NMR spectra were acquired on a 400 MHz Avance Ⅲ spectrometer (Bruker, Rheinstetten, Germany) at an acquisition time of 3.0 s. 2.6.7. Scanning electron microscopy (SEM) The cross section of the SPI-based films was observed using SEM (SU8010, Hitachi High-Technology Corp., Tokyo, Japan) operating at an accelerating voltage of 10 kV. The specimens were studied after measuring their tensile strength. The surface of the specimens was sputtered with a layer of gold before measurement.

2.6.11. Antibacterial assessment S. aureus and E. coli were utilized to evaluate the antibacterial activity of the pristine and modified SPI films via disc diffusion. Briefly, the bacterial dispersion was diluted to a concentration of 108 colonyforming units (CFU)/mL, pipetted onto a Luria-Bertani (LB) medium solid agar plate, and spread to coat the plate uniformly. The 6-mmdiameter film specimens were sterilized via an ultraviolet radiation lamp for 2 h and put onto the E. coli-cultured agar or S. aureus-cultured agar plates. The pristine SPI film was used as a control. After incubation at 37 °C for 24 h, the diameters of the bacterial inhibition zones were measured with a Vernier caliper. Each film group had three replicates.

2.6.8. Thermogravimetric analysis (TGA) TGA of the films was performed using a TGA Q50 analyzer (TA Instruments, New Castle, DE, USA) to evaluate their thermal stability under a nitrogen atmosphere (50 mL/min). Approximately 8 mg of specimen was weighed and scanned from 50 to 600 °C at 10 °C min−1. 2.6.9. Water resistance The water resistance of the protein-based composite films was investigated by measuring the water contact angle (WCA), moisture content (MC), total soluble matter (TSM) and water uptake (WU). The tests were conducted according to the method reported in our previous work (Jin et al., 2018a,b).

2.7. Statistical analysis All assays were conducted on at least three replicates and the results were recorded as mean ± standard deviation (SD). IBM Statistics SPSS

2.6.10. Mechanical tests Tensile mechanical tests of the SPI-based films were performed 273

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

After the incorporation of OA, the characteristic peaks of OSA at 32.4° and 46.5° were seen in the XRD patterns of the SPI/OA composite films. The peak at 77.4° assigned to the (311) lattice plane of Ag was also observed (Liu et al., 2018). The crystalline peak (α-helix) at 2θ = 9.8° was not observed in the pattern for the SPI/OA film. This may be the result of the interaction between OA and SPI causing a change in SPI molecular conformation (Chaturbedy et al., 2010). When the AC was added to the SPI/OA matrix, the interlayer reflection (001) peak of AC at 6.3° disappeared in the XRD patterns of the SPI/OA/AC composite films, signifying the extensive exfoliation of AC within the polymer network (Chen and Wong, 2014). In particular, the emergence of a weak peak (001) for the SPI/OA/AC-11 and SPI/OA/AC-14 films indicated that there was a very small amount of intercalated layered silicate in addition to the exfoliated form (Li et al., 2017a). The interactions between AC, OA, and SPI were examined via FTIR spectroscopy in the range of 3700–750 cm−1 (Fig. 3c). The spectrum of pristine SPI film displayed characteristic bands at 1631 cm−1 (C]O stretching of amide I), 1538 cm−1 (NeH bending of amide II) and 1237 cm−1 (CeH and NeH stretching of amide III) (Wang and Wang, 2017). The OeH bending band at 3272 cm−1, CeH stretching band at 2931 cm−1, and CeO stretching band at 1040 cm−1 were also present (González et al., 2011). The introduction of OA into the SPI caused a new band at 1734 cm−1, corresponding to the C]O vibration of the aldehyde groups on OSA, to appear in the spectrum of the SPI/OA film, and the band of amide I (C]O groups) at 1631 cm−1 shifted to 1634 cm−1. Moreover, the absorption band intensity of eNH2 at 1452 cm−1 decreased and the signal at 1237 cm−1 (NeH bending vibration) disappeared, demonstrating the formation of Schiff base bonds between OSA and protein (Ding et al., 2017a). With the incorporation of AC into SPI/OA, the absorption band of the C]O groups on OSA at 1734 cm−1 and the band of eNH2 derived from AC at 1611 cm−1 disappeared in the spectrum of SPI/OA/AC. However, a new absorption band at 1639 cm−1 associated with the imine stretching vibration (C] N) was observed. These changes may be due to the cross-linking reaction between the OSA polymer and AC molecules (Huang et al., 2015; Wei et al., 2015). In addition, the absorption bands at 3272 cm−1 (eOH bending vibration) and 2931 cm−1 (CeH stretching) in the SPI spectrum shifted to 3270 and 2935 cm−1, suggesting hydrogen bonding interactions between OSA and AC and the SPI matrix (Phua et al., 2013). The above changes were indicative of the multiple interactions between the OSA, AC, and protein polymer. UV–vis spectra were employed to further investigate the interactions between reactants. Fig. 3d showed the absorbance peak of OA solution at 418 nm. After mixing OA with AC, there was a new peak at 254 nm in the spectrum of OA/AC, indicating an interaction between OSA and AC molecules (Shao et al., 2018). The characteristic peak of SPI at 267 nm shifted to 262 nm when SPI was mixed with OA solution. The UV–vis spectrum of SPI/OA displayed higher absorbance, implying the presence of imine bonds between OSA and SPI chains (Sun et al., 2014). Furthermore, the introduction of AC into the SPI/OA system caused the absorbance peak of SPI/OA/AC to shift to 272 nm due to the interactions of AC with OA and SPI (Park et al., 2018).

