Ag2S@WS2 Heterostructure for Rapid Bacteria-Killing Using Near

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Ag2S@WS2 Heterostructure for Rapid Bacteria-Killing Using Near-Infrared Light Yunfan Lin, Donglin Han, Yuan Li, Lei Tan, Xiangmei Liu, Zhenduo Cui, Xianjin Yang, Zhaoyang Li, Yanqin Liang, Shengli Zhu, and Shuilin Wu ACS Sustainable Chem. Eng., Just Accepted Manuscript • DOI: 10.1021/ acssuschemeng.9b03287 • Publication Date (Web): 16 Aug 2019 Downloaded from pubs.acs.org on August 17, 2019

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ACS Sustainable Chemistry & Engineering

Ag2S@WS2 Heterostructure for Rapid Bacteria-Killing Using Near-Infrared Light Yunfan Lin,† Donglin Han,‡ Yuan Li,‡ Lei Tan,† Xiangmei Liu,*,† Zhenduo Cui,‡ Xianjin Yang,‡ Zhaoyang Li,‡ Yanqin Liang,‡ Shengli Zhu,‡ Shuilin Wu*,†,‡ † Hubei Key Laboratory of Polymer Materials, Ministry-of-Education Key Laboratory for the Green Preparation and Application of Functional Materials, School of Materials Science & Engineering, Hubei University, NO. 368 Youyi Avenue, Wuchang District, Wuhan 430062, China ‡ School of Materials Science & Engineering, the Key Laboratory of Advanced Ceramics and Machining Technology by the Ministry of Education of China, Tianjin University, NO. 91 Weijin road, Nankai District, Tianjin 300072, China

* Corresponding Authors Xiangmei Liu. E-mail: [email protected]; Shuilin Wu. E-mail: [email protected]; [email protected]

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ABSTRACT: On a global scale, bacterial infection has been becoming a huge treat to human health. Taking into consideration the increasing drug-resistance bacteria, it is urgent to develop novel non-antibiotics strategies to kill bacteria rapidly. Herein, Ag2S@WS2 was developed as a new kind of antibacterial agents, where exfoliated WS2 nanosheets were decorated with Ag2S nanoparticles through in-situ growth. Under near-infrared (NIR) light irradiation (808 nm), the tight contact between Ag2S and WS2 endowed the composite with outstanding photocatalytic property, which was attributed to effective separation of photoactivated electronics and holes. Because of the synergistic effect of photocatalytic and photothermal properties, highly effective antibacterial efficacy could be achieved for Ag2S@WS2 within 20 min NIR light irradiation, i.e., 99.93% towards Staphylococcus aureus and 99.84% towards Escherichia coli. Moreover, the in vitro cell culture test showed that the synthesized Ag2S@WS2 was non-cytotoxic. These results demonstrate that Ag2S@WS2 can be a promising material for rapid and highly effective disinfection under NIR irradiation.

KEYWORDS:

Antibacterial;

Photocatalysis;

Photodynamic; Photothermal


Ag2S;

WS2

nanosheets;

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INTRODUCTION Bacterial infection could cause a large amount of troubles, ranging from the unsuccessful wound healing after surgery1,

2

to the failure of bone repair or

reconstruction after implantation.3 The patients suffer from much pain and even life-threatening due to bacterial infection. In order to kill bacteria effectively, antibiotics have been widely used in a large amount,4 which prompts the development of drug resistance bacteria, and finally inducing no drugs to use.

5-7

So developing

some new, rapid and effective disinfection strategies have become increasingly important and urgent.8, 9 In recent years, the optical technology is developing rapidly and it has been utilized in several biomedical fields such as imaging and therapy.10-12 Compared with traditional therapy, phototherapy has the advantage of non-destructive feature.13,

14

Photodynamic therapy (PDT) and photothermal therapy (PTT), as typical phototherapies, have shown great potential for treatments for cancer15,16 and bacterial infection.17-19 For the PDT, the therapy depends on the reactive oxygen species (ROS) consisting of ·O2−, 1O2 and OH ∙ . These active substances can be usually produced through the reactions between photogenerated carriers and the molecules in environment, including O2 and H2O.20-23 ROS can directly destroy bacterial membrane structure to kill germs.24,

