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Jan 26, 2017 - Hospital, Harvard Medical School, 181 Longwood Avenue, Boston 02139, ... Biomedical Engineering, Zhejiang University, 38 Zheda Road, ...
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Research Article pubs.acs.org/journal/ascecg

Copper Sulfide Nanoparticle/Cellulose Composite Paper: Room-Temperature Green Fabrication for NIR Laser-Inducible Ablation of Pathogenic Microorganisms Xiujie Huang,† Ning Hu,‡,§ Xiaoying Wang,*,†,‡ Yu Shrike Zhang,*,‡ and Runcang Sun† †

State Key Laboratory of Pulp and Paper Engineering, South China University of Technology, 381 Wushan Road, Guangzhou 510640, China ‡ Biomaterials Innovation Research Center, Division of Biomedical Engineering, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, 181 Longwood Avenue, Boston 02139, United States § Key Laboratory of Biomedical Engineering of Ministry of Education, Biosensor National Special Laboratory, Department of Biomedical Engineering, Zhejiang University, 38 Zheda Road, Hangzhou, Zhejiang 310027, China ABSTRACT: This work reports a new type of near-infrared (NIR) laser-inducible antimicrobial composite paper based on copper sulfide nanoparticles (CuS NPs). For the first time, a smart and green method to prepare CuS NPs was developed by taking advantage of the copper−amine complex as the copper source and sodium sulfide as the sulfur source at room temperature, in which a biopolymer xylan was used as the growth template and stabilizing agent. The obtained xylan/CuS NPs composites (CuS@Xylan NPs) were spherical and stable with an average diameter of ∼10 nm. CuS@Xylan NPs were subsequently allowed to penetrate into cellulose nanofiber (CNF) networks to prepare the composite paper. This CuS@Xylan NPs/CNF composite paper showed strong NIR laser-inducible antimicrobial effect on Escherichia coli, Bacillus subtilis, Stapylococcus aureus, and Aspergillus niger. In addition, the tensile strength, tear strength, and burst strength of the composite paper were improved likely due to the strong hydrogen bonding between xylan and CNFs. This study provides a novel strategy to synthesize CuS NPs and generation of a new proof-of-concept type of composite paper for convenient ablation of pathogenic microorganisms, which has a potential to be applied to skin wound infection prevention for rapid wound healing. KEYWORDS: Xylan, Copper sulfide nanoparticles, Laser-inducible ablation, Antimicrobial paper, Cellulose



INTRODUCTION The overuse of antibiotics has resulted in the evolution of pathogenic microorganisms to resist drugs, leading to significantly decreased efficacy of antimicrobial agents. For example, bacteria resistance is one of the greatest challenges to human public health.1,2 Therefore, development of new materials based on alternative antimicrobial mechanisms are in strong demand.3,4 Among the variety of strategies, near-infrared (NIR) laserinducible photothermal and photodynamic mechanisms are effective for ablation of pathogenic bacteria,5,6 which importantly, will not result in bacterial resistance. To this end, NIR laserinducible ablation technologies based on photoabsorbing agents have become an attractive research focus to achieve sterilization. Currently, several nanomaterials are used as the photoabsorbing agent, such as gold nanoshells,7 gold nanorods,8 gold nanocages,9 carbon nanotubes,10,11 and graphene.12,13 However, a few drawbacks have limited their widespread applications. For example, the NIR absorption of gold nanoparticles is attributed to the surface plasmon resonance phenomenon, and their optical absorption strongly depends on the particle size and morphology, which may cause instability of the absorption due © 2017 American Chemical Society

to particle melting and shape/size alteration during light treatment. The relatively high cost for synthesis of gold nanomaterials posts another obstacle. In comparison, the NIR absorption of copper sulfide nanoparticles (CuS NPs) is derived from the localized surface plasmon resonance, which have already been proposed to be practically exploitable in biomedical imaging, photothermal cancer therapy, energy conversion and storage, and sensing.14−17 The unique optical properties and low cost of production provides a possibility for CuS NPs to act as a promising new type of photoabsorbing agent for ablation of pathogenic microbes. Conventional methods for the synthesis of CuS NPs include hydrothermal, solvothermal, reflux, and microwaving, among others.18−21 However, these synthesis methods almost always require high reaction temperature, organic solvents, and surfactants. They result in complicated preparation, high cost, difficult purification, and environmental pollution, which have Received: December 9, 2016 Revised: January 24, 2017 Published: January 26, 2017 2648

DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655

Research Article

ACS Sustainable Chemistry & Engineering

(AFM) images were obtained using Dimension Fastscan Bio (Bruker, Germany). The CuS@Xylan NPs samples for AFM were prepared on freshly cleaved mica. The structure of CuS, CuS@Xylan NPs, and xylan were analyzed by Fourier transform infrared (FT-IR) spectroscopy. FT-IR spectra were obtained on a Vector 33 spectrophotometer (Bruker, Germany) under a dry air at room temperature by the KBr pellet method. The spectra were collected over the range from 4000 to 500 cm−1 with a resolution of 4 cm−1. Structure Analysis of Xylan before and after the Reaction. The structure of original xylan, regenerated xylan after dissolved in NaOH solution at room temperature, and regenerated xylan after the synthesis of CuSNPs (xylan was obtained from the supernatant separated from colloid of CuS@Xylan NPs after high-speed centrifugation) were analyzed by FT-IR spectroscopy. Preparation and Property of CuS@Xylan NPs/CNF Composite Paper. A 20 mL portion of CuS@Xylan NPs colloid (different concentrations) was added into 50 mL of CNF pulp (dry weight of 0.06 g) and stirred for 2 h. The wet sheet was obtained by suction filtration with 0.22-μm membrane. Then, the wet sheet was dried at 60 °C to prepare the CuS@Xylan NPs/CNF composite paper. The above composite paper was irradiated by NIR laser (808 nm, 1.5 W/cm2) for 2 min and the temperature change of the composite paper was recorded by a temperature probe and UNI-T 1310 thermometer (UNI-T, Hong Kong) to evaluate the photothermal conversion efficiency. Optocouplers laser (MW-GX-808/1-5000 mW) was purchased from Leishi Optoelectronics Technology Co., Ltd. (Changchun, China). The morphological and structural characteristics of the composite papers were carried out with an EVO-18 scanning electron microscope (SEM, Zeiss, Germany). X-ray diffraction (XRD) measurements of the crystal structure were recorded on a D8 Advance X-ray diffractometer (Bruker, Germany) using Cu Kα radiation (λ = 0.15418 nm) at 40 kV with a scanning rate of 2°/min and a scanning scope of 20−80° (2θ). Mechanical properties of the CuS@Xylan NPs/CNF composite paper were determined by L&W Tensile Tester (Sweden), L&W Tear Tester (Sweden), and L&W Burst Tester (Sweden). The stretching test was carried out with an INSTRON 5565 tensile and compression testing machine. The paper sheets were stabilized in a constant temperature and humidity chamber (temperature of 23 ± 1 °C, humidity of 50 ± 2%) for 24 h before testing. The tensile index, tear index, and burst index were calculated according to the standards of ISO 1924, ISO 1974, and ISO 2758. Differences in tensile index, tear index, and burst index were analyzed using two-tailed test. Differences between groups were considered statistically significant at p < 0.05. NIR Laser-Inducible Antimicrobial Experiment. Bacillus subtilis and Stapylococcus aureus are representative Gram-positive bacteria, Escherichia coli is a representative Gram-negative bacterium, and Aspergillus niger is a representative fungus. The NIR laser-inducible ablation effect of the composite paper on these four pathogenic microorganisms would be representative and should be able to prove that its antibacterial effect is universal. Therefore, Escherichia coli, Bacillus subtilis, Stapylococcus aureus, and Aspergillus niger were chosen to test. They provided by Guangdong Microbiology Institute. Agar culture medium was prepared by 1% peptone, 0.5% beef extract, 0.5% sodium chloride, and 2% agar, and the system pH was adjusted to 7.2. The paper sheets (include pure CNF papers and composite papers with 0.3−1.5 mM of concentration of CuS@Xylan NPs) were attached onto culture medium inoculated by different bacterials (Escherichia coli, Bacillus subtilis, Stapylococcus aureus) or fungus (Aspergillus niger), and then irradiated by NIR laser with given power density (NIR laser power density varies between 0.1 W/cm2 and 2.0 W/cm2) for given time (irradiation time varies between 0.5 and 5.0 min), followed by culturing in climate chamber (37 °C, bacterial for 24 h, fungus for 3 days). NIR laser-inducible antimicrobial effects of the paper sheets were verified by measuring the size of antimicrobial circles. Differences in size of antimicrobial circles were analyzed using two-tailed t test. Differences between groups were considered statistically significant at p < 0.05.

