Polyphenol-Assisted Exfoliation of Transition Metal Dichalcogenides

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Polyphenol-Assisted Exfoliation of Transition Metal Dichalcogenides into Nanosheets as Photothermal Nanocarriers for Enhanced Antibiofilm Activity Chao Zhang, Deng-Feng Hu, Jing-Wei Xu, Meng-Qi Ma, Huabin Xing, Ke Yao, Jian Ji, and Zhi-Kang Xu ACS Nano, Just Accepted Manuscript • DOI: 10.1021/acsnano.8b06321 • Publication Date (Web): 03 Dec 2018 Downloaded from http://pubs.acs.org on December 4, 2018

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Polyphenol-Assisted Exfoliation of Transition Metal Dichalcogenides

into

Nanosheets

as

Photothermal

Nanocarriers for Enhanced Antibiofilm Activity Chao Zhang†a, Deng-Feng Hu†a, Jing-Wei Xu†b, Meng-Qi Maa, Huabin Xingc, Ke Yao*b, Jian Ji*a, and Zhi-Kang Xu*a a

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China b Eye Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China c Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou 310027, China E-mail: [email protected], [email protected], [email protected] KEYWORDS: transition metal dichalcogenides (TMDs) • aqueous exfoliation • monolayer nanosheets • photothermal nanocarrier • antibiofilm activity.

ABSTRACT: Transition metal dichalcogenides (TMDs) nanosheets have evoked enormous research enthusiasm and have shown increased potentials in biomedical field. However, a great challenge lies in high-throughput, large-scale and eco-friendly preparation of TMDs nanosheets dispersions with high quality. Herein, we report a universal polyphenol-assisted strategy to facilely exfoliate various TMDs into monolayer or few-layer nanosheets. By optimizing the exfoliation condition of molybdenum disulfide (MoS2), the yield and concentration of as-exfoliated nanosheets is up to 60.5% and 1.21 mg/mL, respectively. This is the most efficient aqueous exfoliation method at present and is versatile for the choices of polyphenols and TMDs nanomaterials. The as-exfoliated MoS2 nanosheets possess superior 1 ACS Paragon Plus Environment

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biomedical stability as nanocarriers to load antibiotic drug. They show high photothermal conversion effect and thus induce a synergetic effect of chemotherapy and photothermal therapy to harvest enhanced antibiofilm activity under near-infrared (NIR) light. All these results offer an appealing strategy toward the synthesis and application of ultrathin TMDs nanosheets, with great implications for their development.

Since the pioneering discovery of graphene,1,2 ultrathin two dimensional (2D) nanomaterials have received much interest because of their exceptionally physical and chemical properties.3-7 As an promising alternative to graphene, ultrathin transition metal dichalcogenides (TMDs, such as MoS2, WS2, MoSe2, and WSe2) have been explored in numerous fields ranging from environment remediation,8,9 catalysis,10-12 sensor13,14 and energy storage15,16 to nanomedicine.17-20 Particularly, monolayer or few-layer TMDs nanosheets have a great deal of merits in biomedical applications: excellent biological stability, high biocompatibility, large surface area and strong near-infrared (NIR) absorption. Therefore, they are ideal nanocarriers for photo-controlled drug delivery and photothermal therapy.17,18 Up to date, despite great progresses have been made in the synthesis method of TMDs nanosheets, it is highly desired to cost-effectively scale high-throughput manufacturing of few-layer TMDs nanosheets. Tremendous efforts have been witnessed to synthesize monolayer or few-layer TMDs nanosheets, mainly through two strategies. One is the bottom-up approach via chemical vapor deposition21 and wet-chemical synthesis22 to use various precursors for the preparation of 2 ACS Paragon Plus Environment

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ultrathin 2D nanomaterials. The other is the top-down approach by directly exfoliating the bulk TMDs crystals into monolayer or few-layer nanosheets. These exfoliation methods mainly

include

micromechanical

cleavage,23

liquid

exfoliation24-26

and

chemical/electrochemical alkali metal intercalation and exfoliation.27,28 Among them, the liquid exfoliation strategy has been considered as the most potential one due to its ease of implementation and large-scale production. In general, it requires specific solvents with appropriate surface tension to well match the surface energy of TMDs (around 40 ∼ 45 mJ/m2). Organic solvents such as N-methylpyrrolidone and dimethylformamide with the surface energy of 40.8 mJ/m2 and 36.5 mJ/m2, respectively, were chosen in previous works.24,29 However, these organic solvents are usually toxic and pose an enormous risk for biomedical applications. Thereby, aqueous exfoliation is the ideal choice from the perspective of applications. In this case, water soluble surfactants,25 biomacromolecules26,30-32 and polymers33-35 have to be used to reduce the surface tension of water (72 mJ/m2) and then to stabilize the as-exfoliated TMDs nanosheets against restacking and aggregation.25 Unfortunately, these exfoliation protocols always suffer from long manufacture time and low yield of monolayer nanosheets. Therefore, it still remains a great challenge to develop a rapid and high-throughput strategy for preparing monolayer TMDs nanosheets via aqueous exfoliation. Natural polyphenols have recently attracted much attention due to their surface-adaptive interfacial adhesion, excellent biocompatibility and post-functionalization accessibility.36-40 Herein, we report an efficient and green approach to exfoliate various TMDs into 3 ACS Paragon Plus Environment