25

And for PTT, it mainly depends on the

hyperthermia produced from photothermal agents to kill the germs when the agents are exposed to light, i.e., near-infrared light (NIR).26, 27 In general, large amount of ROS or high temperature can induce bacterial death.24-27 However, the high 3 ACS Paragon Plus Environment


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temperature with a long therapeutic time is harmful to normal cells and tissues because of the possible empyrosis. Therefore, it is necessary to kill bacteria under moderate temperature about 50 oC. Considering the lower efficiency of PTT at lower temperature, PDT is often introduced simultaneously for a better antibacterial efficacy.28 There exist lots of photothermal agents such as carbon matrix materials,29,30 gold nanoparticles (Au NPs),31 copper sulfide (CuS),32 etc. Among them, the silver sulfide (Ag2S) attracted much attention because it owns PTT and PDT properties simultaneously.33-35 Ag2S has a narrow bandgap of around 1.0 eV, making it well photocatalyst under visible and NIR light. For this reason, Ag2S has been paid much attention as an excellent photocatalyst so that it has been utilized in several areas including H2 evolution,36 organic pollution degradation37, 38 and biological imaging.39 However, the instantaneous electron-hole pairs recombination weakens photocatalytic property of materials, thus reducing yields of ROS significantly and consequently restricting its practical application. To overcome this drawback, a co-catalyst could be introduced to accelerate the transfer of carriers to slow the recombination. Although some other two-dimensional materials, i.e., graphene oxide,

40

and graphitic carbon

nitride,41 could be generally used as co-catalyst materials, they could not form tight heterointerface with Ag2S because of their different structures. Tungsten disulfide (WS2) could easily form tight bonding with Ag2S, because they are both metal sulfide. In addition, as a type of layered transition-metal dichalcogenide, WS2 manifests excellent photo-electric properties.42,

43

Therefore, it is possible for WS2 to be the 4

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promising co-catalyst of Ag2S by in-situ growth process. In this work, the heterostructure of Ag2S@WS2 was fabricated, which exhibited excellent photocatalytic and photothermal performances, thus achieving high antibacterial-efficacy with moderate temperature under NIR light irradiation. During the fabrication process, WS2 was initially exfoliated through ultrasound to form WS2 nanosheets, which could subsequently support the in-situ growth of Ag2S nanoparticles (NPs) through a mild solution method. Afterwards, the Ag2S NPs were dispersed on the surface of WS2 to construct the heterojunction. In Scheme 1, this process was schematically illustrated. The antibacterial activity, cytocompatibility, photocatalytic and photothermal properties of Ag2S@WS2 were investigated systematically.

Scheme 1 The schematic illustration of the preparation process of Ag2S@WS2 composite.

EXPERIMENTAL SECTION Characterization. The surface morphologies and microstructures were determined by scanning electron microscopy (SEM, JSM7100F, JEOL, JP) equipped with 5 ACS Paragon Plus Environment


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energy-dispersive spectroscopy (EDS) and transmission electron microscope (TEM; JEM-2100F, JP). The elemental compositions were analyzed by X-ray photoelectron spectroscopy (XPS, ESCALAB 250Xi, Thermo Scientific, USA). To investigate phase structures, X-ray diffractometry (XRD, D8A25, Bruker, Germany) with Cu Kα radiation (λ = 0.15406 nm) was utilized to record the diffraction angle (2θ) ranging from 10 to 80° with the step size of 0.02°. Ultraviolet visible (UV-vis) absorption was examined

by

a

UV-Vis

spectrophotometer

(UV-3600,

Shimadu,

JP).

Photoluminescence (PL) measurements were performed by a fluorescence spectrometer (LS-55, PE, USA). LOS-BLD-0808 was used as the laser source in this work. Exfoliation of Layered WS2 Nanosheets. The exfoliation of layered WS2 nanosheets was on the basis of previously reported method.44 Briefly, 30 mg of the purchased WS2 powders were added to 10 mL mixture of 45 vol% ethanol/deionized (DI) water. The solution was sonicated for 8 h and centrifuged at 3000 rpm for 20 min to eliminate aggregations. Afterward, the supernatant was collected. Synthesis of Hierarchical Ag2S@WS2 Composites and Pure Ag2S NPs. After 0.15 g thiourea (Tu) was dissolved in 10 mL deionized (DI) water, 10 drops ammonia (7%) was added to provide an alkaline environment. The exfoliated WS2 nanosheets were diluted to 10 mL by DI water according to different weight ratio of WS2 to Ag2S (10%, 20%, and 30%). After 10 mL WS2 supernatant was added to Tu solution, the mixtures were under moderate stir for 10 min, and followed by slowly dripping 10 mL 0.3 M AgNO3 solution to trigger the reaction. The reaction lasted for 20 min at 6 ACS Paragon Plus Environment