so far limited the applications of CuS NPs. It is therefore pressing to develop low-cost, clean, nontoxic, and eco-friendly approaches for the synthesis of CuS NPs. Currently, green synthesis of nanoparticles by taking advantage of plant extracts has been extensively explored.22−25 Hemicelluloses, as abundant forestry and agricultural residues, feature large quantity of hydroxyl groups and are in the form of helical chains or random coils in aqueous solution, which can potentially function as a viable template to achieve synthesis of nanoparticles.26 We hypothesized that, using such a strategy it would be possible to avoid the use of high reaction temperature, organic solvents, and surfactants, where hemicelluloses could act as a growth template and stabilizing agent for synthesis of CuS NPs by capping the synthesized nanoparticles within the special structural network. In this study we used xylan, the most common type of hemicelluloses, to act as the growth template and stabilizing agent to synthesize CuS NPs at room temperature (with [Cu(NH3)4]2+ as the copper source and Na2S as the sulfide source). This strategy has provided a simple, effective, energy-saving, and environmentfriendly method to prepare CuS NPs. More importantly, we further developed a prototype NIR laser-inducible antimicrobial composite paper by infiltrating CuS@Xylan NPs into cellulose nanofiber (CNF) networks. The unique NIR laser-inducible ablation mechanism of the composite paper, differing from those of antibiotics and chemicals, provides a potential solution for microbial resistance. This composite paper has the potential to be applied for skin wound infection prevention and rapid wound healing.



EXPERIMENTAL SECTION

Materials. Xylan (Mw: 4.9 × 104 g/mol) isolated from bagasse was purchased from Shanghai Yuanye Biotechnology Co., Ltd. (Shanghai, China). The sugar composition was as follows: 87.35% xylose, 9.28% arabinose, 0.81% glucose, 0.50% galactose, and 2.06% glucuronic acid. CNFs were purchased from Intelligent Chemicals Pty Ltd. (China). Its average fiber length and average fiber diameter were 400−600 μm and 10−50 nm, respectively. Sodium hydroxide (NaOH), ammonia (25−28%), copper sulfate (CuSO4·5H2O), and sodium sulfide (Na2S·9H2O) were all analytical grade. Preparation of CuS@Xylan NPs. CuSO4·5H2O (0.1 g) was dissolved in water (50 mL). Then, the diluted ammonia (7 mol/L, 4 mL) was added dropwise to the CuSO4·5H2O solution under constant stirring. The deep blue copper−amine complex ([Cu(NH3)4]2+) was obtained after the light blue basic copper sulfate precipitation disappeared.27 Xylan (0.7 g) was dissolved in 2% aqueous NaOH (100 mL). [Cu(NH3)4]2+ solution was added into the above solution and stirred for 2 h in room temperature. Then, Na2S·9H2O (0.04 mol/L, 20 mL) was added dropwise to this solution under stirring at given temperature (room-temperature, 50, 70, and 90 °C) and reacted for given time (5, 10, 30, 50, and 70 min). After the reaction, the CuS@Xylan NPs colloidal solution was dialyzed until the S2− was completely removed (tested with CuCl2). The CuS@Xylan NPs were obtained after lyophilization at −40 °C for 36 h. Characterization of CuS@Xylan NPs. UV−vis spectra were obtained by TU-1810 (Beijing, China) with a scan range of 1100− 400 nm. JEM-2010HR transmission electron microscope (TEM, JEOL, Japan) was used to investigate the microstructure of the CuS@Xylan NPs at an accelerating voltage of 200 kV. TEM samples were prepared by diluting the colloidal CuS@Xylan NPs with water with sonication. A few drops of the suspended CuS@Xylan NPs were placed on a copper grid coated with ultrathin carbon film. Size distribution analysis was carried out using a Nano Particle Analyzer SZ-100 apparatus (HORIBA, Japan). The concentration of colloidal CuS@Xylan NPs was fixed at 0.1% (w/v). Atomic force microscopy 2649

DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655

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ACS Sustainable Chemistry & Engineering



RESULTS AND DISCUSSION Proposed Process of Room-Temperature Fabrication and NIR Laser-Inducible Antimicrobial CuS@Xylan NPs/ CNF Composite Paper. NIR laser-inducible ablation based on nanomaterials is an effective method for solving the problem of bacterial resistance in the cases of antibiotic and chemical treatments.28−31 Due to the intense NIR absorption, CuS-based nanomaterials are a potential class of NIR laser-inducible antimicrobial material.32 In this study, a smart and green method for preparing CuS NPs was proposed, and the synthesis process and NIR laser-inducible antimicrobial behavior of the CuS@Xylan NPs/CNF composite paper was investigated, as shown in Figure 1. In aqueous medium, xylan molecules

CuS nanoclusters. The gap confinement effect of xylan molecules limited the overgrowth of the nanoparticles, which contributed to the formation of dimensionally stable CuS NPs. To this end, the xylan molecules acted as both a growth template and stabilizing agent in the synthesis process of CuS NPs. In this process, [Cu(NH3)4]2+, but not Cu2+, was selected as the copper source. It was because that the reducing end aldehyde of xylan could reduce Cu2+ to elemental copper, and metathesis reaction would trigger when Cu2+ encounters NaOH in the xylan alkaline solution. In comparison, [Cu(NH3)4]2+ was stable in xylan alkaline solution and could not be reduced by the reducing end aldehyde of xylan. To obtain the NIR laser-inducible antimicrobial paper, CuS@Xylan NPs were infiltrated into the CNF networks. The hydrogen bonding between CNF and xylan molecules improved the stability of CuS NPs in the paper. In this process, CNF acted as a carrier for CuS@Xylan NPs, while CuS@Xylan NPs conferred NIR laser-inducible antimicrobial property for the composite paper. Therefore, this CuS@Xylan NPs/CNF composite paper was able to ablate pathogenic microorganisms under NIR laser irradiation. Synthesis Optimization and Characterization of CuS@ Xylan NPs. The reaction temperature and reaction time during the synthesis process have a significant impact on the size and shape of nanoparticles, especially when biomacromolecules are used to act as the growth template and stabilizing agent.33,34 As shown in Figure 2a, significant precipitation was found when the reaction was conducted without xylan (the leftmost), indicating the failure of preparation of CuS NPs. The CuS@Xylan NPs aqueous solution, obtained at room temperature, was dark green. However, a trend of more pronounced precipitation was found in the CuS@Xylan NP aqueous systems as the temperature for the reaction was increased. The reaction temperature and precipitation was positively correlated. This observation might be attributed to the increasing damage of the xylan molecular chains caused by higher reaction temperatures, weakening the role of xylan as a growth template and stabilizing agent. In addition, excessive aggregation of nanoparticles tended to occur at higher temperatures, also potentially leading to the generation of precipitation.35 As shown in Figure 2b, CuS@Xylan NP aqueous systems prepared at different reaction times under room temperature were all dark green and stable; all of which exhibited strong NIR absorption peaks at ∼990 nm. The absorption peak intensity increased with the increase of reaction time, implying the growth and increased number of CuS NPs. The absorption peak intensity no longer increased when the reaction time was beyond 30 min, indicating the reaction equilibrium. Compared with the conventional methods,36,37 this is a green strategy for synthesis of CuS NPs with xylan as growth template and stabilizing agent at room temperature in 30 min, without using organic solvents or surfactants. TEM image in Figure 3a visually proved that the spherical CuS@Xylan NPs were well dispersed with an average diameter of ∼10 nm. In Figure 3b, the lattice of the spherical CuS NPs could be found in the high-resolution TEM (HRTEM) image. Figure 3c and d displays AFM images and height profiles of CuS@Xylan NPs. The CuS@Xylan NPs showed an average height of ∼10 nm, which was in agreement with the result from the TEM image. The particle size distribution (as shown in Figure 3e) confirms that the CuS@Xylan NPs show an average diameter of 10.1 nm. The FT-IR spectra of CuS, CuS@Xylan NPs, and xylan are indicated in Figure 3f. Compared with the spectra of CuS, the characteristic peaks of xylan appeared in the

