Liquid Exfoliation of Atomically Thin Antimony Selenide as an Efficient

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Biological and Medical Applications of Materials and Interfaces

Liquid Exfoliation of Atomically Thin Antimony Selenide as An Efficient 2D Antibacterial Nanoagent Zhaohua Miao, Linxin Fan, Xianli Xie, Yan Ma, Jingzhe Xue, Tao He, and Zhengbao Zha ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b08320 • Publication Date (Web): 09 Jul 2019 Downloaded from pubs.acs.org on July 17, 2019

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ACS Applied Materials & Interfaces

Liquid Exfoliation of Atomically Thin Antimony Selenide as An Efficient 2D Antibacterial Nanoagent Zhaohua Miao,†, ‡, # Linxin Fan,†, # Xianli Xie,† Yan Ma,† Jingzhe Xue,§ Tao He*, † and Zhengbao Zha*, † †

School of Food and Biological Engineering, School of Chemistry and Chemical Engineering,

Hefei University of Technology; Hefei 230009, P.R. China. ‡ State

Key Laboratory of Advanced Welding and Joining, Harbin Institute of Technology,

Harbin, 150001, P. R. China. §

Department of Chemistry, University of Science and Technology of China, Hefei 230026, P.R.

China. #. These authors contribute equally to this work. *. Corresponding authors. E-mail: [email protected], [email protected] KEYWORDS: antimony selenide; antibacterial nanoagent; photothermal effect; multidrugresistant; two-dimensional materials

ABSTRACT: The ever-growing global crisis of multidrug-resistant (MDR) bacteria has triggered a tumult of activity in the design and development of antibacterial formulations. Here, atomically thin antimony selenide nanosheets (Sb2Se3 NSs), a minimal-toxic and low-cost

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semiconductor material, was explored as a high-performance two-dimensional (2D) antibacterial nanoagent via a liquid exfoliation strategy integrating cryo-pretreatment and PVP-assisted exfoliation. When cultured with bacteria, the obtained PVP-capped Sb2Se3 NSs exhibited intrinsic long-term antibacterial capability, probably due to the reactive oxygen species generation and sharp edge-induced membrane cutting during physical contact between bacteria and nanosheets. Upon near-infrared laser irradiation, Sb2Se3 NSs achieved short-time hyperthermia sterilization owing to strong optical absorption and high photothermal conversion efficiency. By virtue of the synergistic effects of these two broad-spectrum antibacterial mechanisms, Sb2Se3 NSs exhibited high-efficiency inhibition of conventional Gram-negative Escherichia coli (E. coli), Gram-positive methicillin-resistant Staphylococcus aureus (MRSA), and wild bacteria from a natural water pool. Particularly, these three categories of bacteria were completely eradicated after treated with Sb2Se3 NSs (300 µM) plus laser irradiation for only 5 min. In vivo wound healing experiment further demonstrated the high-performance antibacterial effect. In addition, Sb2Se3 NSs depicted excellent biocompatibility due to the biocompatible element constitute and bioinert PVP modification. This work enlightened that atomically thin Sb2Se3 NSs hold great promise as a broad-spectrum 2D antibacterial nanoagent for various pathogenic bacterial infections.

INTRODUCTION The rapid evolution of pathogenic bacteria, especially multidrug-resistant (MDR) bacteria, is an ever-growing global crisis in the fields of medicine, food and environment, and thus has triggered a tumult of activity in the design and development of novel antibacterial formulations, which are generally categorized as organic or inorganic.1-5 Organic antibacterial agents like


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antibiotics are the most widely used, but the abuse of antibiotics is easy to induce the emergence and spread of drug-resistant bacteria.6-8 What’s worse, many organic antibacterial agents suffered from several shortcomings such as short life expectancy, high decomposability and low heat resistance, which have limited their applications in some cases.9,10. Therefore, much attention has been paid to inorganic antibacterial agents due to their broad-spectrum and long-term bactericidal activity, in which silver-containing materials are a typical representative.11,12 However, silver ions were easily reduced to metallic silver under light irradiation or high temperature, causing the discoloration of samples.13 In this regard, several other inorganic antibacterial agents, such as zinc oxide (ZnO)14, copper oxide (CuO)14,15 and carbon nanomaterials16-18, have been explored as effective antibacterial agents for various proposes in different fields. Among these inorganic antibacterial agents, two-dimensional (2D) materials with the thickness of atomic layer have received considerable attention recently.3,19 Distinctive from bulk materials, atomically thin 2D materials possess some intriguing properties, such as sharp edge, large surface area and abundant active sites, and thus exhibit a discrepant antibacterial mechanism from other antibacterial agents, which is mainly ascribed to the reactive oxygen species (ROS) generation or sharp edge-induced membrane cutting during physical contact with bacteria.20-22 To be noted, unlike antibiotics, 2D materials are amenable to combat MDR pathogens without the concern of drug resistant due to the physical antibacterial mechanism.23 The first example of 2D materials for combating pathogenic bacteria is graphene. It is reported that graphene nanosheets were able to insert/cut and extract the cell membranes of E. coli, causing many phospholipids were extracted from their cell membranes.2 Another typical example is 2H-MoS2 nanosheets. Thiolated ligands functioned MoS2 nanosheets were reported to


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exhibit high-performance antibacterial efficiency by the generation of large amounts of ROS very recently.24 Apart from these, some other 2D materials including MXene25, carbon nitride26 and black phosphorus nanosheets27 were also explored as antibacterial agents one after another. However, the intrinsic antibacterial activity of most 2D materials is generally limited, and long time or high dosage is required for achieving effective sterilization.27,28 Hence, it is urgent and significative to develop novel 2D antibacterial agents with high-performance sterilization capacity. Antimony selenide (Sb2Se3), a new member to the anisotropic 2D material family, has recently regained interest because of intriguing physicochemical properties.29,30 It is composed of oriented one-dimensional covalently bonded (Sb4Se6)n ribbons. Benefiting from high responsivity and anisotropic in-plane transport, Sb2Se3 nanosheets (Sb2Se3 NSs) hold great potential for electronic devices.30 In addition, Sb2Se3 were explored as an excellent battery anode by virtue of high theoretical mass-specific energy capacity.31 Moreover, Sb2Se3 could also serve as photovoltaics attributing to the optimal bandgap of ∼1.1 eV and strong absorption coefficient.29 However, the biomedical application of Sb2Se3 NSs is rarely reported despite Sb2Se3 is generally considered to be minimal-toxic and low-cost, based on that element Sb with a similar cost to Cu has been used as antimonial drugs in medicine for more than one hundred and Se is a constituent of selenoproteins in vivo. Considering these, very recently we introduced Sb2Se3 NSs as a highperformance photothermal agent for tumor theranostics, which is the sole report about the biomedical application of Sb2Se3 NSs until now32. Hence, much attention should be paid to expand the scope of biomedical applications of Sb2Se3 NSs. In this study, we report that polyvinyl pyrrolidone (PVP)-capped Sb2Se3 NSs with ultrathin atomic thickness and strong absorption coefficient can be employed as a high-performance 2D