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room temperature. Composites were subsequently collected by centrifugation, followed by being washed by DI water and ethanol for three times, respectively, and samples were finally dried at 60 oC. To obtain pure Ag2S NPs, except that 10 mL diluted WS2 nanosheets solution was replaced by 10 mL DI, the whole synthesis process was the same as before. During the process of 20 min reaction, the color turned from light brown to deep black, indicating the successful synthesis of Ag2S NPs. Photothermal Effects. In the EP tubes, four samples (phosphate buffered saline (PBS), Ag2S, WS2 and Ag2S@WS220% ) at the concentration of 200 μg/mL were respectively lighted under NIR light (1 W/cm2) for 10 min. Meanwhile, a thermal imager was used to record temperature every 30 s. The heating-cooling curves of Ag2S@WS220% were recorded under the same conditions for three cycles. Besides, the photothermal conversion efficiency (ƞ) of Ag2S@WS220% was calculated by referring to the reported method as the following equation.45 ƞ=

hA(T𝑚𝑎𝑥 ― T𝑎𝑚𝑏) ― Q0 I(1 ― 10

― 𝐴𝜆

)

(1)

In Equation (1), h stands for the heat transfer coefficient, and A denotes the heated surface area. Tmax and Tamb represent the maximum of temperature and environment temperature, respectively. Q0 is the heating absorption of the container (EP tube in this work). Also, the light power (1 W/cm2) is indicated by I. The 𝐴𝜆 is the 808 nm absorbance intensity while 𝜆 is the wavelength (808 nm). τ=

m0c0

(2)

hA

Equation (2) illustrates the relationship between τ (the time constant quantity) and 7 ACS Paragon Plus Environment


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hA, where 𝑚0 and c0 are constants on behalf of the mass and the heat capacity of DI water used for solving samples. To determine the value of τ, Equation (3) is introduced. T ― T𝑎𝑚𝑏

t = ―τln (θ) = ―τlnT𝑚𝑎𝑥 ― T𝑎𝑚𝑏

(3)

In the cooling process, according to the linear regression curve, τ can be calculated by Equation (3). Reactive Oxygen Species (ROS) Detection. 2′,7′-dichlorofluorescein diacetate (DCFH-DA), which is an oxidation-sensitive fluorescent dye, was utilized as ROS fluorescent probe to reflect the total quantity of ROS generated by samples under 808 nm laser irradiation. After combining with ROS, DCFH could be converted into 2′,7′-dichloro-fluoresce (DCF). The microplate reader (SpectraMax I3, MD, USA) detected the fluorescence intensity of fluorescent DCF (the excitation wavelength 488 nm and absorption wavelength 525 nm), which could indicate the ROS generation. Briefly, 20 μL of 2 mg/mL samples (Ag2S, WS2, Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230%) were mixed with 180 μL DCFH in 96-well plates and the control group was 180 μL DCFH without samples. Each well was lighted by 808 nm laser for 20 min. During the process, the fluorescence intensity was recorded every 2 min intervals. Antibacterial Properties. The spread plate test was employed to investigate the antibacterial capacity in vitro. Firstly, 180 μL bacterial liquid of Staphylococcus aureus (S. aureus) or Escherichia coli (E. aureus) with the density of about 1 × 107 CFU/mL (colony-forming units per milliliter) was added to the 96-well plate. Then 20 8 ACS Paragon Plus Environment

