Enhanced Photothermal Bactericidal Activity of the Reduced

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Enhanced Photothermal Bactericidal Activity of the Reduced Graphene Oxide Modified by Cationic Water-Soluble Conjugated Polymer Linhong Xiao, Jinhua Sun, Libing Liu, Rong Hu, Huan Lu, Chungui Cheng, Yong Huang, Shu Wang, and Jianxin Geng ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b14473 • Publication Date (Web): 23 Jan 2017 Downloaded from http://pubs.acs.org on January 24, 2017

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ACS Applied Materials & Interfaces

Enhanced Photothermal Bactericidal Activity of the Reduced Graphene Oxide Modified by Cationic Water-Soluble Conjugated Polymer Linhong Xiao,†,§ Jinhua Sun,† Libing Liu,‡ Rong Hu,‡ Huan Lu,‡ Chungui Cheng,† Yong Huang,† Shu Wang,‡ and Jianxin Geng*,† †

Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, 29 Zhongguancun East Road, Haidian District, Beijing 100190, China

‡

Beijing National Laboratory for Molecular Sciences, Key Laboratory of Organic Solids, Institute of Chemistry, Chinese Academy of Sciences, Beijing 100190, China §

University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing, 100049, China

ABSTRACT: Surface modification of graphene is extremely important for applications. Here, we report a grafting-through method for grafting water-soluble polythiophenes onto reduced graphene oxide (RGO) sheets. As a result of tailoring of the sidechains of the polythiophenes, the modified RGO sheets, i.e., RGO-g-P3TOPA and RGO-g-P3TOPS, are positively and negatively charged, respectively. The grafted water-soluble polythiophenes provide the modified RGO sheets with good dispersability in water and high photothermal conversion efficiencies (ca. 88%). Notably, the positively charged RGO-gP3TOPA exhibits unprecedentedly excellent photothermal bactericidal activity because the electrostatic attractions between RGO-g-P3TOPA and E. coli bind them together, facilitating direct heat conduction through their interfaces: the minimum concentration of RGO-g-P3TOPA that kills 100% of E. coli is 2.5 µg mL−1, which is only one-sixteenth of that required for RGO-g-P3TOPS to exhibit a similar bactericidal activity. The direct heat conduction mechanism is supported by zeta-potential measurements and photothermal heating tests, in which the achieved temperature of the RGO-gP3TOPA suspension (2.5 µg mL−1, 32 °C) that kills 100% of E. coli is found to be much lower than the

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thermoablation threshold of bacteria. Therefore, this research demonstrates a novel and superior method that combines photothermal heating effect and electrostatic attractions to efficiently kill bacteria.

KEYWORDS: Graphene, water-soluble conjugated polymers, covalent functionalization, electrostatic attraction, photothermal killing of bacteria

INTRODUCTION Surface modification of graphene is extremely important for applications such as photovoltaic devices,1 photodetectors,2 supercapacitors,3 biomedicine,4 and polymer-based nanocomposites.5 Graphene oxide (GO) sheets are an important derivative of graphene; they comprise many oxygencontaining functional groups, which enable various approaches for surface modification, including both non-covalent and covalent strategies.6,7 Non-covalent modifications are advantageous in simple operations and are usually based on π−π stacking, hydrogen-bond interactions, or electrostatic interactions.8,9 Covalent modifications provide stronger binding between the GO sheets and the grafted moieties, leading to more stable composite structures.10 Covalent approaches are based primarily on reactions between functional molecules and the oxygen-containing groups or the −C=C− bonds on the basal planes of GO sheets.11,12 Compared with non-covalent approaches, covalent approaches are more beneficial to stable composite structures and high-efficient intermolecular electron transfer in the composites.13−15 To date, the surface modification of GO sheets has been widely investigated using neutral and negatively charged molecules/polymers because they avoid precipitation of the GO sheets resulting from cancellation of GO sheets’ negative charges by positively charged molecules/polymers.16−18 Recently, we developed methods for preparing reduced graphene oxide (RGO)-polythiophene