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antibacterial nanoagent based on the synergistic effects of intrinsic long-term antibacterial property and short-time hyperthermia sterilization under near-infrared (NIR) irradiation (Scheme 1a and 1b). A liquid exfoliation strategy integrating cryo-pretreatment and PVP-assisted exfoliation was adopted for high-efficiency exfoliation of atomically thin Sb2Se3 NSs. When cultured with bacteria, the obtained PVP-functioned Sb2Se3 NSs achieved high inactivation of not only conventional Gram-negative Escherichia coli (E. coli) but also Gram-positive methicillin-resistant Staphylococcus aureus (MRSA). In vivo experiment of wound healing further demonstrated the high-performance antibacterial effect of Sb2Se3 NSs. In addition, we proposed that the reactive oxygen species generation and sharp edge-induced membrane cutting

Scheme 1. Schematic illustration of atomically thin Sb2Se3 nanosheets as a high-performance 2D antibacterial nanoagent for combating conventional Gram-negative Escherichia coli but also Gram-positive methicillin-resistant Staphylococcus aureus. (a) Liquid exfoliation process; (b) Synergetic antibacterial mechanism.


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during physical contact may be responsible for the intrinsic antibacterial mechanism of Sb2Se3 NSs. Importantly, Sb2Se3 NSs depicted excellent biocompatibility due to the biocompatible element constitute and bioinert PVP molecule modification. Collectively, this novel 2D antibacterial nanoagent capable of intrinsic long-term antibacterial property and rapid photothermal killing capability is expected to be an alternative to antibiotics for combating drugresistant pathogenic bacteria. EXPERIMENTAL SECTION Chemicals Sb2Se3 powder were obtained from J&K Chemical Co.. PVP and NMP were purchased from Sinopharm

Chemical

Reagent

Co..

Stains

of

the

oxidant-sensitive

dye

2’,7’-

dichlorodihydrofluorescein diacetate (DCFH-DA), SYTO 9 and 3-(4,5-dimethyl-2-thiazolyl)2,5-diphenyl-2-H-tetrazolium bromide (MTT) were obtained from Thermo Fisher. Deionized water was supplied through a Milli-Q water system. Preparation of Atomically Thin Sb2Se3 NSs The preparation of atomically thin Sb2Se3 NSs was according to our previous report.32 Briefly, 100 mg of Sb2Se3 powders were pre-treated in liquid nitrogen for 60 min, followed by immediately ground for 40 min in an agate mortar. Then, the obtained Sb2Se3 powders, together with 200 mg of PVP, were co-added into 20 mL of NMP, and then were exfoliated under bath sonication for 2 h and probe sonication (600 W, 50%, period of 3 s with the interval of 3 s) for 2 h with ice bath, respectively. After centrifugation at 5000 rpm for 15 min to isolate the unexfoliated Sb2Se3 powders, PVP-functioned Sb2Se3 NSs were finally collected by centrifugation


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of the supernatants at 14000 rpm for 15 min and washed with DI water for 3 times. The obtained Sb2Se3 NSs were stored at 4 oC for further use. Characterization The microstructure and morphology of as-prepared Sb2Se3 NSs and treated bacteria were observed by a scanning electron microscope (SEM, FEI Quanta 200F) and a transmission electron microscope (TEM, JEOL JEM 2100). Raman spectra (LabRAM XploRA) and X-ray photoelectron spectroscopy (XPS, ESCALAB MK II X-ray photoelectron spectrometer) were also acquired. Photothermal Behavior of Sb2Se3 NSs Different concentrations of Sb2Se3 NSs were irradiated with an 808-nm laser, and the temperature was monitored by an IRT camera (Ti400, Fluke, USA) during irradiation. DI water was used a control. The photothermal stability was evaluated by irradiated with a laser (808 nm, 2 W) for five circles, and the absorbance before and after irradiation were recorded. The photothermal conversion efficiency of Sb2Se3 NSs was calculated according to a previous report33, and the detailed calculated procedure was shown in supporting information. Antibacterial Investigation Bacterial strains of E. coli (DH5α) and methicillin-resistant S. aureus (Mu50) were employed in our studies. In brief, the bacteria were cultivated overnight in Luria−Bertani (LB) broth medium at 37 °C and reached a concentration approximate 4 × 108 CFU mL-1. To investigate the antibacterial effect, the bacterial suspensions were diluted to 4 × 105 CFU mL-1 and mixed with different concentrations of Sb2Se3 NSs suspensions at the same volume respectively. Then, the


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non-laser groups of bacteria-Sb2Se3 hybrid suspensions were spread onto LB agar plates uniformly without any treatment, while the laser-treated groups were spread onto LB agar plates after subjected to laser irradiation (808 nm, 2 W) for 5 min. After cultivated at 37 °C for 24 h, the bacterial colonies were counted and the survival rate of bacteria were calculated using the following equation: Bacterial viability (%) = Nt/Nc × 100%, where Nt is the number of colony on Sb2Se3 treated group, Nc is the number of colony on control group (without Sb2Se3 or laser). To determine the influence of Sb2Se3 NSs on bacterial growth, 2 × 108 CFU mL-1 bacterial suspensions were cultivated at 37 °C in the presence of different concentrations of Sb2Se3 NSs, with or without laser irradiation (808 nm, 5 min). Optical density values of the bacterial suspensions at 600 nm were recorded every 2 h. Morphological Observation of the Bacteria The bacterial suspensions (2 × 105 CFU mL-1) were treated with Sb2Se3 NSs only (75 μM, 5 min), NIR only (808 nm, 5 min), or the Sb2Se3 NSs plus laser irradiation, respectively. Then, the bacterial samples were collected by centrifugation (3000 rpm, 3 min) and fixed with 2.5% paraformaldehyde for 12 h. Such samples were dehydrated by sequential treatment of ethanol solutions (20%, 30%, 40%, 50%, 60% and 70%) for 10 min, respectively, and dried in the air. SEM (FEI Quanta 200F) were used to investigate the morphology of bacteria. The bacterial samples without treated by either Sb2Se3 or laser irradiation was used as control. Live/Dead Staining Test The bacteria suspensions of different treatments were co-stained by SYTO 9 and propidium iodide for 30 min for direct observation of living and dead bacteria, respectively. After that, the