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high-quality nanosheets dispersions using polyphenols as stabilizers (Figure 1). The process costs 2 h to achieve high concentration dispersions of monolayer TMDs nanosheets, which is the fastest aqueous exfoliation route until now. The as-exfoliated monolayer TMDs nanosheets can be applied for biomedical application and play two important roles: 1) utilizing their large surface area to act as the drug nanocarrier to load antibiotics Penicillin (Pen) by non-covalent adsorption (i.e. hydrophobic interaction), and 2) employing their NIR photothermal effect to regulate antibiotics release, as well as reduce drug tolerance of bacterial biofilm and facilitate antibiotics delivery into biofilm, so as to realize excellent antibacterial activity. This work not only highlights the promise of synthesizing ultrathin 2D nanosheets dispersions, but also further broadens their biomedical applications. RESULTS AND DISCUSSION Natural polyphenols have been widely found in plant tissues,41 including epigallocatechin (EGC), epicatechin gallate (ECG), epigallocatechin gallate (EGCG), tannic acid (TA) and tea catechins, just to name a few (Figure 1a). First, TA was used as a typical polyphenol (substitutable by above other polyphenols) to demonstrate the feasibility of our exfoliation approach (Figure 1b). Taking MoS2 as an example, the bulk crystals are normally suspended on the water surface and cannot form homogeneous dispersions. However, with the assistance of TA and ultrasonic cell crusher, they are facilely exfoliated into nanosheets by sonication and stably dispersed in the aqueous solution (Figure S1 in the Supporting Information). The TA-stabilized MoS2 dispersions exhibit two absorption peaks at 610 (B-exciton peak of MoS2) and 670 nm (A-exciton peak of MoS2) in the UV-vis absorption spectra, and the according 4 ACS Paragon Plus Environment

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color of MoS2 changes from black to dark green after exfoliation (Figure S2 in the Supporting Information) because of the direct excitonic transition at the K point of Brillouin zone.30 Additionally, their UV-vis absorption intensities and exfoliation yield gradually increase along with the sonication time and power (Figure 2a and Figure S3 in the Supporting Information). As we can see, the concentration and yield of the as-exfoliated MoS2 nanosheets can reach up to 1.21 mg/mL and 60.5%, respectively, when the sonication time and power are 2 h and 300 W. Table 1 compares the aqueous exfoliation results of TMDs using different water soluble stabilizers. Obviously, our method has the highest aqueous exfoliation rate and yield. It should be pointed out that the exfoliation yield of MoS2 in TA solution is only 11.2% when we used the conventional bath sonication tool to carry out the similar exfoliation experiment (Figure S4 in the Supporting Information), indicating that ultrasonic cell crusher is more powerful than that of conventional bath sonication. To further ensure the reliability of our results, several reported aqueous stabilizers, such as sodium alginate26 and bovine serum albumin (BSA),30 were used to execute the same exfoliation process using ultrasonic cell crusher. It can be seen that the resulted dispersions show much lower UV-vis absorption than those of TA as the stabilizer (Figure S5 in the Supporting Information). In addition, the absorption intensity is also much lower for the sonication-exfoliated MoS2 nanosheets dispersions without stabilizer than those with TA as a stabilizer. This absorption appears a significant reduction after 7 days incubation (Figure S6 in the Supporting Information), implying the as-exfoliated nanosheets tend to restack and aggregate. To our delight, the TA-stabilized nanosheets dispersions are highly stable without 5 ACS Paragon Plus Environment

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any changes even after incubated more than 7 days (Figure S6 in the Supporting Information). All these results demonstrate that TA is an outstanding stabilizer for the rapid and efficient exfoliation of MoS2 crystals into stable nanosheets dispersions assisted by ultrasonic cell crusher. The as-prepared nanosheets were evaluated by transmission electron microscopy (TEM) and atomic force microscopy (AFM). They are ultrathin 2D nanoflakes (Figure 2b) with a lattice spacing of 0.27 nm (Figure 2c) attributed to the (100) lattice plane of 2H MoS2.30 These 2D nanoflakes stay the crystal structure of 2H MoS2 as indicated by the hexagonal spot pattern (inset in Figure 2c). In addition, X-ray diffraction (XRD) results also confirm the 2H crystal structure of the as-exfoliated nanoflakes (Figure S7 in the Supporting Information). The average lateral sizes and thicknesses of these nanoflakes are 38.6 ± 1.3 and 0.88 ± 0.04 nm, respectively, analyzed using the Gaussian distribution (Figure 2d-f). In general, the theoretical thickness of monolayer MoS2 is around 0.65 nm,30,42 indicating the TA-assisted aqueous exfoliation with a dominance of monolayer nanosheets and a minority of few-layer nanosheets. To recap, our approach is able to prepare high-quality monolayer MoS2 nanosheets dispersions, which is very favorable to offer large surface area for loading functional molecules. TEM mapping images were conducted to detect the elements distribution on the nanosheet surfaces and to further elucidate the role of TA molecules. There are C and O elements on the nanosheet surfaces (Figure S8 in the Supporting Information), ascribed to the TA molecules as the stabilizer. The zeta potential of the TA-stabilized MoS2 nanosheets is -33 mV, which is 6 ACS Paragon Plus Environment