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composites, including covalent functionalization of RGO sheets using poly(3-hexylthiophene)12−14 and non-covalent modification of RGO sheets using a negatively charged polythiophene.19 However, negatively charged RGO sheets cannot be used for assembly with negatively charged moieties such as DNA, RNA, and bacteria because of electrostatic repulsions.20 A few positively charged RGO sheets, e.g., polyethyleneimine-grafted GO, have been used for drug nanocarriers,21 gene delivery,20 and immobilization of inorganic polyanions.22 The development of positively charged RGO sheets containing a broad range of functional polymers is critical for expanding the applications of graphene materials. Among functionalized polymers, ionic water-soluble conjugated polymers (WSCPs) comprising conjugated aromatic backbones and ionic sidechains have drawn considerable attention because of their designable molecular structures,23−25 good solubilities in water, intriguing optoelectronic properties, and wide applications in various sensors.26−28 However, the surface modification of GO sheets using ionic WSCPs, particularly using cationic WSCPs (positively charged), via covalent bonding has not been developed. The photothermal effect of RGO-based materials has been studied recently in various areas, including photocontrolled switches,13 light-controlled actuators,29 photothermal miniature reactors,30 photothermally induced drug delivery,31 and photothermal therapy.32,33 RGO can absorb light from the UV to near-infrared (NIR) region and convert the absorbed light into heat through nonradiative decay.34 Compared with other photothermal nanomaterials such as gold-based nanoparticles,35,36 organic nanoparticles,37 and carbon nanotubes (CNTs),38,39 RGO is more attractive because of its facile accessibility, high optical absorption from the UV to the NIR region, good photostability, and good photothermal heating effect at its high reduced state.13,32 Notably, grafting conjugated polymers onto RGO sheets can further improve the photothermal heating effect of the resultant RGO-based materials

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because of the enhanced optical absorption and the photoinduced electron transfer in the resultant composites.13 Herein, we report positively and negatively charged RGO composites prepared by covalently grafting poly(3-(3′-thienyloxy)propyltrimethylammonium bromide) (P3TOPA, a cationic conjugated polymer) and poly(sodium 3-(3′-thienyloxy)propanesulfonate) (P3TOPS, a anionic conjugated polymer) to RGO sheets via a chemical oxidation polymerization of thiophene monomers using a graftingthrough method. The composites were designated as RGO-g-P3TOPA and RGO-g-P3TOPS, respectively. The positively charged RGO-g-P3TOPA was obtained by quaternization of its neutral counterpart. The incorporation of the WSCPs, i.e., P3TOPA and P3TOPS, maintains good dispersability of the RGO sheets in water; it also enhances the photothermal heating effect of the RGO because of the enhanced optical absorption and photoinduced electron transfer from the WSCPs to RGO.13 Notably, the positively charged RGO-g-P3TOPA readily binds to negatively charged Escherichia coli (E. coli) through electrostatic attractions, facilitating direct heat conduction through their interfaces for the efficient photothermal killing of bacteria. As a result, 100% of E. coli can be killed using a RGO-gP3TOPA suspension with a concentration as low as 2.5 µg mL−1, which is only one-sixteenth of the concentration required for the negatively charged RGO-g-P3TOPS to obtain a similar bactericidal effect. This research demonstrates a new and superior method that combines the photothermal heating effect and electrostatic attractions for the efficient photothermal killing of bacteria. Moreover, the systematic modifications of RGO sheets using WSCPs will potentially open new applications of RGO materials in biology, photofunctional materials, and sensing.

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RESULTS AND DISCUSSION Synthesis and characterization of the RGO-g-P3TOPS and the RGO-g-P3TOPA composites. Scheme 1. Surface modification of GO sheets with water-soluble polythiophene derivatives. (a) The RGO-g-P3TOPS composite. (b) The RGO-g-P3TOPA composite.