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bacterial samples were washed with PBS solution and then subjected to investigation with fluorescence microscopy. Detection of ROS Production The production of ROS during physical contact between Sb2Se3 NSs and bacteria was detected by ROS indictor DCFH-DA dye. E. coli cells were incubated with 150 µM of Sb2Se3 for 30 min, followed by the addition of DCFH-DA with a final concentration of 1µM. Fluorescence intensity of the suspensions at 526 nm was measured to evaluate the production level of ROS. In addition, the fluorescence of bacteria or Sb2Se3 was measured as controls. GSH Oxidation The oxidation of GSH catalyzed by Sb2Se3 NSs was evaluated by a standard Ellman’s assay. In brief, 0.4 mM GSH in 50 mM bicarbonate buffer (pH =8.7) was mixed with different concentrations of Sb2Se3 NSs dispersions for different time periods under the darkness, followed by the addition of 50 mM Tris-HCl and 10 mM DNTB solution. After centrifugation at 3000 rpm for 5 min, the optical absorbance of supernatant at 412 nm was measured. In addition, 1 mM H2O2 was used as positive control. Cell Toxicity of Sb2Se3 NSs The cell toxicity of Sb2Se3 NSs was evaluated by a standard MTT assay. In brief, human umbilical vein endothelial cell lines (HUVEC) with a density of 1 × 104 per well were incubated in cell culture medium containing different concentrations of Sb2Se3 NSs (0, 18.8, 37.5, 75, 150, 225, 300 and 375 µM) for 24 h at 37 °C, 5% CO2. After removing the supernatant, 20 µL MTT with a final concentration of 1 mg/mL was added to form the formazan crystals, which was


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dissolved by the following addition of DMSO. Finally, the absorbance of the solution at 570 nm was measured using a microplate reader to determine the relative cell viability. Wound Healing Animal Experiments Five SD rats (230 g, male) were chosen for the wound healing test. After anesthetized by intraperitoneal injection of chloral hydrate (10%, 0.3 mL per 100 g bodyweight), the dorsal hair of rats was shaved. Then, two full-thickness skin round wounds in the diameter of approximately 0.8 cm were prepared at each side of depilated back skin of hip on each rat. To construct an MRSA infectious wound model, an aliquot of MRSA suspension (100 µL, 106 CFU/mL) was inoculated onto each skin wound area. The Sb2Se3 NSs (100 µL, 0.3 mM) dispersions were injected and the right wound in each rat was then irradiated with an 808-nm laser, while the left wound remained untreated. Then measured the area of the infectious wound at 2, 4, 6, 8 and10 days post-treatment. H&E and Masson’s Trichrome staining were used to evaluate the wound healing process. All the animal experimental protocols were approved by the Institutional Animal Care and Use Committee (IACUC) of Anhui Medical University (LLSC20150134). Results and Discussion Preparation and Characterization of Sb2Se3 NSs Atomically thin Sb2Se3 NSs were prepared via a liquid exfoliation strategy integrating cryopretreatment and PVP-assisted exfoliation. The cryo-pretreatment of raw Sb2Se3 powder smashed large powders particles into small fragments, favorable for enhancing the following sonication exfoliation efficiency (Figure S1). During tip/bath sonication, bioinert PVP was added to endow the colloidal stability of exfoliated NSs by virtue of the high binding capability of PVP on the surface of 2D materials. The transmission electron microscope (TEM) image showed that


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Sb2Se3 NSs had the typical sheet-like morphology with a lateral size ranging from 50-150 nm (Figure1a and S2), and a crystalline lattice of 2.87 Å assigned to the (221) plane of Sb2Se3 crystal was observed by high-resolution TEM (HRTEM) (inset of Figure 1a). The atomic force microscopy (AFM) image revealed that the thicknesses of two typical Sb2Se3 NSs were 1.5 and 1.8 nm, respectively (Figure 1b), indicating the successful exfoliation of large and thick particles into small and atomically thin NSs due to the combined effects of cryogenic fracturing and ultrasound wave–mediated lattice breakup.34 The Raman spectra depicted a red shift of 8 nm between atomically thin Sb2Se3 NSs and bulk Sb2Se3 (Figure 1c), which was ascribed to the


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Figure 1. Characterization of atomically thin PVP-functioned Sb2Se3 NSs. (a) TEM image with inset HRTEM image, (b) AFM image with inset height profiles, (c) Raman spectra of bulk Sb2Se3 and Sb2Se3 NSs , (d-g) STEM-EDS mapping, (h-j) XPS spectra, weaker long-range Coulombic interaction in less-layer material.35 The scanning transmission electron microscopy energy dispersive X–ray spectrometry (STEM–EDS) mapping images (Figure 1d-g) confirmed the uniform distribution of elemental Sb and Se. X-ray photoelectron spectroscopy (XPS) spectra (Figure 1h-j) further demonstrated that NSs were composed of Sb3+ and Se2-, indicating that the phase compositions were well maintained after exfoliation.36 Fourier transform infrared spectroscopy (FTIR) spectra in Figure S3 confirmed the successful modification of PVP on the surface. Interestingly, PVP, the organic constituent of iodophor, has been clinically used for antibacterial applications due to high biocompatibility and high binding capability to iodine.37 These results clearly demonstrated the successful liquid exfoliation of atomically thin PVP-functioned Sb2Se3 NSs. Photothermal Behavior of Sb2Se3 NSs As a typical 2D materials, Sb2Se3 NSs exhibited considerable optical absorbance from ultraviolet (UV) to NIR region, and the absorbance intensity decreased along with the increase of wavelength, similar with other layered materials including graphene38 and black phosphorus39 (Figure 2a). The molar extinction coefficient at 808 nm is as high as 1.64 × 108 M−1 cm−1, indicating the potential of Sb2Se3 NSs as a high-efficient photothermal agent. To investigate the photothermal conversion ability, Sb2Se3 NSs suspensions with various concentrations were irradiated by a NIR laser under different powers (0.5, 1 and 2 W). As shown in Figure 2b-e, the temperature elevation of Sb2Se3 NSs suspensions was positively associated with NSs


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concentrations and laser power. Particularly, the temperature change of Sb2Se3 NSs suspensions (300 µM) irradiated with the laser power of 2 W was up to 29.9 oC (Figure 2c), high enough for effective short-time hyperthermia sterilization due to irreversible protein denaturation or cell

Figure 2. Photothermal performance of Sb2Se3 NSs. (a) UV-vis-NIR absorbance of Sb2Se3 NSs suspensions with different concentrations, (b) Photothermal heating curves of the corresponding Sb2Se3 NSs suspensions under laser irradiation (808 nm, 2 W), (c) The temperature change vs Sb2Se3 NSs concentrations, (d) The infrared thermography of Sb2Se3 NSs suspensions (225 µM) under laser irradiation with different laser powers (0.5, 1 and 2 W), (e) The corresponding photothermal heating curves under laser irradiation with different laser powers, (f) The photothermal heating curve of Sb2Se3 NSs suspensions (225 µM) under laser irradiation and the cooling curve after laser shutting off, (g) The corresponding fitting linear curve between –lnθ vs data time obtained for the cooling period. (h) Turning on-off temperature