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slightly higher than that without TA (-40 mV) (Figure S9 in the Supporting Information). All these results indicate that TA molecules are tightly adsorbed on the MoS2 nanosheet surfaces during the exfoliation process, resulting in the high stability of the exfoliated monolayer nanosheets dispersions. Binding energy simulation between one TA molecule and monolayer MoS2 nanosheet was employed to further understand the stabilization mechanism (Figure 2g and h). It is worth noting that the binding energy between TA and MoS2 reaches up to near 75.95 eV, whereas the binding energy of two neighboring monolayer MoS2 nanosheets is only 0.21 eV.30 As a result, the adsorption of TA onto the MoS2 nanosheets can be faster than the restacking and aggregation of the nanosheets themselves when the sonication breaks the weak van der Waals interactions between neighboring MoS2 layers. In addition, the binding energy of catechol on MoS2 nanosheet is 1.12 eV, which is much larger than that of benzene (0.76 eV), phenol (0.85 eV) and hydroxyl motif (0.25 eV) (Figure 2h). It is resulted from the fascinating adhesion forces based on the catechol-inspired chemistry via multiple non-covalent interactions, and the origin of their interaction is mainly attributed to the hydrophobic interaction between the TMDs monolayer and hydrophobic aromatic structures in polyphenols.43 And hydrophilic hydroxyl motifs of polyphenols can be employed to facilitate the stable dispersion of the exfoliated nanosheets. Thus, TA and its polyphenol analogous are unparalleled candidates to rapidly stabilize and effectively enhance the aqueous exfoliation of TMDs. To assess the universality of our method, other natural polyphenols such as EGC, EGCG and tea catechins were selected to carry out the exfoliation experiments. The UV-vis 7 ACS Paragon Plus Environment

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absorption spectra show all three polyphenols can successfully exfoliate MoS2 into nanosheets (Figure 3a-c), and the exfoliation yield of MoS2 using EGC, EGCG and tea catechins is 40.5%, 52.1% and 35.4%, respectively. The according digital pictures (the inset in Figure 3a-c) and absorbance change results (Figure S10 in Supporting Information) indicate as-exfoliated nanosheets can form highly stabilized dispersions without the appearance of aggregation phenomenon even incubated 7 days. In addition, this method is also able to exfoliate other TMDs into nanosheets, such as tungsten disulfide (WS2), molybdenum selenium (MoSe2) and tungsten selenium (WSe2). Figure 3d-f demonstrate the UV-vis absorption spectra exhibit some characteristic peaks at 630, 706 and 760 nm, attributed to the A-exciton peaks of WS2, the B-exciton peaks of MoSe2 and the A-exciton peaks of WSe2 nanosheets, respectively. Similarly, TEM and AFM images provide definite evidence to demonstrate that all these TMDs are successfully exfoliated into monolayer or few-layer nanosheets (Figure 3h and Figure S11 in the Supporting Information). The average lateral size is around 60.8 ± 2.8, 54.4 ± 1.3 and 49.5 ± 5.1 nm for the as-exfoliated WS2, MoSe2 and WSe2 nanosheets, respectively, and the corresponding average thickness is 1.51 ± 0.93, 1.09 ± 0.12 and 0.99 ± 0.05 nm. Furthermore, our polyphenol-assisted exfoliation strategy is very easy and fast to prepare the monolayer or few-layer TMDs nanosheets dispersions on a large scale (Figure S12 in the Supporting Information). It is well known that TMDs nanosheets have various advanced properties in biomedical applications, and our polyphenol-assisted exfoliation method is green and eco-friendly without any toxic components. Therefore, the as-prepared monolayer or few-layer TMDs 8 ACS Paragon Plus Environment

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nanosheets are capable of serving as the promising nanocarriers to load drug, and antibiotic Pen was used as a typical drug model in this work (Figure 4a and Figure S13 in the Supporting Information). It can be seen that the zeta-potential of MoS2 nanosheets has a slight change after loading Pen, but they are still negatively charged in aqueous solutions with pH value from 4 to 10 (Figure 4c). These Pen-loaded MoS2 (MoS2-Pen) nanosheets exhibit excellent dispersion stability not only in phosphate-buffered (PBS, 10 mM) and 0.9% NaCl solution but also in biological complex media such as tryptone soy broth (TSB, biofilm culture medium), bull serum albumin (BSA, 5 mg/mL), 100% fetal bovine serum (FBS), and cell culture medium (DMEM+10% FBS) at pH 7.4 (Figure 4b and Figure S14 and 15 in the Supporting Information). Their FT-IR spectra show weak absorption peaks at 2850 and 2960 cm-1 attributed to the symmetrical and asymmetrical stretching vibration of CH3, respectively, and two peaks at 690 and 755 cm-1 belonged to the bending vibrations of N-H (Figure 4d). These characteristic peaks are ascribed to antibiotic Pen, implying it was loaded onto the nanosheet surfaces. The loading content is around 16.5% as quantitatively measured by TGA (Figure 4e). In addition, the MoS2-Pen nanosheets demonstrate excellent NIR photothermal conversion effect. Figure 4f shows the solution temperature can be effectively raised under the 808 nm NIR light irradiation (3 W/cm2), and it increases with the concentration increase of MoS2-Pen nanosheets. The temperature can also be precisely tuned by varying NIR laser power (Figure 4g). It should be pointed out that the solution temperature can be heated to near 55 °C when the concentration of MoS2 nanosheets is 4.43 mg/mL (inset in Figure 4h).