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μL suspensions of 2 mg/mL samples (Ag2S, WS2 and Ag2S@WS220%) were added into wells. Each well was illuminated by NIR laser for 20 min or kept in the darkness for 20 min. In addition, the NIR light power was controlled in the range from 0.40 W/cm2 to 0.50 W/cm2 to keep the temperature at around 55 oC, thus avoiding high temperature. The bacterial solution with 20 μL PBS was served as the control group. For PTT group, the bacterial solution with Ag2S@WS220% was kept in the water bath at 55 oC for 20 min without light and for PDT group, the bacterial solution with Ag2S@WS220% was kept in the cold water bath under irradiation for 20 min to avoid warming. After NIR irradiation, the bacterial liquid was diluted about 100 fold, and 20 μL diluted liquid was dropped onto an agar plate and smeared by a glass spreader. All the agar plates were cultured at 37 oC for 1 day to record the number of bacterial colonies. Fluorescent-Based Bacterial Live/Dead Test. Fluorescent bacterial live/dead assay was utilized to further investigate the antimicrobial activity of samples. Three kinds of samples (Ag2S, WS2 and Ag2S@WS220%) (20 μL 2 mg/mL) were placed into wells containing 180 μL bacterial liquid (1 × 107 CFU/mL), and the wells were lighted by 808 nm laser for 20 min. The pure bacterial liquid without materials was selected as the control group. Next, each well was stained by the mixtures of two fluorescent dyes, SYTO9 and PI (LIVE/DEAD Baclight Bacterial Viability Kit, Beyotime, for microscopy & quantitative assays) for 15 min before being washed by PBS for three times. And the 96-well plate was stored in the darkness and observed by an inverted fluorescence microscope (IFM, Olympus, IX73). 9 ACS Paragon Plus Environment


Bacterial morphology observation. First, the glass sheets were settled on the wells. Then, 180 μL bacterial liquid (1 × 107 CFU/mL) and 20 μL suspensions of 2 mg/mL samples (Ag2S, WS2 and Ag2S@WS220%) were added into the wells. After 20 min NIR irradiation, the glass sheets with bacteria and samples were immersed in the glutaraldehyde (200 μL 2.5%) for 2 h, followed by being washed by PBS for three times. Afterward, glass sheets were dehydrated with alcohol (30%, 50%, 70%, 90%, and 100%) in the succession (15 min each). Finally, samples were dried and conserved for SEM observation. Cytocompatibility Evaluation. To probe into the cytocompatibility of composites, the cell toxicity assay was carried out. 3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyl tetrazolium bromide (MTT, Aladdin Reagent Co., China) was employed to investigate the cytocompatibility on MC3T3-E1 cells (WuHan Union Hospital). 180 μL of cell suspensions at the concentration of 1 × 104 cells/cm2 and 20 μL suspensions of 2 mg/mL samples (Ag2S, WS2 and Ag2S@ WS220%) were co-cultured on 96-well plate for 1, 3 and 7 days in an incubator (37 °C, 5% CO2), while cell medium was refreshed every 2 days. Then, 200 μL MTT solved in PBS (0.5 mg/mL) were added to continue culturing for another 4 h. After removing former cell medium, 200 μL Dimethyl sulfoxide (DMSO) were added into each group. Eventually, plates were evaluated by the microplate reader (SpectraMax I3 MD USA) to survey optical density (OD) on wavelength of 490 nm and 570 nm. Cell Morphology. Similar to the MTT test, 180 μL of cell suspensions (1 × 104 cells/cm2) and 20 μL suspensions of 2 mg/mL samples (Ag2S, WS2 and 10 ACS Paragon Plus Environment

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Ag2S@WS220%) were initially cultivated together for 1 day in an incubator. One day later, the medium was extracted and wells were washed by PBS, then fixed by 4 % formaldehyde (Sinopharm Chemical Reagent Co., China) for 10 min. Next, samples were stained by FITC for 40 min, avoiding the light. After being rinsed by PBS, samples were then stained by DAPI (YeaSen, China) for 30 s. Finally, after removing the liqud, the samples were reserved at 4 oC for further investigation by fluorescence microscopy (IFM, Olympus, IX73).