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curves of Sb2Se3 NSs suspensions for five circles. (i) UV-vis-NIR absorbance change of Sb2Se3 NSs dispersions before and after irradiation. Inset is the corresponding digital photographs of Sb2Se3 NSs dispersions. membrane destruction.40-42 To further evaluate the photothermal performance, the photothermal conversion efficiency (PTCE) of PVP-capped Sb2Se3 NSs was measured. Based on the sample system time constant (τs) of 313.38 s by fitting the time data in the cooling period versus the negative natural logarithm of driving force temperature, the PTCE was calculated to be 42.08% according to the previous method (Figure 2f and g).33 In addition, the photothermal stability of Sb2Se3 NSs was evaluated. The temperature of Sb2Se3 NSs dispersions could reach the maximum during five-cycle irradiation, and the absorbance before and after irradiation depicted little change, suggesting the high photothermal stability of Sb2Se3 NSs (Figure 2h and i). In addition, the storage stability of Sb2Se3 NSs was also evaluated. As shown in Figure S4, the hydrodynamic diameter and absorbance of Sb2Se3 nanosheets in different mediums for a week depicted no obvious change, indicating relative high stability for biomedical applications. Hence, such high photothermal performance indicated that Sb2Se3 NSs could serve as a potential photothermal antibacterial agent for short-time hyperthermia sterilization. Synergistic Antibacterial Activity of Sb2Se3 NSs The rapid evolution of pathogenic bacteria, especially MDR bacteria, is an ever-growing global crisis, but the current and traditional antibiotics are ineffective to combat MDR bacteria.43 Hence, novel broad-spectrum inorganic antibacterial agents like 2D materials are receiving more and more attention recently.44 Inspired with the sharp edge and high photothermal performance of Sb2Se3 NSs, we inferred that PVP-functioned Sb2Se3 NSs could serve as an effective 2D


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antibacterial agent to combat various pathogens without the concern of drug resistant. To study the antibacterial activity of Sb2Se3 NSs, E. coli and MRSA are used as the typical models of Gram-negative bacteria and Gram-positive MDR bacteria, respectively. According to Figure 3ad, PVP-functioned Sb2Se3 NSs could only partially inhibit the bacterial colony formation without laser irradiation. The bacterial viability of E. coli and MRSA was 79% and 91%, respectively in the presence of 18.8 μM Sb2Se3 NSs (Figure 3b and d). Although the antibacterial effect could be enhanced with increasing nanoagent concentration, the bacterial viability only decreased to 50%

Figure 3. Antibacterial activity of Sb2Se3 NSs against E. coli and MRSA. (a) Digital photographs of E. coli colony formation in the presence of Sb2Se3 NSs with/without laser irradiation (808 nm, 2 W) for 5 min and further incubation for 24 h. (b) The corresponding relative bacteria viability of E. coli with/without laser irradiation. (c) Digital photographs of MRSA colony formation in the presence of Sb2Se3 NSs with/without laser irradiation (808 nm, 2 W) for 5 min and further incubation for 48 h. (d) The corresponding relative bacteria viability of MRSA with/without laser irradiation.


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and 60% for E. coli and MRSA, respectively, even when the concentration of Sb2Se3 NSs reached 300 μM, suggesting the relatively limited intrinsic antibacterial capability of Sb2Se3 NSs. However, upon laser irradiation, the antibacterial activity of Sb2Se3 NSs was could greatly promoted. After treated by 808 nm laser irradiation (5 min) for 8.8 μM Sb2Se3 NSs groups, the bacterial viability of decreased to 55% and 77% for E. coli and MRSA, respectively. The enhanced antibacterial ability of Sb2Se3 NSs was even more significant under high concentration. Particularly, neither E. coli nor MRSA colony could be found after being treated by 300 μM Sb2Se3 NSs under NIR laser irradiation (Figure 3a and c). As a result, the relative bacterial viabilities decreased to zero for both tested strains (Figure 3b and d). The decline in viable bacterial cells can also be observed in groups of laser irradiation combined with 37.5, 75, 150 μM Sb2Se3 NSs, respectively. The bacterial regrowth after laser irradiation was monitored to further investigate the enhanced antibacterial effect of Sb2Se3 NSs plus laser irradiation. It is obvious that bacterial growth of both E. coli and MRSA being treated by Sb2Se3 with NIR irradiation is drastically slower than the controlled groups without NIR irradiation (Figure S5 and 6), and the inhibition efficiency increased with the increase of Sb2Se3 NSs concentrations for 24 h, indicating that the antibacterial activity was dosage dependent. To clearly evaluate the antibacterial performance of Sb2Se3 NSs, the bacterial samples after various treatments were immediately co-stained by SYTO 9 and propidium iodide for 30 min directly observing the living and dead bacteria, followed by the investigation with fluorescence microscopy. The fluorescence microscopes images showed that only negligible dead cells (red signal) could be found after treatment of Sb2Se3 NSs alone or laser irradiation alone, for both E. coli and MRSA (Figure 4a1,a2, a5 and a6 ). In sharp contrast, large number of dead cells were presented at lower concentration of Sb2Se3 (75 μM) with NIR irradiation treated group (Figure


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4a3 and a7). When the concentration increased to 150 μM, the irradiation groups from both E. coli and MRSA bacteria were almost inactive (Figure 4a4 and a8). As such, these results depicted that laser irradiation could effectively initiate the enhanced antibacterial ability of Sb2Se3 NSs to combat MDR bacteria. To understand the hyperthermia antibacterial mechanism of Sb2Se3 NSs under laser irradiation, SEM was employed to investigate bacterial cellular damage from different groups. Laser irradiation in the absence of Sb2Se3 NSs didn’t introduce any bacterial morphology change

Figure 4. (a) Fluorescent images of the E. coli and MRSA samples subjected to different treatments as indicated: (a1) laser alone for E. coli. (a2) 150 μM of Sb2Se3 NSs alone for E. coli, (a3) 75 μM of Sb2Se3 NSs plus laser irradiation for E. coli, (a4) 150 μM of Sb2Se3 NSs plus laser