The RGO-g-P3TOPS and the RGO-g-P3TOPA composites were synthesized via a grafting-through method, as illustrated in Scheme 1. GO sheets were first modified using a thiophene monomer, 3-(3′bromo)propoxythiophene (3BPT), through nucleophilic substitution reactions of carboxylic acid and

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hydroxyl groups. The intermediate product was designated as RGO-g-3BPT. Next, the negatively charged RGO-g-P3TOPS was synthesized by chemical oxidation polymerization of 3TOPS in the presence of the RGO-g-3BPT (Scheme 1a). For the synthesis of positively charged RGO-g-P3TOPA, direct polymerization of 3TOPA in the presence of the RGO-g-3BPT was difficult because the electrostatic attractions between RGO-g-3BPT and the positively charged monomer led to precipitation of the RGO-g-3BPT. Therefore, a neutral RGO-g-P3BPT was first synthesized by chemical oxidation polymerization of 3BPT in the presence of the RGO-g-3BPT, followed by quaternization of the RGO-gP3BPT using trimethylamine to obtain positively charged RGO-g-P3TOPA. During the multiplestepped synthesis process, GO was converted into RGO.40 Therefore, all names of the intermediates and final products include “RGO”. In this research, polythiophene derivatives were used to modify RGO due to their popularity and good stabilities. The water-dispersible feature of the resultant composites, which was readily evidenced by the formation of stable aqueous suspensions (Figure S1), extended the applications to broader areas such as biological technology. Meanwhile, the grafting-through method shows advantages in simple operations and versatility for structural design over other synthesis approaches such as grafting-to method. The successful synthesis of dispersible RGO sheets carrying with positively charged conjugated polymer is a significant progress in the area of graphene materials. As discussed later, the positively charged RGO-g-P3TOPA exhibited very high photothermal conversion efficiency and photothermal bactericidal activity compared with other photothermal nanomaterials.

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Figure 1. Composition of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites. (a, b) XPS survey and C 1s XPS spectra of the RGO-g-P3TOPA. (c) TGA curves of GO, RGO-g-P3TOPA and RGO-gP3TOPS. (d) Raman spectra of GO, RGO-g-P3TOPA and RGO-g-P3TOPS.

The structures of the RGO-g-P3TOPS and the RGO-g-P3TOPA composites were confirmed by FT-IR spectroscopy (Figure S2). X-ray photoelectron spectroscopy (XPS) data confirmed the conversion of GO to RGO and the covalent functionalization of RGO with P3TOPA and P3TOPS: a decreased signal of the C−O species and the appearance of new signals corresponding to C−N and C−S species were detected in the XPS spectra of these two composites (Figure 1a and 1b for RGO-gP3TOPA, Figure S3 for RGO-g-P3TOPS). The RGO-g-P3TOPA and RGO-g-P3TOPS composites comprised approximately 25% P3TOPA and P3TOPS, respectively, as measured by thermogravimetric analysis (TGA) (Figure 1c). In addition, the G band of the RGO component in the Raman spectra of the composites exhibited high-frequency shifts with respect to that of pristine GO (Figure 1d). These shifts

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suggest that charge transfer occurred between the conjugated polymers, i.e., P3TOPA and P3TOPS, and RGO basal planes in the composites.41 The Raman spectra of the composites contained overwhelmed Raman signals of the conjugated polymers because they have a higher capability to generate Raman signals than graphene materials.12

Figure 2. Morphology of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites. (a, b) TEM images of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets. (c, d) AFM images of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets.

To investigate the morphology and size of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets, the composites were observed using transmission electron microscopy (TEM) and atomic force microscopy (AFM). The TEM images revealed polymer aggregates attached to the surfaces of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets (Figure 2a and 2b); these aggregates led a higher contrast and rougher surface for the composite sheets compared to the GO sheets (Figure S4). These features were also confirmed by AFM observations (Figure 2c and 2d): cross-section analysis indicated that the RGO-gP3TOPA sheets are ca. 5.5 nm thick and that the RGO-g-P3TOPS sheets are ca. 5.3 nm thick. 8