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On the other hand, it gradually decreases to room temperature as the NIR laser is shut off (Figure 4h). It is reasonable to deduce that the increased temperature via NIR photothermal effect can effectively weaken the interactions between the antibiotic Pen and the nanosheet surface to achieve photo-regulated drug delivery via a non-contact control model. From the drug release experiment, there is almost only Pen released from the MoS2 nanosheets at pH 5.5 under NIR laser irradiation (2.0 W/cm2) for 10 min, and its releasing ratio is as high as 16.3% (Figure S16 and S17 the Supporting Information). Moreover, Pen released from MoS2-Pen nanosheet is demonstrated in a power-dependent manner, and about 88% of Pen is released when the power reaches 3.5 W/cm2 for 6 hours (Figure S18 the Supporting Information). In our cases, S.aureus and E. coil were chosen to investigate the antibiofilm activity of MoS2-Pen nanosheets by NIR-triggered drug delivery (Figure 5a, c and d). Note that the amount of free Pen (0.366 mg/mL) added into the biofilm is same as that loaded on the MoS2-Pen, but the amount of Pen released from the MoS2-Pen nanosheets (0.171 mg/mL) is much lower than that of initial loading content, due to the incomplete release of Pen from MoS2-Pen nanosheets. As shown in Figure 5a, c and d, free Pen does not exhibit expected bactericidal property, and most of S.aureus and E. coil are still alive. The possible reason is that these bacterial cells are prone to produce adhesive biofilm to irreversibly cling to the surfaces of material or tissue, which is further sealed by the self-produced extracellular polymeric substances (EPS).44-46 On the one hand, this EPS biofilm is able to act as a compact barrier against antibiotic infiltration by the diffusion reaction inhibition, resulting in strong resistance 10 ACS Paragon Plus Environment

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against antibiotics like Pen. On the other hand, due to the encapsulation of EPS, bacteria in the middle or the bottom of biofilm is on slow growth rates or dormancy, resulting in a sharp decrease of the bacterial sensibility to Pen. And thus, bacterial cells in biofilm can tolerate up to 1000 times higher antibiotic concentration than planktonic bacterial cells,47 leading to free Pen with low antibiofilm activity. Similarly, Pen loaded on the MoS2 nanosheet is difficult to infiltrate this EPS biofilm for killing the bacterial (Figure 5a, c and d). However, it is very appealing that, with the irradiation of NIR light (3 W/cm2), the MoS2-Pen nanosheets exhibit outstanding antibacterial performance and can kill the majority of both S.aureus and E. coil (Figure 5a, c and d), indicating a superior antibiofilm activity. As a contrast, NIR light and MoS2 nanosheets with NIR light display poor antibacterial performance because the rising temperature triggered by NIR photothermal conversion is not high enough to directly kill bacteria.48 Therefore, this superior antibiofilm activity may be attributed

to

the

photothermal-induced

delicately

synergetic

effect.

The

photothermal-increased temperature can not only regulate the drug release and facilitate the drug diffusion into biofilm, but also influence the tissue structure of as-formed biofilm to further promote the diffusion of drug through the biofilm, as well as reduce the tolerance of bacteria on slow growth rates or dormant in the biofilm to Pen. This elegant synergetic effect of chemotherapy and photothermal therapy is used to harvest robust antibiofilm activity in the areas of healthcare, even though the concentration of Pen used in this experiment is below the minimal bactericidal concentration (MBC) for biofilm. In order to further demonstrate the reliability of above synergistic effect, a water bath (55 °C) experiment was used to replace the 11 ACS Paragon Plus Environment

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role of photothermal effect to carry out the similar antibiofilm experiment (Figure S19 in the Supporting Information). The results show that an excellent antibiofilm effect can be obtained only in the presence of water bath treatment and Pen treatment at the same time, which is in highly consistent with above-mentioned photothermal-induced synergistic effect. In addition, the antibiofilm performance is highly dependent on the concentration of MoS2 nanosheet (Figure S20 in the Supporting Information). Moreover, the cell viability of 3T3 fibroblasts was evaluated in detail (Figure 5b) in the presence of the as-exfoliated MoS2 nanosheets whether loaded drug or not. Both MoS2 and MoS2-Pen nanosheets possess high cell viability during the assay, demonstrating no toxicity and damage to healthy tissues. This is ascribed to the inherently excellent biocompatibility of MoS2 and the green exfoliation method without the participation of toxic materials. CONCLUSION In summary, we propose a facile, environment-friendly and versatile strategy to exfoliate TMDs into monolayer or few-layer nanosheets stabilized by polyphenol. Our results demonstrate that polyphenols are much better water-soluble stabilizer than those of ever reported, and it only takes 2 h to obtain high yield (∼ 60.5%) of monolayer MoS2 nanosheets dispersions under optimization condition, which is the fastest sonication-assisted aqueous exfoliation method up to date. Owing to the excellent biocompatibility, the high stability and the strong NIR light adsorption, the as-prepared high-quality MoS2 nanosheets have exceptional capability of serving as drug nanocarriers to load antibiotic Pen. In addition, the MoS2-Pen nanosheets exhibit outstanding antibiofilm activity via a synergetic teamwork of 12 ACS Paragon Plus Environment