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irradiation for E. coli. (a5) laser alone for MRSA. (a6) 150 μM of Sb2Se3 NSs alone for MRSA, (a7) 75 μM of Sb2Se3 NSs plus laser irradiation for MRSA, (a8) 150 μM of Sb2Se3 NSs plus laser irradiation for MRSA. (b) SEM images of the E. coli and MRSA samples subjected to different treatments as indicated: (b1) control for E. coli, (b2) laser alone for E. coli, (b3) 150 μM of Sb2Se3 NSs alone for E. coli, (b4) 150 μM of Sb2Se3 NSs plus laser irradiation for E. coli, (b5) control for MRSA, (b6) laser alone for MRSA, (b7) 150 μM of Sb2Se3 NSs alone for MRSA, (b8) 150 μM of Sb2Se3 NSs plus laser irradiation for MRSA. (Figure 4b2 and b6), similar with the control group (Figure 4b1 and b5). When treated with Sb2Se3 alone, E. coli cells shrunk slightly to an intact rod-like structure and the morphology of part MRSA cells was destroyed (Figure 4b3 and b7), which may be partly attributed to the sharp edgeinduced membrane damage.45 The ultrathin nanosheet was believed to cut and destroy the cells membrane, leading to destructive lipid extraction.2 In addition, EDS mapping of E. coli bacteria after incubation with Sb2Se3 NSs was shown in Figure S7. Elemental Sb and Se were both distributed on the surface of E. coli bacteria, indicating the direct contact between bacteria and Sb2Se3 NSs. When treated with both Sb2Se3 NSs and laser irradiation, E. coli cells showed abnormal enlargements on its surface and the morphology of most MRSA cells was seriously destroyed (Figure 4b4 and b8) due to high temperature produced by the photothermal effect. Based on previous reports46,47, the high temperature could inactive both eukaryotic and prokaryotic cells, and hyperthermia-based therapy was effective in combating with bacterial infection. Therefore, under irradiation, the bacterial cell was believed to be more vulnerable to withstand external interference, as the structure and function of the cell was disordered by high temperature.


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To clarify the intrinsic long-term antibacterial mechanism of Sb2Se3 NSs without the irradiation, the detection assay of ROS produced during physical contact between NSs and bacteria was conducted. Several earlier 2D materials including graphene and MoS2 have demonstrated that the produced ROS could induce the intracellular oxidative stress to arise bacterial death.2,24 DCFH-DA is a fluorescent probe which could be transformed to DCFH after interacting with ROS. As shown in Figure 5a, no fluorescence was observed for E. coli bacteria or Sb2Se3 NSs. However, upon the mixing of E. coli bacteria and Sb2Se3 NSs for 30 min at 37 oC,

the bacterial suspension in the presence of Sb2Se3 NSs displayed a sharp increase in

fluorescent intensity at 526 nm, indicating the generation of considerable ROS. As we know, ROS in bacteria mainly originates from the enzymatic reactions between the leaked electrons from the respiratory chain and oxygen or other electron acceptors in bacteria48,49. For bacteria, the respiratory chain was located in cell membrane. Hence, when the cell membrane was damaged by the sharp edge of atomically thin Sb2Se3 NSs, the electronic transport along the respiratory chain may be impeded and more leaked electrons from the respiratory chain will react with oxygen or other electron acceptors in bacteria to produce more ROS. In addition, the disturbed balance of oxidative stress in bacteria can also affect the production of ROS. Because glutathione (GSH) tripeptide containing thiol groups is often applied as an oxidative stress indicator in cells, a standard Ellman’s assay was conducted to evaluate the oxidation of GSH. As shown in Figure 5c-d, Sb2Se3 nanosheets resulted in significant loss of GSH, and the oxidation of GSH increased with the increase of nanosheets concentrations and culture time. Such highperformance GSH depletion may be attributed to the electrical properties of Sb2Se3 nanosheets because Sb2Se3 NSs as a p-type semiconductor can allow oxidation in the presence of an excess of holes as previously reported24. After the mixture of Sb2Se3 NSs and bacteria, a portion of GSH


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in bacteria will be depleted, which may further increase the level of ROS in bacteria due to the loss of reduced GSH. Based on these results, we think that the high ROS generation after the mixture of Sb2Se3 NSs and bacteria should be mainly attributed to these two mechanisms: (1) the impeded electronic transport along the respiratory chain in the damaged cell membrane caused by the sharp edge of Sb2Se3 NSs; (2) the good ability of GSH depletion catalyzed by Sb2Se3 NSs. Hence, the excessively reactive ROS could destroy bacterial cellular organism and structures and result in the death of the bacterial cells. Based on the above findings, a potential synergistic mechanism for high-efficient antibacterial performance was proposed. On one hand, it is reasonable to speculate that the ROS produced by Sb2Se3 NSs would be more toxic to bacteria once the heating initiated. Normally, the cells could regulate moderate level of ROS under physiological temperature. However, the intracellular antioxidant mechanism such as catalase and superoxide dismutase system which could eliminate the ROS damage may be weakened under high temperature. As a result, the ROS damage on bacteria was enhanced and contributed to the synergistic antibacterial effect. On the other hand, when exposed to heating, the destructive physical interaction between bacteria and the sharp edge of Sb2Se3 NSs would be enhanced due to increased components motion under high temperature. Thus, the cooperation between heating and sharp edge-induced membrane damage may also promote the synergistic antibacterial performance. Collectively, these two antibacterial mechanisms, i.e. intrinsic antibacterial capability (ROS production and sharp edge) and hyperthermia sterilization, are responsible for the high-performance antibacterial ability.


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Figure 5. (a) The produced ROS estimation with fluorescent probe of DCFH-DA after bacteria incubated with Sb2Se3 NSs (150 μM). (b) Cell toxicity of different concentrations of Sb2Se3 NSs for 24 h. (c) Loss of GSH after incubation with different concentrations of Sb2Se3 nanosheets dispersion for 2 h. (d) Loss of GSH after incubation with Sb2Se3 nanosheets dispersion (300 µM) for different time periods. H2O2 (1 mM) was used as a positive control. Antibacterial agents for biomedical applications must be biocompatible. Hence, the primary biocompatibility in vitro of Sb2Se3 NSs was evaluated using a standard MTT assay. As shown in Figure 5b, no obvious cytotoxicity was observed after HUVEC cells incubated with different concentrations of Sb2Se3 NSs, which may be attributed to the biocompatible element constitute of Sb2Se3 NSs and the surface of bioinert PVP. For instance, even when the concentration of Sb2Se3 NSs was as high as 375 μM, the cell viability of HUVEC cells was still up to 85.6%, indicating the low cytotoxicity of Sb2Se3 NSs for biomedical applications.