21.0 statistical software (IBM, Armonk, NY, USA) was used for the analysis of variance (ANOVA) of the data. Tukey’s test was utilized to determine the differences of the mean values (p < 0.05). 3. Results and discussion 3.1. Analysis of OSA and OA The reaction process of OSA is shown in Fig. 1a. During oxidation, eOH groups on the repetitive units of sodium alginate were oxidized by sodium periodate, leading to the formation of aldehyde groups by cleaving the carbon–carbon bond (Wei et al., 2015). The resultant OSA was characterized by FTIR and 1H-NMR spectra. The FTIR spectra of sodium alginate and OSA are shown in Fig. 1b. The sodium alginate spectrum displayed the characteristic absorption bands of a polysaccharide structure at 1317, 1128, 1042, and 947 cm−1, which corresponded to the stretching vibration of CeO, CeC, CeO and CeOeC, respectively. The absorption bands at 1634 and 1426 cm−1 were related to the asymmetric and symmetric stretching vibration of carboxylate groups on alginate (Liu et al., 2017). The band corresponding to the C]O vibration of the aldehyde group at 1734 cm−1 was almost imperceptible in the FTIR spectrum of OSA, indicating a very low efficiency in the oxidation reaction, which was confirmed by 1H NMR. The 1H NMR spectrum of OSA (Fig. 1c) exhibited two peaks at 5.28 and 5.60 ppm, which were assigned to the hemiacetal groups from the aldehyde and adjacent hydroxyl groups, respectively (Ding et al., 2017a). Compared to the sodium alginate spectrum, there was a new signal in the OSA spectrum at 8.35 ppm, attributed to the aldehyde groups (Wei et al., 2018), which indicated that the OSA was formed successfully. Fig. 2a displays the representative TEM images of AgNPs in OSA solution and Fig. 2b shows the corresponding histograms of their sizes. The prepared AgNPs were sphere-like with diameters ranging from 8.9–22.0 nm (mean diameter = 13.7 ± 3.1 nm). Furthermore, DLS was employed to analyze the prepared AgNPs. Their size distribution is shown in Fig. 2d, where the Z-average hydrodynamic diameter of the AgNPs was shown to be 65.4 ± 2.6 nm. The average size of the AgNPs measured using DLS was larger than that found by TEM. This phenomenon occurred because DLS detected OSA layers adsorbed onto the surface of the AgNPs, which affected the accuracy of the particle size measurement. This result was consistent with those of previous reports (Scherer et al., 2019; Latha et al., 2019). Usually, particles are believed to be highly monodisperse when the polydispersity index (PDI) ≤ 0.1, moderately monodisperse when PDI = 0.1–0.7, and polydisperse when PDI > 0.7 (Scherer et al., 2019; Akaighe et al., 2011). Thus, the prepared AgNPs were highly monodisperse with a PDI of 0.084. Fig. 2c showed that the color of prepared OA solution turned to amber because of the formation of the AgNPs (Wu et al., 2018). The UV–vis spectra of OSA and OA are shown in Fig. 2e. Compared with the OSA spectrum, the OA spectrum had a new characteristic band at 418 nm, confirming the successful preparation of the AgNPs (Qi et al., 2018). 3.2. Structural analysis of materials by XRD, FTIR and UV–vis spectra

3.3. Water resistance and wettability The XRD patterns of AC, pristine SPI, SPI/OA and SPI/OA/AC composite films are shown in Fig. 3a. The basal peak at 6.3° (001) was attributed to the bilayer arrangement of propylamine groups in the AC. The broad in-plane diffraction peaks at 22.5° (020, 110) and 34.9° (130, 200) were associated with the stacking of the AC nanosheets (Bui et al., 2018). The intralayer reflection peak at about 2θ = 59.5°, corresponding to the 2:1 trioctahedral Mg-phyllosilicate clay, was relatively weak due to the staking disorder induced by the organic functional groups (Khan and Kumaraswamy, 2018). The XRD pattern for the pristine SPI film had two basal crystalline peaks at 2θ = 9.8° and 20.1°, which were related to the α-helix and β-sheet structures of the secondary conformation of the protein, respectively (Li et al., 2017b).

The water resistance and wettability of the SPI-based composite films were assessed by MC, WU, TSM, and WCA measurements. As shown in Fig. 4b, the modification of SPI with OA resulted in the SPI/ OA film having lower WU than pristine SPI film. This was mainly due to the interaction between the aldehyde groups of OSA and the amino groups of protein (Jiang et al., 2018). In addition, the WU of SPI films significantly decreased upon the introduction of AC and was the lowest (26.0 ± 1.8%, a 65.2% decrease compared to the control) with an AC loading of 8 wt% in the dynamic moisture uptake test. Specifically, the aldehyde groups in OSA were considered to cross-link with the AC and protein chains to form a dense network, thereby preventing the protein 274

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 2. (a) Transmission electron microscopy (TEM) images of silver nanoparticles (AgNPs) dispersed in oxidized sodium alginate (OSA) solution. (b) Corresponding histograms of the sizes of the AgNPs. (c) Photo of OSA@AgNPs (OA) solution. (d) Distribution of AgNPs diameters determined by dynamic light scattering (DLS). (e) Ultraviolet–visible (UV–vis) spectra of OSA and OA solutions.