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NIR-driven photothermal effect and antibiotics Pen released from the MoS2 nanosheet surface. Moreover, this work provides an appealing insight in the preparation of ultrathin 2D nanosheets, as well as brings great opportunities to investigate their potential properties. EXPERIMENTAL SECTION Materials. Molybdenum disulfide (MoS2), tungsten disulfide (WS2), molybdenum selenium (MoSe2), tungsten selenium (WSe2), epigallocatechin (EGC) and epigallocatechin gallate (EGCG) were purchased from Sigma-Aldrich (China). Tannic acid (TA, 1.7 kDa, AR) was obtained from Aladdin (China). Tea catechins were kindly provided from Xing Yuan Chemical Products Co., Ltd. (Henan, China). Bovine serum albumin (BSA, pI = 4.8, 67 kDa) and sodium alginate were acquired from Sinopharm Chemical Reagent Co., Ltd. (China). Dulbecco’s modified Eagle’s medium (DMEM) and penicillin were purchased from Genom Biomedical-tech (Hangzhou, China). All the reagents were used as received without further purification. The water used in all experiments was deionized and ultrafiltered to 18.2 MΩ·cm with an ELGA 136 LabWater system (France). Polyphenol-assisted aqueous exfoliation of TMDs nanomaterials. The exfoliation process was executed using ultrasonic cell crusher with a tunable power from 0 to 450 W. The tip of ultrasonic cell crusher can utilize strong ultrasound to produce cavitation effect in liquid to cause the solid particles or cellular tissue in liquid to break up, which is more powerful ultrasonic method than that of conventional bath sonication treatment. In brief, 120 mg MoS2 powder was added into 60 mL aqueous solution containing 60 mg tannic acid, and then the suspensions were sonicated under 300 W for 0.5, 1, 1.5, 2, 3 and 4 h. Finally, the supernatant 13 ACS Paragon Plus Environment

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MoS2 nanosheets were collected after centrifugation at 6000 rpm for 15 min to remove unexfoliated MoS2. Alternatively, various polyphenols (EGC, EGCG and tea catechins) were used to replace tannic acid for preparing MoS2 nanosheets under the similar procedure. In addition, other excellent stabilizers such as sodium alginate26 and bovine serum albumin (BSA)30 were also used to carry out the similar experiment, which acts as references to compare with our approach. Note that the ultrapure water (pH ≈ 6.0) was used during all the exfoliation experiments to prevent the aggregation of exfoliated nanosheets via oxidative crosslinking of polyphenols. Our exfoliation approach was also suitable for producing other TMDs (WS2, MoSe2, WSe2, etc.) nanosheets. Typically, 120 mg TMDs powder was added into 60 mL aqueous solution containing 60 mg tannic acid, and then the suspensions were sonicated under 300 W for 2 h. Finally, the supernatant TMDs nanosheets were collected after centrifugation at 6000 rpm for 15 min to totally remove unexfoliated TMDs. Binding energy simulation. Simulated annealing method was used to evaluate the physical adsorption of various molecules on MoS2 nanosheets.49 It was performed under cvff force field on the Material Studio 2017 R2 with Adsorption Locator module. First, all the molecules and the MoS2 (0 0 1) layer were constructed and geometrically optimized using the Forcite module. The MoS2 layer was modeled using 12 × 12 supercells. The vacuum slam was set as 50 Å to avoid any non-bond interactions between two adjacent layers. Then, in performing the Adsorption Locator simulation, the molecule was randomly distributed over the MoS2 layer. The optimal configuration was determined by carrying out a Monte Carlo 14 ACS Paragon Plus Environment

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simulation on the configurational space of the molecule within the surface region. The max adsorption distance was set as 15 Å. The binding energy (Eb) of the given molecules on MoS2 layer is calculated as Eb = EMoS2-molecule – EMoS2 – Emolecule, where Emolecule, EMoS2, and EMoS2-molecule are the energies of the bound molecule, the MoS2 layer, and the complex of MoS2 and molecule, respectively. Release experiment of Pen from the MoS2-Pen. First, a solution of MoS2 or MoS2-Pen (4.43 mg) in PB (pH 5.5) was placed in a bottle and irradiated with an 808 nm NIR laser at a power density of 2.0 W/cm2 over a period of 10 min, respectively. After irradiation, 1 mL of treated solution was taken out and centrifuged by ultrafiltration at 5000 rpm for 10 min. The released TA or Pen was then quantified by UV-vis spectra. Moreover, a solution of MoS2 or MoS2-Pen (4.43 mg) in PB (pH 5.5) without NIR laser irradiation was stored at room temperature for 60 min, respectively. Then, 1 mL of solution was taken out and centrifuged by ultrafiltration at 5000 rpm for 10 min. The released TA or Pen was then quantified by UV-vis spectra. Finally, the ratio of TA or Pen released from MoS2 or MoS2-Pen was calculated. Culturing and Harvesting MRSA Biofilm. S. aureus (ATCC 6538, bought from China General Microbiological Culture Collection Center) and E. coli (ATCC 8739, bought from China General Microbiological Culture Collection Center) were employed in this study. For culturing S. aureus biofilm, a 100 μL droplet of a S. aureus suspension (108 bacteria/mL) and 100 μL tryptone soy broth medium (TSB) were placed on 96 well plates to culture at 37 °C. After 24 h, TSB medium was replaced with fresh TSB and the biofilm was grown for another 15 ACS Paragon Plus Environment