Figure 1. Schematic on the synthesis of CuS@Xylan NPs and NIR laser-inducible ablation of the CuS@Xylan NPs/CNF composite paper. In this synthesis process, CuS NPs were prepared at room temperature using [Cu(NH3)4]2+ as the copper source and Na2S as the sulfide source, while xylan molecules functioned as the growth template and stabilizing agent. NIR laser-inducible photothermal antimicrobial composite paper was prepared by combination of CNFs and CuS@ Xylan NPs. Step 1: the introduction of copper source ([Cu(NH3)4]2+), forming a complex with xylan molecules. Step 2: the introduction of sulfide source (Na2S·9H2O), forming CuS nanoclusters with [Cu(NH3)4]2+ with the induction of xylan molecule template. Step 3: growth of CuS nanoclusters with xylan molecules coating onto the surface of CuS NPs as a stabilizing agent. Step 4: the combination of CNFs and CuS@Xylan NPs to prepare the composite paper. Step 5: the NIR laser-induced antimicrobial behavior of the composite paper. It is noteworthy to mention that the shapes and relative sizes of various components shown in this schematic are for illustrative purpose only, and they are not indicative of the actual structures.

possessed numerous hydroxyl groups and were in the form of helical chains or random coil chains, which could form complexes with [Cu(NH3)4]2+. This resulted in the enrichment of [Cu(NH3)4]2+ surrounding xylan molecules, providing potential nucleation sites for crystallization of CuS NPs. With the introduction of the sulfide source (Na2S·9H2O), CuS nanoclusters were then formed in the place enriched by [Cu(NH3)4]2+, while further reactions promoted the growth of 2650

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Figure 2. Macroscopic appearance and UV−vis spectra of CuS@Xylan NPs. (a) Effect of xylan and reaction temperature on the synthesis of CuS@ Xylan NPs at fixed reaction time of 5 min; the leftmost reaction was conducted without xylan at room temperature (26 °C), and the rest of the reactions were conducted with xylan at room temperature, 50, 70, and 90 °C, respectively. (b) Effect of reaction time on the synthesis of CuS@Xylan NPs at fixed reaction temperature of room temperature, showing the UV−vis spectra of CuS@Xylan NPs prepared by different reaction times. Inset: macroscopic photographs of CuS@Xylan NPs colloids prepared at room temperature with different reaction times. The dosage of samples was consistent and the CuS@Xylan NPs aqueous systems were allowed to stabilize for 48 h before photographing.