with that of the control (Fig. 4c). The surface wettability results for the SPI-based composite films are shown in Fig. 4d. Compared to the WCA value (55.7° ± 1.7°) of neat SPI film, that of the SPI-based film was significantly higher (103.3° ± 2.0°) after the introduction of OA and AC (Pan et al., 2014). The improved surface hydrophobicity of the SPI/OA/AC-8 film can be explained as follows: 1) The multiple bonding interface induced the rearrangement of SPI chains, which dramatically reduced the amount of hydrophilic groups and exposed some hydrophobic amino acids on the film surface (Yu et al., 2018). 2) The formation of intermolecular hydrogen bonds between the amino groups of the SPI chains and the hydroxyl groups of OSA contributed to a decrease in the ability to build a connection with water molecules (Jiang et al., 2018). 3) The unique and compact

matrix from swelling in a humid environment and improving the water resistance of the SPI film (Cao et al., 2017; Ciannamea et al., 2018). This obvious decrease in water absorption by the modified biopolymer film because of the formation of a physical and chemical cross-linking network was also reported by Wang et al. (2017). On the other hand, an increase in AC content from 8 to 11 wt% increased the WU value relative to that of SPI/OA/AC-8 film. This increase was ascribed to an increase in the number of hydrophilic amino groups from AC molecules (Jin et al., 2018a,b). In addition, excessive AC content in the system resulted in decreased stability of the protein network, which enhanced the permeation and binding capacity of water molecules, thereby reducing the water resistance of the film (Yu et al., 2018). There were no significant changes in the TSM values of the SPI/OA/AC films compared 275

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 3. (a) X-ray diffraction (XRD) patterns of aminoclay (AC) and films. (b) Atomic structure of AC. (c) Fourier transform infrared (FTIR) spectra of AC and films. (d) Ultraviolet–visible (UV–vis) spectra of solutions with different components.

et al., 2018). In addition, the favorable dispersion and interfacial combination of AgNPs in the protein matrix, with the assistance of OSA, played an important role in the effective energy dissipation and mechanical reinforcement of the SPI-based film (Akaighe et al., 2011). After integrating AC into the SPI/OA film, the mechanical properties of the SPI-based films were significantly improved and could be tailored by controlling the AC content. When the AC content was below 8 wt%, the network structure was relatively loose because of insufficient crosslinking and hydrogen bonding interactions between OA, AC, and SPI. As a result, the mechanical properties of the SPI/OA/AC-5 film were not greatly improved (Li et al., 2019). However, when the AC content was more than 8 wt%, the TS and W values of the SPI/OA/AC films decreased. One reason for this could be that the agglomeration effect of the AC sheets caused the formation of an unstable polymer network in the system, hindering stress transfer and energy dissipation under stress loading (Zhang et al., 2016). Notably, the SPI/OA/AC-8 film exhibited the highest TS of 10.9 ± 0.4 MPa and maximum W of 12.9 ± 0.3 MJ m−3, counting the increases of 230.3% and 148.1%, respectively, with respect to the values of the neat SPI film. The improved mechanical properties of the SPI/OA/AC-8 film were ascribed to its unique and compact network structure resulting from the enormous chain entanglement of SPI, OSA, and AC via sufficient cross-linking and hydrogen bonding interactions (Fig. 6d), thereby achieving the efficient transfer of load (Shirdast et al., 2016). In addition, the organic aminosilane between the inorganic platelets in the AC molecule could

network structure formed by OSA, AgNPs and AC in the SPI matrix gave rise to a decrease in the surface free energy of the SPI film (Li et al., 2019). However, an increase in the content of AC from 8 to 14 wt% decreased the WCA value of the SPI/OA/AC film. This was ascribed to the introduction of excess hydrophilic amino groups from AC molecular chains, which promoted the formation of hydrogen bonds with water molecules when water droplets were on the surface of the film (Lee et al., 2011). 3.4. Mechanical properties of SPI-based films The macro-mechanical properties of the SPI composite films were investigated at room temperature, and the results are shown in Fig. 5. The tensile strength (TS), elongation-at-break (EB), and toughness (W) of the neat SPI film were 3.3 ± 0.3 MPa, 192.2 ± 7.3%, and 5.2 ± 0.6 MJ m−3, respectively. The low TS and W values of the neat SPI film were mainly associated with the weak interfacial adhesion of the protein matrix (Li et al., 2017). However, the mechanical behavior of the SPI/OA film was enhanced because of the reinforcement effect of the AgNPs and the interaction between OSA and SPI (Yan et al., 2017). The aldehyde groups of OSA cross-linked with the amino groups of the protein via Schiff base reactions, and hydrogen bonding interactions occurred between the hydroxyl groups of OSA and the amino groups of SPI. Thus, the backbone chains of OSA were intrinsically assembled into the SPI matrix and an integrated polymer network was formed (Wei 276

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 4. (a) Moisture content, (b) water uptake as a function of time, (c) total soluble matter, and (d) water contact angle of soy protein isolate (SPI)-based composite films.