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Additional TEM and AFM images of these composites are provided in the Supporting Information (SI) (Figure S5 and S6). The thicknesses of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets were determined to range from ca. 4.5 to 8 nm based on AFM observations. These values are greater than the thickness of GO sheets (ca. 0.8 nm, Figure S4) because of the P3TOPA and P3TOPS covalently attached to the surfaces of the RGO basal planes. The conjugated polymers should be grafted onto both sides of the RGO basal planes because the reactive functional groups, i.e., carboxylic acid and hydroxyl groups, are situated on both sides of the GO sheets. In addition, the dimensions of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets were found to be smaller than those of the GO sheets (ca. hundreds of nanometers for the former and ca. microns for the latter) because of the sonication step in the synthesis process. The data obtained from dynamic light scattering measurements supported that the RGO-gP3TOPA and the RGO-g-P3TOPS sheets had average sizes of hundreds of nanometers. The zetapotential values of the RGO-g-P3TOPA and RGO-g-P3TOPS composites were measured to be ca. 40.2 and ca. −25.1 mV, respectively, illustrating the opposite charging features of the RGO-g-P3TOPA and RGO-g-P3TOPS sheets. Compared with negatively charged RGO sheets, positively charged RGO sheets have been rarely reported, particularly in the case of sheets obtained by grafting of cationic conjugated polymers.

Electronic properties of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites. To investigate the electronic properties of the RGO-g-P3TOPA and RGO-g-P3TOPS composites, UV-visible (UV-Vis) and photoluminescence (PL) spectra were collected. Figure 3a shows the UV-Vis spectra for the RGO-g-P3TOPA suspension, GO suspension, and P3TOPA solution in deionized (DI) water. Compared with the GO suspension, the RGO-g-P3TOPA suspension yielded an optical absorption spectrum that contains a featured absorption peak of P3TOPA at 508 nm, an enhanced

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optical absorption from the UV to the NIR region, and a red-shifted absorption maximum of GO (from ca. 233 to 268 nm). The enhanced optical absorption from the UV to the NIR region, as well as the redshifted absorption maximum of GO, is ascribed to the restoration of the π conjugated structures in the resultant RGO materials (Figure 3a).13,34,42 A P3TOPA solution showed an optical absorption spectrum containing an absorption maximum at ca. 488 nm, corresponding to the π−π* transition of the conjugated main chains. Interestingly, the P3TOPA component in the RGO-g-P3TOPA exhibited a redshifted absorption maximum at ca. 508 nm. This finding suggests an increased electron delocalization along the polymer main chains, i.e., a reduced bandgap, because of the interactions between the P3TOPA chains and the RGO basal planes.43 The same phenomena were observed in the optical absorption spectrum of the RGO-g-P3TOPS suspension, which exhibits enhanced optical absorption in the wavelength range from the UV to the NIR region and characteristic absorption maxima of RGO (ca. 268 nm) and P3TOPS (ca. 770 nm) (Figure 3b). The conversion of GO to RGO in the synthesis was verified by XPS measurement (Figure 1a, 1b, and Figure S3).

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Figure 3. Electronic properties of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites. (a) UVVis spectra of the RGO-g-P3TOPA, GO, and P3TOPA suspensions or solutions in DI water. (b) UV-Vis spectra of the RGO-g-P3TOPS, GO, and P3TOPS suspensions or solutions in DI water. (c) PL spectra of the P3TOPA solution and the RGO-g-P3TOPA suspension in DI water. (d) PL spectra of the P3TOPS solution and the RGO-g-P3TOPS suspension in DI water. The concentrations of the RGO-gP3TOPA and RGO-g-P3TOPS suspensions are 40 µg mL−1; the concentrations of the GO suspension, the P3TOPA solution, and the P3TOPS solution are 30, 10, and 10 µg mL−1, respectively, which are equivalent to the concentrations of their components in the composites.

The photoinduced electron transfer in the RGO-g-P3TOPA and RGO-g-P3TOPS composites were also studied using PL spectroscopy. With an excitation wavelength of 480 nm, the P3TOPA solution generated a PL spectrum containing an emission peak at 573 nm (Figure 3c). As expected, the PL emission of the P3TOPA component was completely quenched by RGO in the RGO-g-P3TOPA composite, indicating photoinduced electron transfer from P3TOPA to RGO.19 The complete quenching of P3TOPA’s PL emission is possibly due to both the covalent bonding of P3TOPA chains to RGO basal planes and the electrostatic attractions between the two components. Therefore, P3TOPA and RGO form a donor-acceptor system. The light absorbed by RGO-g-P3TOPA is thermally dissipated into the suspension through nonradiative decay.34 In contrast to RGO-g-P3TOPA, the PL emission of the P3TOPS component in the RGO-g-P3TOPS composite was not fully quenched (Figure 3d). This incomplete quenching might reflect the less intimate interactions between P3TOPS and the RGO basal planes compared with those in the RGO-g-P3TOPA composite because of the electrostatic repulsions between the negatively charged RGO basal planes and P3TOPS chains. Although both P3TOPA and P3TOPS were tethered to the surfaces of RGO through the same linkage, the opposite charges on their

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flexible main chains would cause different interactions between the respective main chains and the RGO basal planes.