RESULTS AND DISCUSSION Morphology and Structure. The concise preparation process of the composite was presented in Scheme 1. Ag2S@WS2 was fabricated via a traditional solution method. The exfoliated WS2 nanosheets with various weight reacted with thiourea and AgNO3 solution, and the products were named as Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230%, respectively, according to the weight ratio between Ag2S and WS2 (9:1; 8:2, and 7:3). Figure 1a and Figure 1b showed the morphologies of pure WS2 nanosheets and Ag2S NPs, respectively. Obviously, the pure WS2 nanosheets showed smooth surface and the Ag2S NPs exhibited conglobate structure. After loading with Ag2S NPs, WS2 nanosheets were densely covered with sphere-like NPs (Figure 1c). The EDS pattern in Figure 1c1 showed that the content of Ag, W and S was 14.25 at.%, 39.04 at.% 46.71 at.%, respectively. The elemental mapping revealed the homogeneous distribution of Ag (Figure 1c2), W (Figure 1c3) and S (Figure 1c4) in the composite. 11 ACS Paragon Plus Environment


In Figure 1d, TEM image disclosed the nanosheet-like structure of the exfoliated WS2, which was in conformity with SEM result in Figure 1a. Figure 1e displayed the aggregated Ag2S NPs, which was in accordance with the SEM observation in Figure 1b. Figure 1f exhibited the microstructure of Ag2S@WS2 hybrid, in which numerous NPs covered the nanosheets. This hybrid was schematically illustrated by Figure 1g. As shown in Figure 1h, high-resolution TEM (HRTEM) detected a 0.618 nm lattice fringe from the prepared nanosheets, which belonged to the typical (002) plane of WS2 (JCPDS no.08-0237). It was seen from Figure 1i that the detected crystalline planes (-112) from prepared NPs corresponded to the lattice fringes of 0.283 nm of Ag2S (JCPDS no.14-0072). The HRTEM image obtained from the prepared Ag2S@WS2 (Figure 1j) detected the tight interfacial contact between WS2 and Ag2S, indicating an intimate heterojunction between WS2 nanosheets and Ag2S NPs. The corresponding crystal structures of Ag2S and WS2 were illustrated in Figure 1k, showing the lattice plane from Ag2S (-112) and WS2 (002) schematically.


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Figure 1. SEM images of (a) WS2 nanosheets, (b) Ag2S, and (c) Ag2S@WS2 composite (Ag2S@WS220%); (c1) EDS detection of Ag2S@WS2 composite (Ag2S@WS220%); Element mappings of Figure 1c ((c2): Ag, (c3): W and (c4): S); TEM images of (d) WS2 nanosheets, (e) Ag2S, (f) Ag2S@WS2 composite (Ag2S@WS220%); (g) The morphology illustration of Ag2S@WS2 composite; HRTEM images of (h) WS2 nanosheets, (i) Ag2S, (j) Ag2S@WS2 composite (Ag2S@WS220%); (k) Crystal structure of WS2 and Ag2S.

XRD and XPS Analysis. XRD was utilized to further verify the composition and structure of the synthesized materials. Figure 2a illustrated that exfoliated WS2 (JCPDS no.08-0237) exhibited nine peaks at 14.3o, 28.8o, 32.7o, 33.5o, 39.5o, 43.9o, 49.6o, 58.3o, 59.8o, corresponding to the crystal faces of (002), (004), (100), (101), (103), (006), (105), (110), (110) and (112). As for the pure Ag2S (JCPDS no.14-0072), diffraction planes (-111), (111), (-112), (120), (-121), (-103), (031) and (200) were 13 ACS Paragon Plus Environment


indexed by the peaks at 26.0o, 29.0o, 31.5o, 33.6o, 34.4o, 37.7o, and 40.8o.46 In the case of as-prepared Ag2S@WS2 samples, the curves exhibited almost the same pattern as that of the pure Ag2S, which should be ascribed to the high content of Ag2S on the surface of the composite. Meanwhile, the comparative lower peaks of composite at 14.3o also demonstrated the existence of diffraction plane (002) of WS2. Compared with pure Ag2S, the typical peaks of samples did not change, suggesting that the in situ growth on WS2 nanosheets did not change the phase structure of Ag2S. The full-scale XPS spectrum of the sample (Ag2S@WS220%) was shown in Figure 2b, indicating that the synthesized materials mainly contained Ag, W and S elements. It was found that two peaks situated at 368.2 eV and 374.2 eV in Figure 2c were Ag 3d3/2 and Ag 3d5/2.47 Furthermore, no other peaks were observed in Figure 2c, indicating that there were no other states of Ag except Ag+.48 Figure 2d reflected the binding energy of W 4f7/2 and W 4f5/2 peaking at 33.0 eV and 35.2 eV, while the peak at 38.0 eV was related to W 5p3/2.49, 50 Figure 2e showed the high-resolution XPS spectrum of S 2p, which can be divided into four peaks. Two higher peaks at 161.5 eV and 162.7 eV belonged to sulfur anions of Ag2S, indicating S 2p3/2 and S 2p1/2 respectively.47 With regard to another two peaks at 162.8 eV and 163.9 eV, they were the typical peaks of WS2 (S 2p3/2 and S 2p1/2).50