vibration of the CH2 group appeared at 2893 cm−1. The absorptions at 1468 and 1384 cm−1 were attributed to CH3 and CH, respectively. The CH shear vibration appeared at 1414 cm−1.26 The band at 1249 cm−1 was related to the C−O linkage in the acetyl group, and the band at 1172 cm−1 was related to the C−O linkage in the ether group. The characteristic peak of typical xylan at 1040 cm−1 was assigned to C−O and C−C stretching and the contributions of glycoside (C−O−C). The absorptions at 980 and 2129 cm−1 originated from CC and CC stretching vibrations, respectively. Another important band appeared at 896 cm−1, corresponding to the β-configuration of the 1−4 glycosidic bonds between the xylopyranose units of the main xylan linkages.38 In addition, the absorptions at 2350 and 1656 cm−1 were related to the presence of CO2 and H2O in the testing sample. Compared with Xylan1, the FT-IR spectra of Xylan2 and Xylan3 presented new characteristic absorption peaks with weak strength at 1220 cm−1, which was related to the ester group linkage in the acetates. It indicated that peeling reaction of reducing end group of xylan occurred in the xylan/NaOH aqueous medium. The FT-IR spectra of Xylan2 and Xylan3 had almost similar characteristic absorption peaks, showing that the original chemical structure of xylan was intact during the synthesis procedure. Therefore, it could be concluded that xylan mainly acted as the growth template and stabilizing agent in the synthesis of CuS@Xylan NPs. Characterization and NIR Laser-Inducible Antimicrobial Property of CuS@Xylan NPs/CNF Composite Papers. The composite paper was prepared by infiltrating CuS@Xylan NPs into the CNF network. As shown in the EDS image (inset) in Figure 4a, the surface of the CuS@Xylan NPs/CNF composite paper included the elements Cu and S, confirming the presence of CuS NPs in the CNF network and a large number of CuS NPs were filled in CNF network. As a result of the coating of xylan onto CuS NPs, CuS@Xylan NPs could tightly adhere to the surface of CNF potentially due to the hydrogen bonding between xylan and CNF (Figure 4a and b). In comparison, the CNF paper presented only interleaved network without any nanoparticles (Figure 4c and d). In addition, the structure of the paper with CuS@Xylan NPs was more compact than that of paper with only CNF.

Figure 3. (a, b) TEM images of CuS@Xylan NPs. (c, d) Tapping model of AFM topographic images and relative height profiles of CuS@Xylan NPs. (e) Particle size distribution of CuS@Xylan NPs. (f) FT-IR spectra of the CuS, CuS@Xylan NPs, and xylan (Xylan1: original xylan. Xylan2: regenerated xylan dissolved in the NaOH solution at room temperature followed by lyophilization. Xylan3: regenerated xylan after the synthesis of CuS NPs, which were obtained by high-speed centrifugation of the supernatant and lyophilization).

spectra of CuS@Xylan NPs, confirming the loading of xylan on CuS NPs. These evidence confirmed that CuS@Xylan NPs with relatively uniform morphology and size were successfully synthesized in xylan solution at room temperature. Structure Analysis of Xylan before and after Reaction. The FT-IR spectra of Xylan1 (original xylan), Xylan2 (regenerated xylan dissolved in NaOH solution at room temperature followed by lyophilization), and Xylan3 (regenerated xylan after the synthesis of CuS@Xylan NPs, obtained by high-speed centrifugation of the supernatant and lyophilization) are shown in Figure 3f. For Xylan1, the strong band at 3429 cm−1 was originated from −OH stretching vibrations. The C−H stretching 2651

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verified and the NIR laser-inducible antimicrobial conditions were also optimized by measuring the sizes of antimicrobial circles. First, the effect of different concentrations of CuS@Xylan NPs in the composite papers on the antimicrobial property was evaluated. The composite papers with different concentrations of CuS@Xylan NPs (0.3, 0.6, 1.0, 1.3, and 1.5 mM) were attached onto the agar plate inoculated with Stapylococcus aureus, irradiated with the same doses of NIR irradiation (808 nm, 1.5 W/cm2) for 2 min. After incubation, the sizes of antimicrobial circles were significantly larger with CuS@Xylan NPs concentrations of 1.3 and 1.5 mM than those with CuS@Xylan NPs concentrations of 0.3, 0.6, and 1.0 mM (Figure 5a and b,