Photothermal heating and bactericidal properties of the RGO-g-P3TOPA and the RGO-gP3TOPS composites.

Figure 4. Photothermal heating curves for the suspensions of (a) RGO-g-P3TOPA composite and (b) RGO-g-P3TOPS composite with various concentrations in DI water.

The RGO-g-P3TOPA and RGO-g-P3TOPS composites exhibited good photothermal heating effects (Figure 4a and 4b). Under low-powered irradiation (532 nm, 0.79 W cm−2) for 10 min, the suspensions of the RGO-g-P3TOPA and RGO-g-P3TOPS composites in DI water with concentrations of 40 µg mL−1 exhibited rapid temperature increases from ca. 20 to 60 °C, which is higher than the 12


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thermoablation threshold of bacteria (50 °C).44 The photothermal conversion efficiency (η), which reflects the capability of the composites to convert absorbed light into thermal energy, were calculated to be 88.5% for RGO-g-P3TOPA and 88.1% for RGO-g-P3TOPS from their temperature decay curves obtained after irradiation was stopped (Figure S7).45 These values are higher than those of their respective components, i.e., 54.6% for P3TOPA, 48.4% for P3TOPS, and 56.0% for GO. In addition, the η values exhibited by our WSCP-modified RGO sheets are substantially higher than previously reported values for inorganic photothermal materials such as gold and copper chalcogenide nanoparticles (ranging from ca. 36 to 53%)46,47 and organic photothermal materials such as polyaniline, polypyrrole, and poly(3,4-ethylenedioxythiophene) (ranging from ca. 44 to 50%).48−50 Such high η values for our WSCP-modified RGO sheets are attributed to the high optical absorption, the photoinduced electron transfer from the WSCPs to RGO basal planes in the composites,13 and the efficient photothermal conversion of RGO sheets through nonradiative decay.32,34 The photothermal heating curves of the RGO-g-P3TOPA and RGO-g-P3TOPS composites were also collected by decreasing the concentration of their suspensions (Figure 4a and 4b). Temperature versus concentration plots indicated that RGO-g-P3TOPA exhibited slightly higher photothermal heating effect than RGO-gP3TOPS at relatively higher concentrations (e.g. 40 µg mL−1); but the differences between their photothermal heating effects were greater at relatively lower concentrations (right Y axis in Figure 5c and 5d and Figure S8).

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Figure 5. Photothermal bactericidal tests of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites. (a, b) Photothermal bactericidal activities toward E. coli of the suspensions of RGO-g-P3TOPA and RGO-g-P3TOPS composites with various concentrations in the dark and under irradiation for 10 min. (c, d) The correlation between the photothermal heating capabilities and the photothermal bactericidal activities for the suspensions of the RGO-g-P3TOPA and RGO-g-P3TOPS composites.

Because the RGO-g-P3TOPA and RGO-g-P3TOPS composites exhibit outstanding photothermal heating effects and good dispersability in water, we used them as photothermal bactericidal agents for killing E. coli, which is a widely used Gram-negative bacterium. Photothermal bactericidal experiments were performed using a surface plating method, and the survival rates were evaluated by counting the bacterial colonies (see Figure S9 for the photographs of E. coli colonies). As a control, the bactericidal 14