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24 h. Finally, the TSB medium was removed, and the S. aureus biofilm attached on 96 well plates was harvested. The culture method of E. coli is similar to the method aforementioned. Standard plate counting assays. After NIR irradiation, 100 µL sterile PBS was added into each well in 96 well plates. The plate was sonicated and then blown and inhaled by pipette carefully to disperse the biofilms. The suspensions were serially diluted with sterile PBS and 100 µL diluted samples were spread on the tryptone soy agar (TSA) plates. After incubation at 37 °C for 12 h, the colonies formed were counted. Live/Dead staining assays. After NIR irradiation, the wells in 96 well plates were washed with sterile PBS slightly and then biofilms in 96 well plates were incubated using BacLight Live/Dead dye in dark for 15 minutes. After incubation, the redundant dye was washed by sterile PBS slightly for three times. At last, the biofilms in 96 well plates were observed under fluorescence microscope. Cell viability assays. The cell viability of MoS2 and MoS2-Pen nanosheets were evaluated by MTT assays. 3T3 fibroblast cells were used as model cells and seeded into 96 well plates (8000 cells per well) with 180 μL DMEM culturing medium each well for 24 hours. MoS2 and MoS2-Pen nanosheets solution with different concentrations were added to the cells, respectively. After incubation for 48 hours, 20 μL MTT solution (0.1 mg/ml) was added to each well and cultured for another 4 hours. Then the medium was removed and 150 mL DMSO was added to each well to dissolve the obtained crystals. The absorbance was recorded at 570 nm by a microplate reader (MODEL 550, Bio Rad).


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Characterization. The topologies (size and thickness) of as-exfoliated TMDs nanosheets were examined by atomic force microscopy (AFM, Veeco, USA). The morphology of as-exfoliated TMDs nanosheets was further observed by transmission electron microscope (TEM, JEM-1230, Japan) at 80 kV in bright-field mode. UV-vis absorption of the TMDs nanosheets dispersions was measured with an ultraviolet spectro-photometer (UV 2450, Shimadzu, Japan). The exfoliation concentration and yield of as-obtained MoS2 nanosheets dispersions were calculated by two methods: measuring the mass of MoS2 after freeze drying the exfoliated dispersions (adsorbed TA on as-exfoliated nanosheets surface was subtracted from TGA analysis) and UV-vis absorption spectra.30 The crystal structure of MoS2 nanosheets was detected through X-ray diffraction (XRD, Rigaku Corporation, Japan) using a Rigaku D/Max-2550PC X-ray diffractometer and Cu as the anode material (Kα1 wavelength = 1.54 nm). The drug loading was measured by thermogravimetric analysis (TGA, TGA-2050, USA) on a Perkin-Elmer Series 7 analyzer under a N2 flow (30 mL/min) at a heating rate of 10 °C/min. The chemical structure of MoS2 nanosheets before and after loaded antibiotic Pen was collected by fourier transform infrared (FTIR, Nicolet FTIR/Nexus 470, USA) spectra using KBr pellets. The zeta-potential of MoS2 nanosheets dispersions before and after loaded antibiotic Pen was measured at 25 °C using a Delsa Nano C particle analyzer (Beckman Coulter Ireland Inc., USA) in PBS (10 mM) from pH 4 to 10. ASSOCIATED CONTENT Supporting Information


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This Supporting Information material is available free of charge via the Internet at http://pubs.acs.org. Details of digital pictures of the exfoliated MoS2 nanosheets in TA solution (Figure S1), color of MoS2 before and after exfoliation (Figure S2), exfoliation yield of the MoS2 nanosheets under different sonication time points and powers (Figure S3), exfoliation result of the MoS2 nanosheets in TA solution using conventional bath sonication tool (Figure S4), UV-vis absorption spectra of exfoliated MoS2 nanosheets using sodium alginate and BSA solution (Figure S5), colloidal stability of the as-exfoliated MoS2 nanosheets using TA (Figure S6), XRD spectra of bulk MoS2 powders and MoS2 nanosheet (Figure S7), TEM image and corresponding elements mapping images of the exfoliated MoS2 nanosheets (Figure S8), zeta potential of MoS2 nanosheets dispersions (Figure S9), colloidal stability of the as-exfoliated MoS2 nanosheets using different polyphenols (Figure S10), AFM image, corresponding lateral sizes and thickness of the exfoliated TMDs nanosheets(Figure S11), large-scale exfoliation of MoS2 (Figure S12), molecular structure of antibiotic penicillin (Figure S13), stability of MoS2-Pen under different conditions (Figure S14 and S15), release amount of TA and Pen from MoS2 nanosheets in the absence and presence of 808 nm NIR laser (Figure S16 and S17), release profile of Pen from MoS2 nanosheets (Figure S18), antibiofilm activity under bath water treatment (Figure S19) and Number of (a) S.aureus and (b) E.coli treated with different antibacterial agents at different concentrations (Figure S20). The authors declare no competing financial interest. 18 ACS Paragon Plus Environment

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AUTHOR INFORMATION Corresponding Author E-mail: [email protected], [email protected], [email protected].