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Encouraged by the excellent antibacterial activity in the lab, the antibacterial activity of Sb2Se3 NSs for practical application was investigated. Wild bacteria were randomly collected from water pool outside for further use. As suggested from Figure 6a, when only laser irradiation has been applied, a decline of bacterial viability by 18% was observed. Meanwhile, 300 μM of Sb2Se3 NSs reduced the bacterial viability by 25% without laser irradiation, which was slight

Figure 6. (a) Digital photographs of the formed E. coli colonies organed from natural water with or without the treatment of Sb2Se3 NSs (300 μM ) or laser irradiation (2 W, 808 nm) for 5 min. (b) The corresponding relative bacterial viabilities treated as indicated. better than the former. However, the treatment with both Sb2Se3 NSs and laser irradiation resulted in approximate 100% antibacterial activity (Figure 6b). These resulted indicated that the enhanced synergistic antibacterial ability of Sb2Se3 with the aid of laser irradiation could be effectively extended to other bacteria. To further demonstrate the antibacterial effect of Sb2Se3 NSs, the skin wound treatment in vivo was conducted. SD rats were used as MRSA infectious wound mode by inoculated onto skin wound area. As shown in Figure 7a, compared with the MRSA infected untreated control group


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(left), the Sb2Se3 NSs treated group (right) exhibited obviously accelerated wound healing and epidermis regeneration. It could be observed that only 58% of wound areas were closed from untreated group after 10 days, indicating the wound suffering from the MRSA infection was difficult to heal. As a comparison, 93% of the infected wound areas in the Sb2Se3 NSs treated group have been healed after 10 days, indicating that the NSs was beneficial to wound healing (Figure 7b). Hematoxylin & Eosin staining (H&E) and Masson’s Trichrome staining have been employed to evaluated the wound healing. As shown in Figure 7c), no structure of epidermis was formed and dermis still had obvious defect in the control groups group after 10 days. Moreover, though few collagen fibers could be observed in the control group, the arrangement of the fibers was not regular and the space between the collagens was relatively large. On the contrary, the wounds in the treated group formed complete regeneration epithelium and a lager of collagen fibers with regular arrangement. Particularly, the amount of mature hair follicles appeared the full healing of wounds. Hence, these results demonstrate that Sb2Se3 NSs under the laser irradiation can promote the wound healing in vivo through high-performance antibacterial effect.


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Figure 7 (a) Two round MRSA infectious wounds were constructed at two sides of depilated back skin of hip on each rat. The left wound remained untreated, while the right wound was treated by NSs, and pictures were collected after 2, 4, 6, 8 and 10 days in the wound healing process respectively; (b) Wound closure comparison between untreated and treated groups; (c) Photomicrographs showing section of skin tissues with H&E staining and Masson’s Trichrome staining of wound sites after 10 days (40×). Black dash circle, black arrow, read arrow indicated collagen fibers, epidermis, hair follicles, respectively

Conclusions We have successfully demonstrated that atomically thin Sb2Se3 NSs could serve as a new member of high-performance 2D antibacterial nanoagents. A liquid exfoliation strategy integrating cryo-pretreatment and PVP-assisted exfoliation was utilized for effective production of Sb2Se3 NSs. The obtained Sb2Se3 NSs exhibited intrinsic long-term antibacterial capability, probably due to the ROS generation and sharp edge-induced membrane damage. Meanwhile, Sb2Se3 NSs were capable of short-time hyperthermia sterilization under laser irradiation by virtue of strong optical absorbance and high PTCE. Benefiting from these two antibacterial mechanisms, various pathogens including E. coli, MRSA and wild bacteria could be effectively inhibited. Particularly, these three categories of bacteria were completely eradicated after treated with Sb2Se3 NSs (300 µM) plus laser irradiation for only 5 min. The wound healing test further depicted the excellent bacterial property in vivo. In addition, Sb2Se3 NSs depicted minimal cytotoxicity, suggesting the high potential for biomedical applications. Hence, atomically thin


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Sb2Se3 NSs are a promising 2D broad-spectrum antibacterial nanoagent for combating various pathogenic bacteria, especially MDR bacteria. ASSOCIATED CONTENT Supporting Information Available. The detailed calculated procedure of photothermal conversion efficiency, SEM images of raw Sb2Se3 powder and cryo-pretreatment Sb2Se3 powder, EDS mapping, FTIR spectra of raw Sb2Se3, PVP-functioned Sb2Se3 NSs and PVP, the bacterial growth curves with/without laser irradiation and storage stability of Sb2Se3 NSs for a week. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author *E-mail: [email protected], [email protected] Notes The authors declare no competing financial interest. Acknowledgements This work was supported by the National Natural Science Foundation of China (No. 31800834, 21574035), State Key Lab of Advanced Welding and Joining (No. AWJ-19M12), and the Fundamental Research Funds for the Central Universities (No. JZ2018HGBZ0156, JZ2018HGPA0273, JZ2018HGTB0247). REFERENCES


25


1.

Page 26 of 32

Liu, C.; Kong, D.; Hsu, P.-C.; Yuan, H.; Lee, H.-W.; Liu, Y.; Wang, H.; Wang, S.; Yan,

K.; Lin, D.; Maraccini, P. A.; Parker, K. M.; Boehm, A. B.; Cui, Y., Rapid Water Disinfection using Vertically Aligned MoS2 Nanofilms and Visible Light. Nat. Nanotechnol. 2016, 11, 10981104. 2.

Tu, Y.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z.; Huang, Q.; Fan, C.;

Fang, H.; Zhou, R., Destructive Extraction of Phospholipids from Escherichia Coli Membranes by Graphene Nanosheets. Nat. Nanotechnol. 2013, 8, 594-601. 3.

Miao, H.; Teng, Z.; Wang, C.; Chong, H.; Wang, G., Recent Progress in Two-

Dimensional Antimicrobial Nanomaterials. Chem. - Eur. J. 2019, 25 (4), 929-944. 4.

Yang, Y.; Ma, L.; Cheng, C.; Deng, Y.; Huang, J.; Fan, X.; Nie, C.; Zhao, W.; Zhao, C.,

Nonchemotherapic and Robust Dual-Responsive Nanoagents with On-Demand Bacterial Trapping, Ablation, and Release for Efficient Wound Disinfection. Adv. Funct. Mater. 2018, 28 (21), 1705708. 5.

Lu, X.; Feng, X.; Werber, J. R.; Chu, C.; Zucker, I.; Kim, J.-H.; Osuji, C. O.; Elimelech,

M., Enhanced Antibacterial Activity Through The Controlled Alignment of Graphene Oxide Nanosheets. Proc. Natl. Acad. Sci. U. S. A. 2017, 114 (46), E9793-E9801. 6.

Bu, Q.; Wang, B.; Huang, J.; Liu, K.; Deng, S.; Wang, Y.; Yu, G., Estimating The Use of

Antibiotics for Humans Across China. Chemosphere 2016, 144, 1384-1390. 7.

Chu, J.; Vila-Farres, X.; Inoyama, D.; Gallardo-Macias, R.; Jaskowski, M.; Satish, S.;

Freundlich, J. S.; Brady, S. F., Human Microbiome Inspired Antibiotics with Improved β-Lactam Synergy against MDR Staphylococcus aureus. ACS Infect. Dis. 2018, 4 (1), 33-38.


26

Page 27 of 32 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


8.

Hu, L.; Wang, H.; Xia, T.; Fang, B.; Shen, Y.; Zhang, Q.; Tian, X.; Zhou, H.; Wu, J.;

Tian, Y., Two-Photon-Active Organotin(IV) Complexes for Antibacterial Function and Superresolution Bacteria Imaging. Inorg. Chem. 2018, 57 (11), 6340-6348. 9.