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experiments were performed in the presence of a photothermal bactericidal agent but in the dark. Photothermal bactericidal experiments were first performed using the RGO-g-P3TOPA suspension with a concentration of 10 µg mL−1. As shown in Figure 5a, the survival rate of the E. coli treated in the dark was ca. 92%, indicating that the alkalinity of RGO-g-P3TOPA does not show a remarkable bactericidal effect on E. coli. By contrast, the survival rate of E. coli was zero when the bactericidal experiment was performed under irradiation. The photothermal bactericidal activity of the RGO-g-P3TOPA composite was further investigated by decreasing its concentration. It was found that the high photothermal bactericidal activity could be maintained with a very low concentration of RGO-g-P3TOPA, i.e., 2.5 µg mL−1. Notably, the RGO-g-P3TOPA suspension with this concentration only reached ca. 32 °C in the photothermal heating test (Figure 4a and 5c), which is much lower than the thermoablation threshold of bacteria (50 °C). Therefore, the RGO-g-P3TOPA composite must kill the E. coli via a different mechanism in the photothermal bactericidal experiments. Considering the opposite surface charges of E. coli and the RGO-g-P3TOPA sheets, we speculate that the electrostatic attractions between E. coli and the RGO-g-P3TOPA sheets bind them together and lead to direct heat conduction from the RGO-gP3TOPA sheets to the E. coli. Therefore, the photothermal bactericidal activity of the RGO-g-P3TOPA composite is substantially improved compared with an indirect heat conduction mode, wherein a photothermal agent heats the suspension and then the high temperature of the suspension kills the bacteria.51,52 The high photothermal bactericidal activity of the RGO-g-P3TOPA was also confirmed by confocal laser scanning microscopy (CLSM) and scanning electron microscopy (SEM) (Figure S10). In the aforementioned photothermal bactericidal tests, the mixtures of RGO-g-P3TOPA and E. coli were stable in the suspensions because the E. coli was a dominated component in the suspensions. The negatively charged RGO-g-P3TOPS composite was also used as a photothermal bactericidal agent for killing E. coli (see Figure S11 for the photographs of E. coli colonies). It was found that the

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RGO-g-P3TOPS composite exhibited an effective bactericidal effect only when its suspensions were capable of being photothermally heated to a temperature higher than 50 °C: the survival rates of E. coli were 22% and zero for the RGO-g-P3TOPS suspensions with concentrations of 30 and 40 µg mL−1, respectively (Figure 5b). These suspensions produced temperatures of ca. 54 and 59 °C, respectively, in photothermal heating tests. By contrast, the survival rates of E. coli were approximately 100% for all concentrations of RGO-g-P3TOPS when the bacteria were treated in the dark, indicating that the RGOg-P3TOPS composite does not exhibit an intrinsic bactericidal effect on E. coli. Therefore, the photothermal bactericidal activity displayed by the RGO-g-P3TOPS composite follows the well-adopted mechanism in which photothermal agents heat the suspensions and the resulting high temperatures of the suspensions kill the bacteria.51,52 The photothermal bactericidal effect of the RGO-g-P3TOPS suspension with a concentration of 40 µg mL−1 was confirmed through CLSM and SEM observations (Figure S12). The photothermal heating capabilities and bactericidal activities for the RGO-g-P3TOPA and the RGO-g-P3TOPS composites are summarized in Figure 5c and 5d as a function of the concentration of the photothermal bactericidal agents. One can see that the concentration required for RGO-g-P3TOPA to achieve 99% mortality of E. coli was as low as 2.5 µg mL−1, which is only onesixteenth of that required for RGO-g-P3TOPS to achieve similar bactericidal activity (40 µg mL−1). The high photothermal bactericidal activity of RGO-g-P3TOPA demonstrates its superiority as an efficient photothermal bactericidal agent. In addition, the RGO-g-P3TOPA and RGO-g-P3TOPS composites were confirmed to exhibit good biocompatibilities using Cell Counting Assay Kit-8 on MCF-7 (Figure S13). Recently, various graphene-based materials have been reported to exhibit outstanding bactericidal activities.42,44,53−57 However, these previous photothermal bactericidal tests were commonly performed at high concentrations, e.g., 10−100 µg mL−1, under long irradiation periods, e.g., 15 min, and with a high power density of laser irradiation, e.g., 1.5 W cm−2.42,44,53−57 By contrast, our photothermal

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bactericidal tests using RGO-g-P3TOPA as a photothermal bactericidal agent were performed at a very low concentration (2.5 µg mL−1), a short irradiation period (10 min), and with a low power density of irradiation (0.79 W cm−2), demonstrating the superiority of our RGO-g-P3TOPA composite as an efficient photothermal bactericidal agent.