Author Contributions †

C. Zhang, D. F. Hu and J. W. Xu contributed equally to this work.

ACKNOWLEDGMENT Financial support is acknowledged to the National Natural Science Foundation of China (Grant no. 21534009) and the Fundamental Research Funds for the Central Universities (Grant no. 2017XZZX001-03B). The authors thank Dr. Hong-Qing Liang from University of Texas at San Antonio (USA) for the simulation and analysis of binding energy between one molecule and one MoS2 nanosheet. We are grateful for the support of the Research Computing Center in College of Chemical and Biological Engineering at Zhejiang University for assistance with the calculations carried out in this work

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28. Zeng, Z.; Sun, T.; Zhu, J.; Huang, X.; Yin, Z.; Lu, G.; Fan, Z.; Yan, Q.; Hng, H. H.; Zhang, H. An Effective Method for the Fabrication of Few-Layer-Thick Inorganic Nanosheets. Angew. Chem., Int. Ed. 2012, 51, 9052-9056. 29. Jawaid, A.; Nepal, D.; Park, K.; Jespersen, M.; Qualley, A.; Mirau, P.; Drummy, L. F.; Vaia, R. A. Mechanism for Liquid Phase Exfoliation of MoS2. Chem. Mater. 2015, 28, 337-348. 30. Guan, G.; Zhang, S.; Liu, S.; Cai, Y.; Low, M.; Teng, C. P.; Phang, I. Y.; Cheng, Y.; Duei, K. L.; Srinivasan, B. M.; Zheng, Y.; Zhang, Y.-W.; Han, M.-Y. Protein Induces Layer-by-Layer Exfoliation of Transition Metal Dichalcogenides. J. Am. Chem. Soc. 2015, 137, 6152-6155. 31. Guan, G.; Xia, J.; Liu, S.; Cheng, Y.; Bai, S.; Tee, S. Y.; Zhang, Y. W.; Han, M. Y. Electrostatic-Driven Exfoliation and Hybridization of 2D Nanomaterials. Adv. Mater. 2017, 29, 1700326. 32. Ravula, S.; Essner, J. B.; Baker, G. A. Kitchen-Inspired Nanochemistry: Dispersion, Exfoliation, and Hybridization of Functional MoS2 Nanosheets Using Culinary Hydrocolloids. ChemNanoMat 2015, 1, 167-177. 33. Jia, W.; Tang, B.; Wu, P. Nafion-Assisted Exfoliation of MoS2 in Water Phase and the Application in Quick-Response NIR Light Controllable Multi-Shape Memory Membrane. Nano Res. 2018, 11, 542-553. 34. Vega‐Mayoral, V.; Backes, C.; Hanlon, D.; Khan, U.; Gholamvand, Z.; O'Brien, M.; Duesberg, G. S.; Gadermaier, C.; Coleman, J. N. Photoluminescence from Liquid-Exfoliated WS2 Monomers in Poly (vinyl alcohol) Polymer Composites. Adv. Funct. Mater. 2016, 26, 1028-1039. 35. Yuan, Y.; Li, R.; Liu, Z. Establishing Water-Soluble Layered WS2 Nanosheet as a Platform for Biosensing. Anal. Chem. 2014, 86, 3610-3615. 36. Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. Mussel-Inspired Surface Chemistry for Multifunctional Coatings. Science 2007, 318, 426-430. 37. Zhang, C.; Ou, Y.; Lei, W. X.; Wan, L. S.; Ji, J.; Xu, Z. K. CuSO4/H2O2-Induced Rapid Deposition of Polydopamine Coatings with High Uniformity and Enhanced Stability. Angew. Chem. 2016, 128, 3106-3109. 38. Zhang, C.; Gong, L.; Xiang, L.; Du, Y.; Hu, W.; Zeng, H.; Xu, Z.-K. Deposition and Adhesion of Polydopamine on the Surfaces of Varying Wettability. ACS Appl. Mater. Interfaces 2017, 9, 30943-30950. 39. Sileika, T. S.; Barrett, D. G.; Zhang, R.; Lau, K. H. A.; Messersmith, P. B. Colorless Multifunctional Coatings Inspired by Polyphenols Found in Tea, Chocolate, and Wine. Angew. Chem., Int. Ed. 2013, 52, 10766-10770. 22 ACS Paragon Plus Environment

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Figure 1. (a) Molecular structures of natural polyphenols: EGC, EGCG and ECG. Tea catechins mainly contain EGC, EGCG and ECG. (b) Schematic illustration for the polyphenol-assisted aqueous exfoliation process of TMDs under sonication. The bulk TMDs crystal comprises a laminated structure with a lot of monolayers assembled via the weak van der Waals interactions. The form of polyphenol molecular is a typical 3D model to briefly describe its stereochemical configuration, namely Space Filling scale model.