Fang, M.; Chen, J.-H.; Xu, X.-L.; Yang, P.-H.; Hildebrand, H. F., Antibacterial Activities

of Inorganic Agents On Six Bacteria Associated with Oral Infections by Two Susceptibility Tests. Int. J. Antimicrob. Agents 2006, 27 (6), 513-517. 10.

Krishnamoorthy, K.; Veerapandian, M.; Zhang, L.-H.; Yun, K.; Kim, S. J., Antibacterial

Efficiency of Graphene Nanosheets against Pathogenic Bacteria via Lipid Peroxidation. J. Phys. Chem. C 2012, 116 (32), 17280-17287. 11.

Le Ouay, B.; Stellacci, F., Antibacterial Activity of Silver Nanoparticles: A Surface

Science Insight. Nano Today 2015, 10 (3), 339-354. 12.

Marchetti, F.; Palmucci, J.; Pettinari, C.; Pettinari, R.; Scuri, S.; Grappasonni, I.;

Cocchioni, M.; Amati, M.; Lelj, F.; Crispini, A., Linkage Isomerism in Silver Acylpyrazolonato Complexes and Correlation with Their Antibacterial Activity. Inorg. Chem. 2016, 55 (11), 54535466. 13.

Imazato, S., Antibacterial Properties of Resin Composites and Dentin Bonding Systems.

Dent. Mater. 2003, 19 (6), 449-457. 14.

Varaprasad, K.; Raghavendra, G. M.; Jayaramudu, T.; Seo, J., Nano Zinc Oxide–Sodium

Alginate Antibacterial Cellulose Fibres. Carbohydr. Polym. 2016, 135, 349-355. 15.

Malwal, D.; Gopinath, P., Efficient Adsorption and Antibacterial Properties of

Electrospun CuO-ZnO Composite Nanofibers for Water Remediation. J. Hazard. Mater. 2017, 321, 611-621.


27


16.

Page 28 of 32

Liu, J.; Lu, S.; Tang, Q.; Zhang, K.; Yu, W.; Sun, H.; Yang, B., One-step Hydrothermal

Synthesis of Photoluminescent Carbon Nanodots with Selective Antibacterial Activity Against Porphyromonas Gingivalis. Nanoscale 2017, 9 (21), 7135-7142. 17.

Yang, J.; Zhang, X.; Ma, Y.-H.; Gao, G.; Chen, X.; Jia, H.-R.; Li, Y.-H.; Chen, Z.; Wu,

F.-G., Carbon Dot-Based Platform for Simultaneous Bacterial Distinguishment and Antibacterial Applications. ACS Appl. Mater. Interfaces 2016, 8 (47), 32170-32181. 18.

Li, R.; Mansukhani, N. D.; Guiney, L. M.; Ji, Z.; Zhao, Y.; Chang, C. H.; French, C. T.;

Miller, J. F.; Hersam, M. C.; Nel, A. E.; Xia, T., Identification and Optimization of Carbon Radicals on Hydrated Graphene Oxide for Ubiquitous Antibacterial Coatings. ACS Nano 2016, 10 (12), 10966-10980. (19)

Sun, W.; Wu, F.-G. Two-Dimensional Materials for Antimicrobial Applications:

Graphene Materials and Beyond. Chem. –Asian J. 2018, 13, 3378-3410. 20.

Gupta, A.; Sakthivel, T.; Seal, S., Recent Development in 2D Materials Beyond

Graphene. Prog. Mater. Sci. 2015, 73, 44-126. 21.

Kim, T. I.; Kwon, B.; Yoon, J.; Park, I.-J.; Bang, G. S.; Park, Y.; Seo, Y.-S.; Choi, S.-Y.,

Antibacterial Activities of Graphene Oxide–Molybdenum Disulfide Nanocomposite Films. ACS Appl. Mater. Interfaces 2017, 9 (9), 7908-7917. 22.

Yang, X.; Li, J.; Liang, T.; Ma, C.; Zhang, Y.; Chen, H.; Hanagata, N.; Su, H.; Xu, M.,

Antibacterial Activity of Two-dimensional MoS2 Sheets. Nanoscale 2014, 6 (17), 10126-10133. 23.

Pang, X.; Xiao, Q.; Cheng, Y.; Ren, E.; Lian, L.; Zhang, Y.; Gao, H.; Wang, X.; Leung,

W.; Chen, X.; Liu, G.; Xu, C., Bacteria-Responsive Nanoliposomes as Smart Sonotheranostics for Multidrug Resistant Bacterial Infections. ACS Nano 2019, 13 (2), 2427-2438.


28

Page 29 of 32 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


24.

Karunakaran, S.; Pandit, S.; Basu, B.; De, M., Simultaneous Exfoliation and

Functionalization of 2H-MoS2 by Thiolated Surfactants: Applications in Enhanced Antibacterial Activity. J. Am. Chem. Soc. 2018, 140 (39), 12634-12644. 25.

Rasool, K.; Helal, M.; Ali, A.; Ren, C. E.; Gogotsi, Y.; Mahmoud, K. A., Antibacterial

Activity of Ti3C2Tx MXene. ACS Nano 2016, 10 (3), 3674-3684. 26.

Huang, J.; Ho, W.; Wang, X., Metal-free Disinfection Effects Induced by Graphitic

Carbon Nitride Polymers under Visible Light Illumination. Chem. Commun. 2014, 50 (33), 4338-4340. 27.

Sun, Z.; Zhang, Y.; Yu, H.; Yan, C.; Liu, Y.; Hong, S.; Tao, H.; Robertson, A. W.;

Wang, Z.; Pádua, A. A. H., New Solvent-Stabilized Few-Layer Black Phosphorus for Antibacterial Applications. Nanoscale 2018, 10 (26), 12543-12553. 28.

Ouyang, J.; Wen, M.; Chen, W.; Tan, Y.; Liu, Z.; Xu, Q.; Zeng, K.; Deng, L.; Liu, Y.-N.,

Multifunctional Two Dimensional Bi2Se3 Nanodiscs for Combined Antibacterial and AntiInflammatory Therapy for Bacterial Infections. Chem. Commun. 2019, 55 (33), 4877-4880. 29.

Zhou, Y.; Wang, L.; Chen, S.; Qin, S.; Liu, X.; Chen, J.; Xue, D.-J.; Luo, M.; Cao, Y.;

Cheng, Y.; Sargent, E. H.; Tang, J., Thin-Film Sb2Se3 Photovoltaics with Oriented OneDimensional Ribbons and Benign Grain Boundaries. Nat. Photonics 2015, 9, 409-415. 30.

Song, H.; Li, T.; Zhang, J.; Zhou, Y.; Luo, J.; Chen, C.; Yang, B.; Ge, C.; Wu, Y.; Tang,

J., Highly Anisotropic Sb2Se3 Nanosheets: Gentle Exfoliation from the Bulk Precursors Possessing 1D Crystal Structure. Adv. Mater. 2017, 29 (29), 1700441. 31.