Figure 6. Photothermal bactericidal mechanism of RGO-g-P3TOPA composite. (a) Zeta-potential values of an E. coli suspension (solid circle), the suspensions of the RGO-g-P3TOPA (solid square) and the RGO-g-P3TOPS (solid triangle), and the mixture suspensions of E. coli and the RGO-g-P3TOPA or the RGO-g-P3TOPS. The hollow squares represent the zeta-potential values of the mixture suspensions of E. coli and the RGO-g-P3TOPA with various ratios. The hollow triangles represent the zeta-potential values of the mixture suspensions of E. coli and the RGO-g-P3TOPS with various ratios. The error bars represent the standard deviations of data obtained from five parallel experiments. (b) Schematic

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illustration of the efficient photothermal bactericidal process by the positively charged RGO-g-P3TOPA, which is characterized by direct heat conduction because the RGO-g-P3TOPA sheets and bacteria are bound together through electrostatic attractions.

To obtain further insights into the photothermal bactericidal mechanism of the RGO-g-P3TOPA composite, the interfacial interactions between E. coli and RGO-g-P3TOPA, as well as the interactions between E. coli and RGO-g-P3TOPS, were investigated using zeta-potential measurements (Figure 6a). Because of the negatively charged surfaces of E. coli, its suspension gave a negative zeta-potential value (ca. −33 mV). The RGO-g-P3TOPA suspension showed a positive zeta-potential value (ca. +40 mV) because of the presence of quaternary ammonium groups. The addition of RGO-g-P3TOPA to the E. coli suspension led to positive shifts of the zeta potential of the E. coli suspension, confirming the binding of E. coli to the RGO-g-P3TOPA sheets through electrostatic attractions.58 These interactions resulted in direct heat conduction from the RGO-g-P3TOPA sheets to the E. coli, facilitating the photothermal killing of bacteria. The RGO-g-P3TOPS suspension exhibited a negative zeta-potential value (ca. −25 mV) because of the presence of negatively charged sulfonate groups in the side chains of P3TOPS. Addition of the RGO-g-P3TOPS to the E. coli suspension did not change the negative feature of the zeta potential of the E. coli suspension, regardless of the ratio used. This result suggests that mixing E. coli and RGO-g-P3TOPS did not affect the surface properties of either the E. coli or the RGO-g-P3TOPS sheets, indicating that they were not bound together in the mixture suspension. As a result, the aforementioned different interfacial interactions between E. coli and the two WSCP-modified RGO composites result in different photothermal bactericidal mechanisms. RGO-g-P3TOPS follows a widely adopted photothermal bactericidal process in which RGO-g-P3TOPS heats the suspension and the high temperature of the suspension subsequently kills the bacteria; by contrast, as illustrated in

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Figure 6b, the heat generated by the positively charged RGO-g-P3TOPA is directly conducted to E. coli because they are bound together by electrostatic attractions. Therefore, RGO-g-P3TOPA shows significantly enhanced photothermal bactericidal activity because of this direct heat conduction. To verify the universality of this new concept that electrostatic attraction enhances photothermal bactericidal activity, Staphylococcus aureus (S. aureus), a representative Gram-positive bacterium, was used in photothermal bactericidal tests. Note that, like Gram-negative bacteria, Gram-positive bacteria also have negatively charged surfaces.58 As expected, RGO-g-P3TOPA exhibited much higher bactericidal activity than RGO-g-P3TOPS toward S. aureus (Figure S14).

Figure 7. Photothermal bactericidal tests of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites and their respective components. (a, b) Photothermal heating curves and bactericidal activities of the RGO-g-P3TOPA suspension (2.5 µg mL−1), a GO suspension (1.875 µg mL−1), and a P3TOPA solution (0.625 µg mL−1). The GO suspension and the P3TOPA solution were designed to have concentrations 19



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equivalent to that of their respective components in the RGO-g-P3TOPA composite. (c, d) Photothermal heating curves and bactericidal activities of the RGO-g-P3TOPS suspension (40 µg mL−1), GO suspension (30 µg mL−1), and P3TOPS solution (10 µg mL−1). The GO suspension and the P3TOPS solution were designed to have concentrations equivalent to that of their respective components in the RGO-g-P3TOPS composite.