AC layers (Chaturbedy et al., 2010). In general, tan δ is assumed to be a measure of damping characteristics and is used to evaluate the energy dissipated by internal friction. A higher damping capacity indicates more intense internal friction. The peaks in the tan δ curves (Fig. 6b) were attributed to the glass transition temperatures (Tg) of the SPIbased composites (Pei et al., 2011). Compared with that of the neat SPI film, Tg of the SPI/OA/AC-14 film significantly increased from 76.2–92.1 °C. This phenomenon was attributed to the strong interfacial interaction between the OSA, AC, and SPI that enhanced the internal friction and reduced the number of mobile SPI chains, resulting in a higher Tg (Balakrishnan et al., 2014). In effect, OSA served as a crosslinker reacting with SPI and the tailored AC, thus forming multiple interaction networks in the SPI/OA/AC composite film. This played a vital role in toughening the protein segments upon stress loading (Tian et al., 2013). SEM images were obtained to observe the fracture morphology of SPI-based composite films with different formulations (Fig. 7). The fracture surface of the pristine SPI film displayed some cracks and holes that were easily penetrated by water, destroying the weak interactions of the SPI molecular chains and thus reducing the water resistance and mechanical performance of the film (Pan et al., 2014). The surface of the SPI/OA film was relatively compact owing to the interaction between OSA and SPI (Tian et al., 2013). After the introduction of AC into the SPI/OA film, the cross-sectional structure of the film became continuous and homogeneous. This effect was more pronounced for the SPI/OA/AC-8 film, which had a denser and smoother fracture surface than did SPI/OA/AC-5. When the AC content was below 8 wt%, the hydrogen bonding and cross-linking interactions between SPI, OSA, and AC were insufficient (Chen et al., 2018). As a result, the fracture surface

arrest crack propagation in the SPI films by dissipating the energy within the AC organic layers, thereby improving the toughness of the SPI films (Bui et al., 2018; Martelli-Tosi et al., 2018). SPI-based films exhibit poor mechanical properties and numerous strategies have been employed to improve their performance. Fig. 5c shows a comparison of TS and EB values for the resultant SPI/OA/AC films of this work. Perceptibly, the SPI/OA/AC films exhibited integrated strength and superior ductility. The strength of the SPI/OA/AC films was superior to that of other SPI-based composite films such as SPI/lauric acid/polysaccharide (Pan et al., 2014), SPI/hydroxyethyl cellulose (Zhao et al., 2016), SPI/Yucca schidigera/coconut oil (Carpiné et al., 2016), SPI/cellulose nanocrystals/pine needle (Yu et al., 2018), and SPI/caffeic acid film (Kang et al., 2016). The mechanical behavior of the SPI-based composite films in a broad temperature range was determined via DMA. The temperature dependence of E′ and tan δ for the SPI-based composite films is shown in Fig. 6. E' was measured to investigate the stiffness of the SPI-based films, which was affected primarily by polymer chain mobility in the composite (Chen et al., 2017). The neat SPI film had a higher E′ value than the modified SPI films at an initial temperature below 70 °C. At temperatures above 70 °C, the E′ values of the SPI/OA/AC composite films were slightly higher than that of the control film. This phenomenon was probably due to the kinetic effect of the slow relaxation of the polymer chains around the particles (Carpiné et al., 2016). Moreover, the multiple interfacial cross-linking networks in the SPI/OA/AC composite films increased the percentage of hard domains in the SPI matrix and confined the movement of the molecular chains at high temperature (Shirdast et al., 2016). In particular, the SPI/OA/AC-14 composite film had the highest E′ value, probably because of the excess 277

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 5. (a) Representative stress-strain curves of soy protein isolate (SPI)-based composite films. (b) Tensile strength and toughness of SPI-based composite films. (c) Comparison of mechanical properties of the SPI-based composite films with other SPI composites. (d) Interactions in the SPI matrix.

2018a,b).

of SPI/OA/AC-5 was more uneven than that of SPI/OA/AC-8. This phenomenon signified that the construction of multiple cross-linked networks between AC, OSA, and SPI via sufficient hydrogen bonding and other cross-linking interactions in the SPI/OA/AC-8 film system promoted the formation of a compact fracture surface. This prevented water penetration and improved the mechanical properties of the SPI film, in accordance with the results of mechanical tests and water absorption analysis. However, when the AC content was more than 8 wt%, a rough surface and particle precipitation were observed in the crosssectional SEM images of the SPI/OA/AC composite films (Fig. 7e and f). These may be due to the aggregation of AC in the protein matrix leading to a decrease in the stability of the cross-linked network (Jin et al.,

3.5. Evaluation of antimicrobial behavior The antimicrobial activities of the pristine SPI and SPI-based composite films against E. coli and S. aureus were evaluated using a disc diffusion method, and the results are shown in Fig. 8. The pristine SPI films did not display any detectable inhibition zones. However, the SPI/ OA composite films had a significant effect in lessening the growth of E. coli and S. aureus, with the diameters of 14.3 ± 0.5 and 10.8 ± 0.6 mm, respectively. The AgNPs were responsible for the antimicrobial activity because the free radicals generated by them led to 278

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 6. (a) Storage modulus (E′) and (b) tan δ of soy protein isolate (SPI)-based composite films.

et al., 2015). When the AC content was 11 wt% or higher, the local concentration of AgNPs around the bacterial cells may be reduced to some extent (Fu et al., 2015). Therefore, an increase in AC content in the SPI-based composite films had a minor effect on lessening bacterial growth compared to the effect of SPI/OA/AC-8 film. For S. aureus, the diameters of the bacterial lessening zones of the SPI/OA/AC films varied from 10.9–16.9 mm. The above results showed that the SPIbased films had a stronger antibacterial effect on E. coli than S. aureus, probably because the cellular wall of S. aureus possesses a thicker peptidoglycan layer than E. coli. The layer forms a rigid resistance that decreases the amount of Ag+ entering the cell interior (Shuai et al., 2018).