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Figure 2. (a) XRD patterns of Ag2S, WS2, Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230%; (b) The XPS survey spectrum of Ag2S@WS2 composite (Ag2S@WS220%); high-resolution XPS spectra of (c) Ag 3d, (d) W 4f and (e) S 2p obtained from Ag2S@WS2 composite (Ag2S@WS220%).

UV-vis Spectra and Photoluminescence Analysis. In Figure 3a, the UV-vis spectra (Ag2S, WS2, Ag2S@WS210%, Ag2S@WS220%, and Ag2S@WS230%) were shown. All the samples showed a large region of absorption from 400 to 1200 nm. Besides, compared with the pure Ag2S, the light absorption was dramatically enhanced after mixing with appropriate weight ratio of WS2, without any shift in spectra. There was a peak around 800 nm in all the curves, indicating its remarkable 15 ACS Paragon Plus Environment


absorption in NIR region. And the UV-vis spectrum of Ag2S@WS210% was almost overlapped with that of the pure Ag2S, showing no significant improvement of absorption with 10% WS2. When the concentration of WS2 increased to 20%, the composite had the best absorbance in visible and NIR light region. However, if the weight ratio of WS2 reached up to 30%, the absorbance decreased. PL can reflect the recombination speed of photo-activated electron-hole pairs. As shown in Figure 3b, PL spectra (Ag2S, Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230%) were exhibited. The pure Ag2S also showed the strongest PL spectrum with a small peak at 470 nm, indicating the strongest electron-hole pairs recombination. With the addition of WS2 nanosheets, the PL spectra were still similar to that of pure Ag2S, but the fluorescence quenching effect was observed. Ag2S@WS220% performed the strongest quenching, which was the evidence that Ag2S@WS220% was able to restrain the recombination rate of photo-activated carriers..51,

52

Thus, WS2 nanosheets could separate the carriers from Ag2S NPs to

improve the photocatalytic activity.

Figure 3. (a) UV–vis diffuse reflectance spectra of Ag2S, WS2, Ag2S@WS210%, 16 ACS Paragon Plus Environment

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Ag2S@WS220% and Ag2S@WS230%; (b) PL spectra of Ag2S, Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230%.

ROS Detection and Photothermal Effects. The antibacterial ability of photodynamic agents depends on the yields of ROS.53-55 ROS including OH∙, 1O2, and O2− is a type of unique active substance, which can kill bacteria by distorting the oxygen balance inside the cells. Once photogenerated electrons or holes are captured by O2 and H2O in the environment, ROS may be created.20 Dichlorofluorescein diacetate (DCFH-DA), a kind of ROS sensitive sensor, is generally used for ROS detection, thus evaluating the photocatalytic property of samples. From the results in Figure 4a, it was apparent that ROS yields increased after loading the Ag2S NPs on the surface of WS2 nanosheets after 20 min NIR irradiation. Among those samples, Ag2S@WS220% owned the highest ROS yield, demonstrating the best photocatalytic property, which was consistent with the PL results, which was ascribed to the fact that WS2 nanosheets was acted as the platforms to capture photogenerated electrons so that the charge transfer between two materials prolonged the lifespan of carriers. The bandgap energy of Ag2S was 0.84 eV so that Ag2S was easily activated under NIR irradiation. Although WS2 could be activated by NIR light, but ROS yield generated by WS2 was insufficient to kill bacteria. The conduction band (CB)/valence band (VB) potentials of Ag2S and WS2 were −0.41 /+0.43 eV vs NHE and -0.12/+1.18 eV vs NHE.56,

57

Once carriers were produced under NIR irradiation, the heterostructure

between Ag2S and WS2 accelerated the transfer of photogenerated electrons form 17 ACS Paragon Plus Environment