To further evaluate the performances of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites in photothermal heating and photothermal bactericidal applications, we tested their respective components. For clarity, experiments were designed to compare the individual components with the suspensions of the RGO-g-P3TOPA and the RGO-g-P3TOPS composites that resulted in 100% mortality of E. coli. As shown in Figure 7a, photothermal heating effects of DI water, a GO suspension (1.875 µg mL−1) and a P3TOPA solution (0.625 µg mL−1) were tested. The GO suspension and the P3TOPA solution had equivalent concentrations of their respective components in the RGO-g-P3TOPA composite; they exhibited very small temperature increases compared to the temperature elevation displayed by the RGO-g-P3TOPA suspension (2.5 µg mL−1) (Figure 7a). In photothermal bactericidal tests, whereas the RGO-g-P3TOPA showed a very high bactericidal activity for killing E. coli (survival rate 0%), P3TOPA exhibited a slight bactericidal activity (survival rate 78.5%), and GO displayed no bactericidal activity (survival rate 100%) (Figure 7b and Figure S15). The slight bactericidal activity of P3TOPA might be attributable to the quaternary amine groups, which exhibited similar bactericidal effect as positively charged polypeptides.59−61 The photothermal bactericidal activities of RGO-gP3TOPA, P3TOPA, and GO were also confirmed by CLSM and SEM (Figure S16 and S17). Control experiments were performed with GO and P3TOPA in the same concentration as the RGO-g-P3TOPA composite. The data indicated that the composite exhibited higher photothermal heating and

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photothermal bactericidal efficiencies than each of its components (Figure S18). Furthermore, the negatively charged RGO-g-P3TOPS composite (40 µg mL−1) was also proved to show higher efficiencies than each of its components in photothermal heating and photothermal bactericidal tests (Figure 7c and 7d, Figure S19, S20, and S21).

CONCLUSIONS In summary, WSCPs were in situ grafted onto RGO sheets using a grafting-through method. The resultant WSCP-modified RGO sheets were positively or negatively charged by tuning the functional groups in the side chains of the WSCPs. Both RGO-g-P3TOPS and RGO-g-P3TOPA exhibited good dispersability in water and an outstanding photothermal heating effect. Spectroscopic studies indicate that their high photothermal conversion efficiency (ca. 88%) is attributable to the high reduced state of GO in the composite, an enhanced optical absorption from the UV to the NIR region, and the photoinduced electron transfer from the grafted WSCPs to the RGO basal planes. Moreover, as a new graphene material, the positively charged RGO-g-P3TOPA sheets facilitate intimate binding with bacteria through electrostatic attractions. Such binding promotes heat conduction from RGO-g-P3TOPA to the bacteria and enhances the photothermal bactericidal efficiency; as a result, RGO-g-P3TOPA exhibits a very high efficiency (100%) for photothermally killing E. coli, even at a very low concentration of 2.5 µg mL−1, which is only one-sixteenth of that required for the RGO-g-P3TOPS to achieve similar bactericidal efficiency. The excellent bactericidal activity of the RGO-g-P3TOPA demonstrates its superiority because it combines the photothermal effect with electrostatic attractions for photothermal killing of bacteria. Finally, this study may additionally provide a new path for the application of graphene materials in photoresponsive devices, bio-sensing, and information storage devices.

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ASSOCIATED CONTENT Supporting Information Experimental methods, structural and morphological characterization of the polythiophene modified RGO, calculation of photothermal conversion efficiencies, photothermal bactericidal tests. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding author *Email: [email protected] Notes The authors declare no competing financial interest. ACKNOWLEDGMENTS This work was supported by the “Hundred Talents Program” of the Chinese Academy of Sciences and by the National Natural Science Foundation of China (21274158, 91333114).

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Enhanced Photothermal Bactericidal Activity of the Reduced

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