the structural change and degradation of bacterial cell membranes (Wu et al., 2016). The accumulation of AgNPs on the cytomembrane of bacteria has been shown to increase membrane permeability. The AgNPs attached to bacteria released Ag+ and produced many reactive oxygen species (ROS). The former was produced mainly by the oxidization of Ag in the case of oxygen and water, and the latter was obtained via the reaction of electrons and water molecules (Li et al., 2019). Highly reactive Ag+ and ROS can damage bacterial cell structures, effectively inactivating the bacterial protein, and eventually killing the bacterial cells (Shuai et al., 2018). Compared to the SPI/OA film, the SPI/OA/AC composite films decreased the growth of E. coli more effectively, with diameters ranging from 14.9 to 17.1 mm depending on the amount of AC loading, indicative of the enhanced antibacterial activity of the films. A similar phenomenon was also observed on S. aureus. The diameters significantly increased when the AC content increased from 5 to 8 wt%. As the AC content increased from 8 to 14 wt%, the corresponding diameter change remained stable. The SPI/OA/AC composite film had increased antibacterial activity because the electrostatic force of the protonated groups (R-NH2) on the AC lamella drove the antimicrobial effect (Bui et al., 2018). In addition, the functional groups of AC may interact with the cytomembrane components of bacteria (i.e., proteins and lipids) via electrostatic interaction and hydrogen bonding interaction. These interactions could enable AC to be easily adsorbed onto the bacterial cells, hence wrapping and capturing them. Furthermore, the plate-like sharp edges of AC nanosheets could penetrate the cell membrane and damage them (Ravula

3.6. Thermal performance Fig. 9 shows the TGA thermograms of AC and the SPI-based composite films from 50 to 600 °C and Table 1 presents a summary of the degradation data. Pristine SPI film had two main degradation steps in the temperature ranges of 130–250 °C and 250–500 °C, which were ascribed to glycerol evaporation and a thermal breakdown of the SPI molecular skeleton (Kang et al., 2016). The incorporation of OA into the SPI film increased the residual mass of the SPI film at 600 °C from 18.9 ± 0.9–26.4 ± 0.5 wt%. The increase was due to the presence of Ag and the interaction between OSA and peptide chains (Chen and Wong, 2014). The introduction of AgNPs into the SPI-based composite film may provide an additional barrier to the mass transfer of volatile

Fig. 7. Cross-sectional scanning electron microscope (SEM) images of soy protein isolate (SPI)-based composite films (2000 × magnification). 279

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Fig. 8. (a) Antimicrobial zones formed around the soy protein isolate (SPI)-based films; (b) Diameters of bacterial lessening zones against E. coli and S. aureus.

products generated during thermal decomposition (Sarker et al., 2014). Moreover, the hydrogen or amide bonds formed by the SPI and OSA could add more thermal interfacial resistance to the SPI-based film, improving its thermal performance (Balakrishnan et al., 2014). AC had an obvious decomposition peak around 393.2 °C and its residual mass reached 59.8 ± 0.6 wt%. The excellent thermal behavior of AC was related to its Mg phyllosilicate network (Datta et al., 2013). Compared to the temperatures of the maximum degradation rate (Tmax1) of pristine SPI and SPI/OA films, those of the SPI/OA/AC films were higher (above 250 °C), and their residual mass perceptibly increased, indicative of obvious improvement in the thermal behavior of the film. In particular, the SPI/OA/AC film with 8 wt% AC loading had the highest mass fraction value of 36.0 ± 0.5 wt%, which was 15.8% greater than that of the SPI/OA/AC-5 film. This result was due to the introduction of AC with excellent thermal stability and the formation of a denser polymer network via sufficient cross-linking and hydrogen bonding interactions between protein chains, OA, and AC molecules (Ding et al., 2017b). Increasing the AC content from 8 to 14 wt% caused a slight decrease in the residual mass of SPI-based films, possibly because of the reduced stability of the cross-linked structure (Liu et al., 2018). These results signified that the proper AC loading could facilitate the formation of an interconnected network in the system that would hinder oxygen transport and create a dense barrier against gas diffusion, leading to enhanced thermal behavior of the film (González et al., 2011).

Table 1 Thermal characteristics of the DTG curves in Fig. 9b. Samples

Tmax1 (°C)

Tmax2 (°C)

Residual mass (wt%) at 600 °C

SPI SPI/OA AC SPI/OA/AC-5 SPI/OA/AC-8 SPI/OA/AC-11 SPI/OA/AC-14

241.2 224.5 – 260.6 268.7 270.7 274.0

308.2 300.8 393.2 304.1 298.8 298.1 –

18.9 26.4 59.8 31.1 36.0 32.4 35.2

± 0.4 ± 1.1 ± ± ± ±

0.9 0.2 0.4 0.2

± ± ± ± ± ±

1.0 0.7 2.2 0.4 0.1 0.3

± ± ± ± ± ± ±

0.9 0.5 0.6 0.2 0.5 0.7 0.1

Tmax: Temperature of the maximum degradation rate.

and SPI matrix. The aldehyde group of OSA was utilized to synthesize AgNPs, and OA was introduced onto the SPI matrix to enhance antibacterial function. In addition, OSA, acting as a bridge, imparted the composite film with a compact and multiple cross-linked structure by forming interfacial hydrogen bonds and a covalent network with AC and SPI molecules. This contributed to the remarkable mechanical behavior and excellent water resistance of the SPI/OA/AC films. Notably, modification of the SPI/OA composite film with 8 wt% AC led to a 230.3% improvement in strength and a corresponding 148.1% improvement in toughness compared to those parameters of the pristine SPI film. The wettability and water uptake tests showed that the SPI/ OA/AC-8 film was hydrophobic (103.3° ± 2.0°) and had a 65.2% decrease in water uptake. In addition, the SPI/OA/AC composite films presented an effect in lessening the growth of E. coli and S. aureus, with the lessening zones of both strains ≥ 16 mm. Our results also demonstrated that the incorporation of AC significantly enhanced the antibacterial properties of protein films, probably because the electrostatic force of the protonated groups (R-NH2) on the AC lamella induced the