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Figure 2．(a) UV-vis absorption spectra of the exfoliated MoS2 nanosheets in TA solution after sonication at different time points. (b) Low-resolution TEM and (c) High-resolution TEM images of the exfoliated MoS2 nanosheets. The insets in (c) are the fast Fourier transform pattern and crystal structures of MoS2. (d) AFM image of the MoS2 nanosheets exfoliated in tannic acid solution for 2 h sonication. Histograms of (e) MoS2 nanosheet lateral sizes and (f) MoS2 nanosheet thickness by statistical analysis. (g) The optimized structures and binding energies of one TA molecule and monolayer MoS2 nanosheet calculated by the simulated annealing method using Material Studio 2017 R2 with Adsorption Locator module. (h) Comparison on the binding energies of different motifs on monolayer MoS2 nanosheet surface calculated by the simulated annealing method using Material Studio 2017 R2 with Adsorption Locator module. The sonication power is 300 W. The concentration of bulk MoS2 crystals and tannic acid is 2 mg/mL and 1 mg/mL, respectively. 25 ACS Paragon Plus Environment

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Figure 3．UV-vis absorption spectra and corresponding digital pictures of the exfoliated MoS2 nanosheets in different polyphenol solutions after 2 h sonication: (a) Epigallocatechin (EGC), (b) Epigallocatechin gallate (EGCG) and (c) Tea catechins (EGC, ECG and EGCG). UV-vis absorption spectra and corresponding digital pictures of other TMDs nanosheets in TA solution after sonication: (d) WS2, (e) MoSe2 and (f) WSe2. The sonication power is 300 W. The concentration of bulk TMDs and polyphenol is 2 mg/mL and 1 mg/mL, respectively. The sonication time for WS2, MoSe2 and WSe2 is fixed at 2 h.


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Figure 4．(a) Schematic illustration for the loading of Pen onto the MoS2 nanosheets. (b) Digital pictures of MoS2-Pen at different pH values after incubation of 72 h. (c) Zeta-potential of MoS2 nanosheets and MoS2-Pen nanosheets in water with different pH values. (d) FT-IR spectra of MoS2 and MoS2-Pen nanosheets. (e) Thermogravimetric analysis (TGA) curve of MoS2 nanosheets. (f) Temperature increase of MoS2-Pen solutions with different concentrations as a function of NIR laser irradiation time. (g) Temperature increase of MoS2-Pen solutions with different NIR laser powers as a function of irradiation time. (h) Photothermal effect of the irradiation of MoS2-Pen solutions with the NIR laser (3 W/cm2). The laser was shut off after irradiation for 10 min. The concentration of MoS2-Pen is 4.43 mg/mL. The inset: Infrared thermal images of MoS2-Pen solution when irradiated for 10 min. All the experiments were executed at room temperature. High concentration of MoS2 nanosheets was concentrated from the as-exfoliated MoS2 nanosheets by TA after sonication in water at 300 W for 2 h.


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Free Pen

(d) E.coli Free Pen

Figure 5．(a) Number of S.aureus and E. coil in the presence of different antibacterial agents: control, NIR light, MoS2 nanosheets, free Pen, MoS2-Pen nanosheet, MoS2 nanosheets with NIR light and MoS2-Pen nanosheets with NIR light. (b) Cell viability of 3T3 fibroblasts treated with MoS2 and MoS2-Pen nanosheets at different concentrations for 12 h incubation. Fluorescence micrographs of (c) S.aureus and (d) E. coil treated with different antibacterial agents: control, NIR light, MoS2 nanosheets, free Pen, MoS2-Pen nanosheet, MoS2 nanosheets with NIR light and MoS2-Pen nanosheets with NIR light. Green and red fluorescence represent live and dead bacteria, respectively. The power and treatment time of NIR laser are 3 W/cm2 and 20 min, respectively. 28 ACS Paragon Plus Environment

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ACS Nano

Table 1. Comparison of those aqueous exfoliation methods using different water-soluble stabilizers for the preparation of TMDs nanosheets. Stabilizer

Time (h) × Power (W)

Concentration of bulk material (mg/mL)

Concentration of exfoliated nanosheets (mg/mL) and exfoliation yield (%) MoS2

Ref.

WS2

BSA

48 × 100

5.0

1.36

27.2

/

/

[30]

Sodium alginate

20 × 200

7.5

0.65

8.7

1.39

18.5

[26]

BSA

48 × 100

4.0

0.60

15.0

/

/

[31]

/

4 × 100

10.0

/

/

0.09

0.9

[12]

Tannic acid

8×/

10.0

0.15

1.5

/

/

[32]

PAA

6 × 100

7.5

/

/

0.66

8.8

[35]

PSS

8×/

5.0

0.44

8.8

/

/

[33]

PVA

1×750

30.0

/

/

0.5

1.7

[34]

Tannic acid

2 × 300

2.0

1.21

60.5

0.85

42.5

This work

Tannic acid

2 × 100

2.0

0.93

46.5

0.60

30.0

This work

*The aqueous pH value in Ref. [31] and [33] is 4 and 1, respectively. *An ultrasonic cell crusher was employed as the exfoliation power in this work, whereas the other reports (Ref. 12, 26, 30-35) adopted a bath sonication treatment.


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Table of Contents Graphic


Polyphenol-Assisted Exfoliation of Transition Metal Dichalcogenides

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