Ag2S to WS2, consequently producing more ROS and Figure 4b was the illustration of mechanism. During the irradiation period with 808 nm light, the photothermal capability of samples (Ag2S, WS2, and Ag2S@WS220%) were studied by recording the temperature every 30 s. In Figure 4c, the temperature change of the control group (PBS without samples) was not obvious and pure WS2 exhibited a very weak photothermal ability reaching about 30 oC. In addition, although the final temperature of both Ag2S and Ag2S@WS220% reached up to 60 oC with 10 min irradiation, the Ag2S@WS220% performed better photothermal effect, which was ascribed to the strongest NIR light absorbance (Figure 3a). The rising and cooling curves of Ag2S@WS220% were shown in Figure 4d, there were almost no change after three cycles, suggesting that the Ag2S@WS220% had an excellent photo-stability, which would be further proven in the next section.. The linear regression curve calculated from cooling curves was shown in Figure 4e. Eventually, when the τ was 346.77 s, the obtained photothermal conversion efficiency η was 33%.


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Figure 4. (a) ROS production from PBS, Ag2S, WS2, Ag2S@WS210%, Ag2S@WS220% and Ag2S@WS230% detected by DCFH under NIR (808 nm) irradiation; (b) The mechanism diagram of ROS generation after combining Ag2S and WS2 under 808 nm irradiation; (c) Photothermal curves of PBS, Ag2S, WS2, and Ag2S@WS220% under NIR (808 nm) irradiation (1 W/cm2); (d) Heating-cooling curve of Ag2S@WS220% for three cycles under on/off NIR (808 nm) irradiation; (e) Linear regression curve of cooling part from Ag2S@WS220%.

In Vitro Antibacterial Activity. In vitro antibacterial test was investigated by spread plate method. In view of the well photothermal ability and the ROS generation capability, Ag2S@WS220% was selected for further in vitro antibacterial test on behalf of hybrid group. During the irradiation, the temperature of both Ag2S and 19 ACS Paragon Plus Environment


Ag2S@WS220% were kept at 55 oC, while that of WS2 finally reached about 30 oC due to its poor photothermal effects. As shown in Figure 5a, the colonies number of both S. aureus and E.coli did not change without 808 nm irradiation for all the groups, which made it clear that all the samples did not have antibacterial capacity in the darkness. On the contrary, after irradiation, although the bacterial colonies number of the control groups and WS2 groups still remained stable, both Ag2S and Ag2S@WS220% exhibited an evident antibacterial activity. Under the NIR irradiation, pure Ag2S could exhibit both photothermal and photodynamic effect to some extent. Though these effects from Ag2S were not as strong as those of composites, it also killed some part of the germs.28 The single antibacterial efficacy by PTT or PDT was approximately 45% and 53%, respectively (Figure S1). In Figure 5b, the antibacterial efficiency was calculated and WS2 group showed almost no antibacterial ability. Ag2S exhibited excellent antibacterial efficacy towards E.coli with 90.33% but much lower efficiency of 36.18% against S. aureus, which may result from the distinction of the structure between this two germs.58-60 In addition, Ag2S@WS220% showed remarkable antibacterial efficacy against both kind of bacteria trigged by NIR light, which may thank to its outstanding photocatalytic and photothermal performance. The average antibacterial efficacy of Ag2S@ WS220% reached up to 99.93% towards S. aureus and 99.84% towards E. coli. To further investigate the antibacterial effect, fluorescent test was used with a visible cell live/dead staining, in which the live germs were stained in green and other dead germs were painted in red. After NIR irradiation, both the control and WS2 20 ACS Paragon Plus Environment

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groups exhibited almost green spots on the whole surface shown in Figure 5c, indicating no antibacterial activity of these two kinds of groups. In the case of Ag2S, a large amount of red spots appeared on the entire surface with few remaining green spots, indicating strong antibacterial efficiency towards E.coli under NIR irradiation. In contrast, as for Ag2S@WS220% group, almost no green spots existed on the surface, suggesting the death of almost all bacteria, which revealed that Ag2S@WS220% group had the best antibacterial efficacy regardless of S. aureus or E.coli. As shown in Figure 5d, surface morphologies of germs (S. aureus and E.coli) were exhibited. There was no obvious morphologic change towards two types of germs on WS2 group. The membrane of E.coli from Ag2S group was deformed to some extent, which was corresponding with its antibacterial effect towards E.coli (90.33%). Serious damage of membrane for two types of bacteria was observed on Ag2S@WS220% group, indicating its more effective bacteria-killing ability. Both staining images and bacterial morphologies were consistent with the aforementioned spread plate results.