4. Conclusion In summary, a new strategy was developed to integrate excellent antibacterial function into mechanically robust composites of OA, AC,

Fig. 9. (a) Thermogravimetric (TG) and (b) derivative thermogravimetric (DTG) curves of the composite films. 280

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

antimicrobial effect. This study presents a positive exploration to fabricate a biopolymer-based film that has good mechanical integrity, superior water resistance and antimicrobial properties with potential applications in packaging, biomedicine, and hygiene.

nanoparticle: synthesis, characterization and its application in photocatalytic and anticancer activity. Mater. Res. Express 6, 045003. Lee, Y.C., Kim, E.J., Ko, D.A., Yang, J.W., 2011. Water-soluble organo-building blocks of aminoclay as a soil-flushing agent for heavy metal contaminated soil. J. Hazard. Mater. 196, 101–108. Li, Y., Chen, H., Dong, Y., Li, K., Li, L., Li, J., 2016. Carbon nanoparticles/soy protein isolate bio-films with excellent mechanical and water barrier properties. Ind. Crop. Prod. 82, 133–140. Li, K., Jin, S., Han, Y., Li, J., Chen, H., 2017. Improvement in functional properties of soy Protein isolate-based film by cellulose nanocrystal–graphene artificial nacre nanocomposite. Polymers 9, 321. Li, K., Jin, S., Chen, H., He, J., Li, J., 2017a. A high-performance soy protein isolate-based nanocomposite film modified with microcrystalline cellulose and Cu and Zn nanoclusters. Polymers 9, 167. Li, K., Jin, S., Li, J., Chen, H., 2019. Improvement in antibacterial and functional properties of mussel-inspired cellulose nanofibrils/gelatin nanocomposites incorporated with graphene oxide for active packaging. Ind. Crop. Prod. 132, 197–212. Lin, J., Chen, X., Chen, C., Hu, J., Zhou, C., Cai, X., Wang, W., Zheng, C., Zhang, P., Cheng, J., Guo, Z., Liu, H., 2018. Durably antibacterial and bacterially antiadhesive cotton fabrics coated by cationic fluorinated polymers. ACS Appl. Mater. Inter. 10, 6124–6136. Liu, S., Bastola, A.K., Li, L., 2017. A 3D printable and mechanically robust hydrogel based on alginate and graphene oxide. ACS Appl. Mater. Inter. 9, 41473–41481. Liu, Y., Yu, S.-H., Bergström, L., 2018. Transparent and flexible nacre-like hybrid films of aminoclays and carboxylated cellulose nanofibrils. Adv. Funct. Mater. 28, 1703277. Martelli-Tosi, M., Masson, M.M., Silva, N.C., Esposto, B.S., Barros, T.T., Assis, O.B.G., Tapia-Blacido, D.R., 2018. Soybean straw nanocellulose produced by enzymatic or acid treatment as a reinforcing filler in soy protein isolate films. Carbohyd Polym 198, 61–68. Pan, H., Jiang, B., Chen, J., Jin, Z., 2014. Blend-modification of soy protein/lauric acid edible films using polysaccharides. Food Chem. 151, 1–6. Park, S.-H., Hwang, S.O., Kim, T.-S., Cho, A., Kwon, S.J., Kim, K.T., Park, H.-D., Lee, J.-H., 2018. Triclosan-immobilized polyamide thin film composite membranes with enhanced biofouling resistance. Appl. Surf. Sci. 443, 458–466. Pei, A., Malho, J.-M., Ruokolainen, J., Zhou, Q., Berglund, L.A., 2011. Strong nanocomposite reinforcement effects in polyurethane elastomer with low volume fraction of cellulose nanocrystals. Macromolecules 44, 4422–4427. Perez-Puyana, V., Felix, M., Romero, A., Guerrero, A., 2018. Development of eco-friendly biodegradable superabsorbent materials obtained by injection moulding. J. Clean. Prod. 198, 312–319. Phua, S.L., Yang, L., Toh, C.L., Guoqiang, D., Lau, S.K., Dasari, A., Lu, X., 2013. Simultaneous enhancements of UV resistance and mechanical properties of polypropylene by incorporation of dopamine-modified clay. ACS Appl. Mater. Inter. 5, 1302–1309. Qi, L., Liu, Z., Wang, N., Hu, Y., 2018. Facile and efficient in situ synthesis of silver nanoparticles on diverse filtration membrane surfaces for antimicrobial performance. Appl. Surf. Sci. 456, 95–103. Ravula, S., Essner, J.B., La, W.A., Polo-Parada, L., Kargupta, R., Hull, G.J., Sengupta, S., Baker, G.A., 2015. Sunlight-assisted route to antimicrobial plasmonic aminoclay catalysts. Nanoscale 7, 86–91. Sarker, B., Papageorgiou, D.G., Silva, R., Zehnder, T., Gul-E-Noor, F., Bertmer, M., Kaschta, J., Chrissafis, K., Detsch, R., Boccaccini, A.R., 2014. Fabrication of alginate–gelatin crosslinked hydrogel microcapsules and evaluation of the microstructure and physico-chemical properties. J. Mater. Chem. B 2, 1470. Scherer, M.D., Sposito, J.C.V., Falco, W.F., Grisolia, A.B., Andrade, L.H.C., Lima, S.M., Machado, G., Nascimento, V.A., Goncalves, D.A., Wender, H., Oliveira, S.L., Caires, A.R.L., 2019. Cytotoxic and genotoxic effects of silver nanoparticles on meristematic cells of Allium cepa roots: a close analysis of particle size dependence. Sci. Total Environ. 660, 459–467. Shao, C., Wang, M., Meng, L., Chang, H., Wang, B., Xu, F., Yang, J., Wan, P., 2018. Mussel-inspired cellulose nanocomposite tough hydrogels with synergistic selfhealing, adhesive, and strain-sensitive properties. Chem. Mater. 30, 3110–3121. Shirdast, A., Sharif, A., Abdollahi, M., 2016. Effect of the incorporation of sulfonated chitosan/sulfonated graphene oxide on the proton conductivity of chitosan membranes. J. Power Sources 306, 541–551. Shuai, C., Guo, W., Wu, P., Yang, W., Hu, S., Xia, Y., Feng, P., 2018. A graphene oxide-Ag co-dispersing nanosystem: dual synergistic effects on antibacterial activities and mechanical properties of polymer scaffolds. Chem. Eng. J. 347, 322–333. Sun, P., Wang, J., Yao, X., Peng, Y., Tu, X., Du, P., Zheng, Z., Wang, X., 2014. Facile preparation of mussel-inspired polyurethane hydrogel and its rapid curing behavior. ACS Appl. Mater. Inter. 6, 12495–12504. Tian, Y., Cao, Y., Wang, Y., Yang, W., Feng, J., 2013. Realizing ultrahigh modulus and high strength of macroscopic graphene oxide papers through crosslinking of musselinspired polymers. Adv. Mater. 25, 2980–2983. Wang, H., Wang, L., 2017. Developing a bio-based packaging film from soya by-products incorporated with valonea tannin. J. Clean. Prod. 143, 624–633. Wei, Z., Yang, J.H., Liu, Z.Q., Xu, F., Zhou, J.X., Zrínyi, M., Osada, Y., Chen, Y.M., 2015. Novel biocompatible polysaccharide-based self-Healing hydrogel. Adv. Funct. Mater. 25, 1352–1359. Wei, X., Xiong, H., Zhou, D., Jing, X., Huang, Y., 2018. Ion-assisted fabrication of neutral protein crosslinked sodium alginate nanogels. Carbohydr. Polym. 186, 45–53. Wu, M., Ma, B., Pan, T., Chen, S., Sun, J., 2016. Silver-nanoparticle-colored cotton fabrics with tunable colors and durable antibacterial and self-Healing superhydrophobic properties. Adv. Funct. Mater. 26, 569–576. Wu, C.N., Fuh, S.C., Lin, S.P., Lin, Y.Y., Chen, H.Y., Liu, J.M., Cheng, K.C., 2018. TEMPOoxidized bacterial cellulose pellicle with silver nanoparticles for wound dressing.