Ou, X.; Yang, C.; Xiong, X.; Zheng, F.; Pan, Q.; Jin, C.; Liu, M.; Huang, K., A New

rGO-Overcoated Sb2Se3 Nanorods Anode for Na+ Battery: In Situ X-Ray Diffraction Study on a Live Sodiation/Desodiation Process. Adv. Funct. Mater. 2017, 27 (13), 1606242.


29


32.

Page 30 of 32

Fan, L.; Huang, D.; Wang, Y.; Miao, Z.; Ma, Y.; Zhao, Q.; Zha, Z., Cryo-Assisted

Exfoliation of Atomically Thin 2D Sb2Se3 Nanosheets for Photo-Induced Theranostics. Chem. Commun. 2019, 55 (19), 2805-2808. 33.

Roper, D. K.; Ahn, W.; Hoepfner, M., Microscale Heat Transfer Transduced by Surface

Plasmon Resonant Gold Nanoparticles. J. Phys. Chem. C 2007, 111 (9), 3636-3641. 34.

Wang, Y.; Liu, Y.; Zhang, J.; Wu, J.; Xu, H.; Wen, X.; Zhang, X.; Tiwary, C. S.; Yang,

W.; Vajtai, R.; Zhang, Y.; Chopra, N.; Odeh, I. N.; Wu, Y.; Ajayan, P. M., Cryo-Mediated Exfoliation and Fracturing of Layered Materials into 2D Quantum Dots. Sci. Adv. 2017, 3 (12), e1701500. 35.

Hellgren, M.; Baima, J.; Bianco, R.; Calandra, M.; Mauri, F.; Wirtz, L., Critical Role of

the Exchange Interaction for the Electronic Structure and Charge-Density-Wave Formation in TiSe2. Phys. Rev. Lett. 2017, 119 (17), 176401. 36.

Zhao, B.; Wan, Z.; Luo, J.; Han, F.; Ashraf Malik, H.; Jia, C.; Liu, X.; Wang, R.,

Efficient Sb2Se3 Sensitized Solar Cells Prepared through A Facile SILAR Process and Improved Performance by Interface Modification. Appl. Surf. Sci. 2018, 450, 228-235. 37.

Uchiyama, S.; Dahesh, S.; Nizet, V.; Kessler, J., Enhanced Topical Delivery of Non-

Complexed Molecular Iodine for Methicillin-Resistant Staphylococcus Aureus Decolonization. Int. J. Pharm. 2019, 554, 81-86. 38.

Tayyebi, A.; Akhavan, O.; Lee, B.-K.; Outokesh, M., Supercritical Water in Top-Down

Formation of Tunable-Sized Graphene Quantum Dots Applicable in Effective Photothermal Treatments of Tissues. Carbon 2018, 130, 267-272.


30

Page 31 of 32 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


39.

Sun, C.; Wen, L.; Zeng, J.; Wang, Y.; Sun, Q.; Deng, L.; Zhao, C.; Li, Z., One-Pot

Solventless Preparation of PEGylated Black Phosphorus Nanoparticles for Photoacoustic Imaging and Photothermal Therapy of Cancer. Biomaterials 2016, 91, 81-89. 40.

Zhang, W.; Shi, S.; Wang, Y.; Yu, S.; Zhu, W.; Zhang, X.; Zhang, D.; Yang, B.; Wang,

X.; Wang, J., Versatile Molybdenum Disulfide Based Antibacterial Composites for In Vitro Enhanced Sterilization and In Vivo Focal Infection Therapy. Nanoscale 2016, 8 (22), 1164211648. 41.

Li, Y.; Liu, X.; Tan, L.; Cui, Z.; Yang, X.; Zheng, Y.; Yeung, K. W. K.; Chu, P. K.; Wu,

S., Rapid Sterilization and Accelerated Wound Healing Using Zn2+ and Graphene Oxide Modified g-C3N4 under Dual Light Irradiation. Adv. Funct. Mater. 2018, 28 (30), 1800299. 42.

Wu, W.-Y.; Xu, Y.; Ong, X.; Bhatnagar, S.; Chan, Y., Thermochromism from Ultrathin

Colloidal Sb2Se3 Nanowires Undergoing Reversible Growth and Dissolution in an Amine–Thiol Mixture. Adv. Mater. 2019, 31 (4), 1806164. 43.

Kumari, M.; Pandey, S.; Giri, V. P.; Bhattacharya, A.; Shukla, R.; Mishra, A.; Nautiyal,

C. S., Tailoring Shape and Size of Biogenic Silver Nanoparticles to Enhance Antimicrobial Efficacy against MDR Bacteria. Microb. Pathog. 2017, 105, 346-355. 44.

Liu, C.; Shan, H.; Chen, X.; Si, Y.; Yin, X.; Yu, J.; Ding, B., Novel Inorganic-Based N-

Halamine Nanofibrous Membranes As Highly Effective Antibacterial Agent for Water Disinfection. ACS Appl. Mater. Interfaces 2018, 10 (51), 44209-44215. 45.

Feng, Y.; Chen, Q.; Yin, Q.; Pan, G.; Tu, Z.; Liu, L., Reduced Graphene Oxide

Functionalized with Gold Nanostar Nanocomposites for Synergistically Killing Bacteria through Intrinsic Antimicrobial Activity and Photothermal Ablation. ACS Appl. Bio Mater. 2019, 2 (2), 747-756.


31


46.

Page 32 of 32

Yin, W.; Yu, J.; Lv, F.; Yan, L.; Zheng, L. R.; Gu, Z.; Zhao, Y., Functionalized Nano-

MoS2 with Peroxidase Catalytic and Near-Infrared Photothermal Activities for Safe and Synergetic Wound Antibacterial Applications. ACS Nano 2016, 10 (12), 11000-11011. 47.

Shao, J.; Ruan, C.; Xie, H.; Li, Z.; Wang, H.; Chu, P. K.; Yu, X.-F., Black-Phosphorus-

Incorporated Hydrogel as a Sprayable and Biodegradable Photothermal Platform for Postsurgical Treatment of Cancer. Adv. Sci. 2018, 5 (5), 1700848. 48

Zhao, Y.; Wang, Z.-B.; Xu, J.-X. Effect of Cytochrome c on the Generation and

Elimination of O and H2O2 in Mitochondria. J.Biol. Chem 2003, 278, 2356-2360. 49

Loschen, G.; Azzi, A.; Richter, C.; Flohé, L. Superoxide Radicals as Precursors of

Mitochondrial Hydrogen Peroxide. FEBS Lett. 1974, 42, 68-72.

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Liquid Exfoliation of Atomically Thin Antimony Selenide as an Efficient

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