Figure 4. (a) SEM surface morphology image. (inset) Energy dispersive spectrometer (EDS) about the surface of composite paper. (b) Cross-section image of the CuS@Xylan NPs/NFC composite paper. (c) SEM surface morphology image and (d) cross section image of the pure NFC paper. (e) XRD patterns of CNF paper and composite paper. (f) Heating curve of the composite papers containing different concentrations of CuS@Xylan NPs, irradiated by NIR laser (808 nm, 1.5 W/cm2) for up to 2 min. ΔT refers to the temperature difference of the papers before and after irradiation by NIR laser for corresponding times in part f. The concentrations of CuS@Xylan NPs in the composite papers were all 1.3 mM in parts a, b, and e.

The XRD patterns of the CNF paper and the composite paper are shown in Figure 4e. In contrast with the peaks of CNF paper, three characteristic diffraction peaks (corresponding to facets (101), (102), and (110), respectively) of CuS appeared on the composite paper, validating the presence of CuS@Xylan NPs in the CNF network. Compared to the standard JCPDS (no. 89-3722) of CuS,39 other characteristic diffraction peaks of CuS were obscure, which might be due to the coating of xylan on CuS NPs. The NIR laser-inducible heating ability of the composite paper was evaluated. CuS@Xylan NPs colloids at different concentrations were combined with CNF to prepare composite papers, on which an NIR laser was irradiated and the change of temperature was continuously monitored. As shown in Figure 4f, the temperatures of the papers in all cases increased with prolonged irradiation time to eventually plateaus. The temperature of pure CNF paper (without CuS@Xylan NPs) increased by 19.1 °C. In comparison, the temperature of the composite papers increased by 32.3, 44.5, 52.3, 60.5, and 67.5 °C, for concentrations of CuS@Xylan NPs of 0.3, 0.6, 1.0, 1.3, and 1.5 mM, respectively. The higher concentration of CuS@Xylan NPs resulted in the higher heating rate of the composite paper and the greater temperature change. Compared to CuS NPs previously reported,32 the CuS NPs composite papers showed higher heating rates with the same NIR laser irradiation. This laid a good foundation for the NIR laser-inducible antimicrobial property of CuS@Xylan NPs/CNF composite paper. The NIR laser-inducible antimicrobial efficiency of the CuS@Xylan NPs/CNF composite papers was subsequently

Figure 5. Effect of the composite paper and NIR laser irradiation conditions on the antimicrobial effects. (a and b) Effect of concentration of CuS@Xylan NPs in the composite paper on the antimicrobial property at fixed NIR laser power density of 1.5 W/cm2 and irradiation time of 2 min. (c and d) Effect of NIR laser power on the antimicrobial property at fixed CuS@Xylan NPs concentration of 1.3 mM and irradiation time of 2 min. (e and f) Effect of NIR laser irradiation time on the antimicrobial property at fixed CuS@Xylan NPs concentration of 1.3 mM and NIR laser power density of 1.5 W/ cm2. Note: Stapylococcus aureus was selected as the target microbes. * indicates p < 0.05.

p < 0.01), indicating that proper contents of CuS@Xylan NPs in the composite papers (≥1.3 mM) could guarantee good NIR laser-inducible antimicrobial effect. The second parameter that we optimized was the irradiation power of NIR laser. The five identical pieces of the composite papers (CuS@Xylan NPs concentration of 1.3 mM) were attached onto the agar plate inoculated with Stapylococcus aureus, irradiated with different NIR laser power densities (0.1, 0.5, 1.0, 1.5, and 2.0 W/cm2) for 2 min. After incubation, the sizes of antimicrobial circles were significantly larger with NIR laser irradiation power densities of 2652

DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655

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ACS Sustainable Chemistry & Engineering 1.5 and 2.0 W/cm2 than those with power densities of 0.1, 0.5, and 1.0 W/cm2 (Figure 5c and d, p < 0.01), indicating that overly low NIR laser irradiation power ( Escherichia coli > Stapylococcus aureus > Aspergillus niger. Overall, the composite paper shows strong NIR laser-inducible ablation effects on all microorganisms tested, including Gram-positive bacteria and Gram-negative bacteria, as well as fungus, which potentially allow it to be a novel type of efficient and powerful surface bacteriostats. Therefore, this composite paper has potential for skin wound infection prevention. Mechanics of CuS@Xylan NPs/CNF Composite Papers. The mechanical properties of the CuS@Xylan NPs/CNF composite papers are crucial for their applications. Typically pure CNF papers already possess excellent physical strength,57 which, however, were expected to undergo further enhancement by the introduction of CuS@Xylan NPs. Therefore, we further investigated the effect of CuS@Xylan NP infiltration on the physical strengths of the CNF-based papers. The tensile strength, tear strength, bursting strength, and tensile test of the composite papers with different concentrations of CuS@Xylan NPs are shown in Figure 7. With the introduction of CuS@ Xylan NPs, the tensile index (Figure 7a), tear index (Figure 7c), and bursting index (Figure 7d) of the composite papers all increased by ∼50% and higher concentration of NPs resulted in more enhancement of the physical strength of the composite papers (p < 0.01). In a 15 N tension, the pure CNF paper note (without CuS@Xylan NPs) undergoes fracture, while the composite paper note (with 1.3 mM CuS@Xylan NPs) is intact 2653

DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655

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ACS Sustainable Chemistry & Engineering

(2015ZD03), and Natural Science Foundation of Guangdong Province (No. 2014A030313252).



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Figure 7. Effect of concentrations of CuS@Xylan NPs on (a) tensile index, (c) tear index, and (d) bursting index of CuS@Xylan NPs/CNF composite papers. (b) Tensile test of composite paper note (15 mm width, the right) and pure CNF paper note (15 mm width, the left) with 15 N of tension. Note: Basis weight of paper sheets was 40 g/m2; the tensile index, tear index, and burst index were calculated according to the standards of ISO 1924, ISO 1974, and ISO 2758. * indicates p < 0.05.

(as shown in Figure 7b). The improved mechanics of the composite papers might be attributed to the fact that the CuS@ Xylan NPs filling the tiny gap of CNF network could lead to the formation of denser networks (as confirmed in Figure 4). Moreover, the hydrogen bonds that could have formed between CNF and xylan would also benefit the structural stability of the composition between CuS@Xylan NPs and CNFs.



CONCLUSIONS In this study, a novel green synthesis method for CuS NPs was developed, where the nanoparticles were prepared in xylan solution at room temperature using copper−amine complex as the copper source and Na2S as the sulfide source, in which xylan molecules acted as the growth template and stabilizing agent. Spherical CuS@Xylan NPs were well dispersed with an average diameter of ∼10 nm. After infiltrating CuS@Xylan NPs into CNF networks, the composite papers not only possessed strong NIR laser-inducible antimicrobial property but also obtained improved mechanical strength of the papers. This work provided a novel strategy to prepare stable and uniform CuS NPs and the fabrication of a new prototype of NIR laser-inducible antimicrobial paper, which has a potential to be applied to skin wound infection prevention for rapid wound healing.



REFERENCES

AUTHOR INFORMATION

Corresponding Authors

*Tel. and Fax: +86-020-87111861. E-mail address: xyw@scut. edu.cn (X.W.). *E-mail address: [email protected] (Y.S.Z.). ORCID

Xiaoying Wang: 0000-0002-9303-6509 Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (Nos. 31622044 and 51403069), the State Key Laboratory of Pulp & Paper Engineering 2654

DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655

Research Article

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DOI: 10.1021/acssuschemeng.6b03003 ACS Sustainable Chem. Eng. 2017, 5, 2648−2655