Acknowledgments This work was financially supported by the Nation Key Research and Development Program of China (2017YFD0601205), and National Natural Science Foundation of China (No. 21703009). References Achari, A., Datta, K.K., De, M., Dravid, V.P., Eswaramoorthy, M., 2013. Amphiphilic aminoclay-RGO hybrids: a simple strategy to disperse a high concentration of RGO in water. Nanoscale 5, 5316–5320. Akaighe, N., Maccuspie, R.I., Navarro, D.A., Aga, D.S., Banerjee, S., Sohn, M., Sharma, V.K., 2011. Humic acid-induced silver nanoparticle formation under environmentally relevant conditions. Environ. Sci. Technol. 45, 3895–3901. Balakrishnan, B., Joshi, N., Jayakrishnan, A., Banerjee, R., 2014. Self-crosslinked oxidized alginate/gelatin hydrogel as injectable, adhesive biomimetic scaffolds for cartilage regeneration. Acta Biomater. 10, 3650–3663. Bui, V.K.H., Park, D., Lee, Y.-C., 2018. Aminoclays for biological and environmental applications: an updated review. Chem. Eng. J. 336, 757–772. Cao, N., Lyu, Q., Li, J., Wang, Y., Yang, B., Szunerits, S., Boukherroub, R., 2017. Facile synthesis of fluorinated polydopamine/chitosan/reduced graphene oxide composite aerogel for efficient oil/water separation. Chem. Eng. J. 326, 17–28. Carpiné, D., Dagostin, J.L.A., de Andrade, E.F., Bertan, L.C., Mafra, M.R., 2016. Effect of the natural surfactant Yucca schidigera extract on the properties of biodegradable emulsified films produced from soy protein isolate and coconut oil. Ind. Crop. Prod. 83, 364–371. Chaturbedy, P., Jagadeesan, D., Eswaramoorthy, M., 2010. pH-Sensitive breathing of clay within the polyelectrolyte matrix. ACS Nano 4, 5921–5929. Chen, C.Y., Wong, C.P., 2014. Shape-diversified silver nanostructures uniformly covered on aluminium micro-powders as effective SERS substrates. Nanoscale 6, 811–816. Chen, K., Tian, Q., Tian, C., Yan, G., Cao, F., Liang, S., Wang, X., 2017. Mechanical reinforcement in thermoplastic polyurethane nanocomposite incorporated with polydopamine functionalized graphene nanoplatelet. Ind. Eng. Chem. Res. 56, 11827–11838. Chen, G.-G., Hu, Y.-J., Peng, F., Bian, J., Li, M.-F., Yao, C.-L., Sun, R.-C., 2018. Fabrication of strong nanocomposite films with renewable forestry waste/montmorillonite/reduction of graphene oxide for fire retardant. Chem. Eng. J. 337, 436–445. Ciannamea, E.M., Espinosa, J.P., Stefani, P.M., Ruseckaite, R.A., 2018. Long-term stability of compression-molded soybean protein concentrate films stored under specific conditions. Food Chem. 243, 448–452. Datta, K.K.R., Achari, A., Eswaramoorthy, M., 2013. Aminoclay: a functional layered material with multifaceted applications. J. Mater. Chem. A 1, 6707. Ding, F., Shi, X., Wu, S., Liu, X., Deng, H., Du, Y., Li, H., 2017a. Flexible polysaccharide hydrogel with pH-Regulated recovery of self-healing and mechanical properties. Macromol. Mater. Eng. 302, 1700221. Ding, W., Zhou, J., Zeng, Y., Wang, Y.-n., Shi, B., 2017b. Preparation of oxidized sodium alginate with different molecular weights and its application for crosslinking collagen fiber. Carbohyd. Polym. 157, 1650–1656. Echeverría, I., Eisenberg, P., Mauri, A.N., 2014. Nanocomposites films based on soy proteins and montmorillonite processed by casting. J. Membrane Sci. 449, 15–26. Fu, F., Li, L., Liu, L., Cai, J., Zhang, Y., Zhou, J., Zhang, L., 2015. Construction of cellulose based ZnO nanocomposite films with antibacterial properties through one-step coagulation. ACS Appl. Mater. Inter. 7, 2597–2606. González, A., Strumia, M.C., Alvarez Igarzabal, C.I., 2011. Cross-linked soy protein as material for biodegradable films: synthesis, characterization and biodegradation. J. Food Eng. 106, 331–338. Huang, N., Zhang, S., Yang, L., Liu, M., Li, H., Zhang, Y., Yao, S., 2015. Multifunctional electrochemical platforms based on the michael Addition/Schiff base reaction of polydopamine modified reduced graphene oxide: construction and application. ACS Appl. Mater. Interfaces 7, 17935–17946. Jiang, R., Liu, M., Huang, H., Mao, L., Huang, Q., Wen, Y., Cao, Q.-y., Tian, J., Zhang, X., Wei, Y., 2018. Ultrafast construction and biological imaging applications of AIE-active sodium alginate-based fluorescent polymeric nanoparticles through a one-pot microwave-assisted Döbner reaction. Dye. Pigment. 153, 99–105. Jin, S., Li, K., Li, J., 2018a. A general bio-inspired, novel interface engineering strategy toward strong yet tough protein based composites. Appl. Surf. Sci. 447, 452–462. Jin, S., Li, K., Li, J., 2018b. Nature-inspired green procedure for improving performance of protein-based nanocomposites via introduction of nanofibrillated cellulose-stablized graphene/carbon nanotubes hybrid. Polymers 10, 270. Kang, H., Wang, Z., Zhang, W., Li, J., Zhang, S., 2016. Physico-chemical properties improvement of soy protein isolate films through caffeic acid incorporation and trifunctional aziridine hybridization. Food Hydrocolloid 61, 923–932. Khan, A.Y., Kumaraswamy, G., 2018. Soft, Elastic macroporous monolith by templating high internal phase emulsions with aminoclay: preparation, pore structure and use for enzyme immobilization. ACS Appl. Nano. Mater. 1, 3407–3416. Latha, D., Prabu, P., Gnanamoorthy, G., Sampurnam, S., Manikandan, R., Arulvasu, C., Narayanan, V., 2019. Facile Justicia adhatoda leaf extract derived route to silver