Figure 5. (a) Antibacterial capability of samples analyzed by Spread plate method after 20 min NIR lighting and non-lighting; (b) The antibacterial ratios of S. aureus and E. coli after 20 min irradiation (n = 3, mean ± SD: *p < 0.05, **p < 0.01, ***p < 0.001); (c) Live/dead bacteria staining images of S. aureus and E. coli (scale bars = 50 μm); (d) SEM images of bacterial morphology from different samples (control, WS2, Ag2S and Ag2S@WS220%) after irradiation.

In Vitro Cytotoxicity Evaluation. The cytocompatibility of PBS (Control group), 22 ACS Paragon Plus Environment

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WS2, Ag2S and Ag2S@WS220% was investigated by MTT assay for 1, 3 and 7 days. Figure 6a showed that pure Ag2S exhibited the best cell viability around 90% compared with WS2 and Ag2S@WS220% during all the culturing periods. The pure WS2 showed a slightly lower cell viability, especially after 7 days. However, after loading the Ag2S NPs, the cell viability of Ag2S@WS220% was improved compared to pure WS2, which was resulted from the fact that the Ag2S NPs covering hindered the contact between WS2 and cells. During a long-term co-culturing, cell behaviors including adhesion, spreading, and proliferation were influenced by surrounded NPs, which hindered the cell growth compared with the control group. Consequently, several days later, differences in cell number appeared. Finally, the cell viability of Ag2S@WS220% was around 80% after 7 day. The cell fluorescence images that can reflect the growth, extension, spreading and proliferation behaviors, were displayed in Figure 6b. FITC (Red) and DAPI (blue) were utilized to visualize the F-action and nuclei, respectively. Compared with cells on WS2 samples, cells co-cultured with Ag2S and Ag2S@WS220% exhibited polygonal morphologies, indicating the better cell growth on Ag2S and Ag2S@WS220% than the one on WS2.



Figure 6. (a) MTT test of MC3T3-E1 cell co-culturing with samples for different days (n = 3, mean ± SD: *p < 0.05, **p < 0.01, ***p < 0.001); (b) Fluorescence staining of Control, Ag2S, WS2, Ag2S@WS220% after co-culturing with cells for 1 day (scale bars = 50 μm).

CONCLUSIONS In this work, Ag2S@WS2 composite was synthesized by a simple solution method at room temperature, in which pre-exfoliated WS2 nanosheets were utilized as the 24 ACS Paragon Plus Environment

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precursor. After loading with Ag2S NPs, the heterostructure between Ag2S NPs and WS2 nanosheets accelerated the electron mobility and restrained the photogenerated electron-hole pairs recombination. Therefore, the photocatalytic properties of the composite can be dramatically improved to generate ROS under 808 nm irradiation via prolonging the lifespan of photogenerated carriers. This NIR-inspired photocatalytic property endowed the composite an enhanced antibacterial efficacy of 99.93% and 99.84% against S. aureus and E.coli, respectively. Besides, this Ag2S@WS2 exhibited better biocompatibility towards MC3T3-E1 cells, compared with pure WS2. In summary, this heterostructure system would be a promising bio-platform for rapid and safe disinfection.

ASSOCIATED CONTENT Supporting Information Antibacterial efficiency of different methods (photothermal, photodynamic and synergistic effect)

AUTHOR INFORMATION Corresponding Author *X. L. E-mail: [email protected]. Tel: +86-027-15972929178 *S. W. E-mail: [email protected]; [email protected]. Tel: +86-027-13720190755

ORCID 25 ACS Paragon Plus Environment


Shuilin Wu: 0000-0002-1270-1870

Notes The authors declare no conflict of interest to this work.

ACKNOWLEDGEMENTS This work is jointly supported by the Natural Science Fund of Hubei Province, 2018CFA064, National Natural Science Foundation of China, Nos. 51671081, 51871162, 51801056 and 51422102, and the National Key R&D Program of China No. 2016YFC1100600 (sub-project 2016YFC1100604).

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Table of contents (TOC) graphic

Synopsis Ag2S nanoparticles decorated WS2 system generates ROS and heat to kill bacteria in a short period under NIR irradiation.


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Ag2S@WS2 Heterostructure for Rapid Bacteria-Killing Using Near

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