281

Industrial Crops & Products 135 (2019) 271–282

S. Jin, et al.

Zhang, P., Zhang, J., 2013. One-step acrylation of soybean oil (SO) for the preparation of SO-based macromonomers. Green Chem. 15, 641. Zhao, Y., He, M., Zhao, L., Wang, S., Li, Y., Gan, L., Li, M., Xu, L., Chang, P.R., Anderson, D.P., Chen, Y., 2016. Epichlorohydrin-cross-linked hydroxyethyl cellulose/soy protein isolate composite films as biocompatible and biodegradable implants for tissue engineering. ACS Appl. Mater. Inter. 8, 2781–2795. Zheng, W., Liu, Y., West, A., Schuler, E.E., Yehl, K., Dyer, R.B., Kindt, J.T., Salaita, K., 2014. Quantum dots encapsulated within phospholipid membranes: phase-dependent structure, photostability, and site-selective functionalization. J. Am. Chem. Soc. 136, 1992–1999.

Biomacromolecules 19, 544–554. Yan, Y., Wang, K., Wang, Z., Gindl-Altmutter, W., Zhang, S., Li, J., 2017. Fabrication of homogeneous and enhanced soybean protein isolate-based composite films via incorporating TEMPO oxidized nanofibrillated cellulose stablized nano-ZnO hybrid. Cellulose 24, 4807–4819. Yu, Z., Sun, L., Wang, W., Zeng, W., Mustapha, A., Lin, M., 2018. Soy protein-based films incorporated with cellulose nanocrystals and pine needle extract for active packaging. Ind. Crop. Prod. 112, 412–419. Zhang, S., Xia, C., Dong, Y., Yan, Y., Li, J., Shi, S.Q., Cai, L., 2016. Soy protein isolatebased films reinforced by surface modified cellulose nanocrystal. Ind. Crop. Prod. 80, 207–213.

282