Chlorine-Doped Graphene Quantum Dots with Enhanced Anti- and

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Functional Nanostructured Materials (including low-D carbon)

Chlorine-Doped Graphene Quantum Dots with Enhanced Anti- and Pro-Oxidant Properties Lifeng Wang, Yan Li, Yingmin Wang, Wenhui Kong, Qipeng Lu, Xiaoguang Liu, Dawei Zhang, and Liangti Qu ACS Appl. Mater. Interfaces, Just Accepted Manuscript • Publication Date (Web): 23 May 2019 Downloaded from http://pubs.acs.org on May 23, 2019

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ACS Applied Materials & Interfaces

Chlorine-Doped Graphene Quantum Dots with Enhanced Anti- and Pro-Oxidant Properties Lifeng wang †, Yan Li Liangti Qu

†

†,*,

Yingmin Wang †, Wenhui Kong †, Qipeng Lu †, Xiaoguang Liu †, Dawei Zhang†,

‡

School of Materials Science and Engineering, University of Science and Technology Beijing, Beijing 100083, P.R.

China ‡

Beijing Key Laboratory of Photoelectronic/Electrophotonic Conversion Materials, Key Laboratory of Cluster Science,

Ministry of Education, School of Chemistry, Beijing Institute of Technology, Beijing 100081, P.R. China

Keywords: graphene quantum dots, heteroatom doping, enhanced antioxidant, antibacterial Abstract Production or elimination of highly-reactive oxygen species is critical in antioxidant, photodynamic therapeutic and antibacterial applications. Recent studies have demonstrated graphene quantum dots (GQDs) possess anti- and pro-oxidant properties simultaneously. But their efficiency is low. Here we report chlorine-doped graphene quantum dots (Cl-GQDs) with tunable Cl doping amount and improved anti- and pro-oxidant activities. The scavenging performance and the free radicals produced efficiency of Cl-GQDs are about 7-fold and 3-fold, respectively, higher than the undoped GQDs. Meanwhile, Cl-GQDs are considered to be promising for antibacterial applications due to their enhanced singlet oxygen generating ability. We hope this study could provide a new strategy to develop nanomaterials for application in anti- and pro-oxidant field. *Corresponding

author. E-mail: [email protected] 1

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1. Introduction Reactive oxygen species (ROS), including singlet oxygen (1O2), superoxide anion (O2•-) and hydroxyl radicals (•OH) are derived from molecular oxygen containing one or more unpaired electrons.

1

The unpaired electrons endow them with high reactivity. A suitable ROS content is

essential for normal cell in physiological processes, such as proliferation and homeostasis.

2

However, a burst of ROS in cell could cause oxidative damage to cell membranes, protein structures and DNA, and probably induce cancer-causing mutations.

3-7

Therefore, antioxidant materials are

essential to keep the ROS content to balance. From another perspective, high levels of ROS generated from photosensitizers by light excitation could kill cancer cells because they are more vulnerable to exogenous ROS than ordinary cells.1, 8 And ROS could also cause membrane damage of bacterial cells to exert antimicrobial activity.

9-10

Accordingly, highly-efficient ROS-generating

materials will also be required for photodynamic therapy and antibacterial fields. Several groups reported that carbon nanomaterials (including fullerenes, carbon nanotubes, graphene and functionalized carbon dots) could scavenge ROS by hydrogen donation, adduct formation or electron transfer.

11-15

Furthermore, carbon nanomaterials with defects or heteroatom

sites could also generate ROS through surface reactions under light irradiation, which often involves defect or heteroatom sites.

16-17

GQDs, small fragments of graphene sheet containing abundant

surface functional groups, have attracted more interest owing to their outstanding optical properties and favorable biocompatibility.18-19 Especially, the unpaired electrons from the defects and the π-conjugated nature of GQDs facilitate their electron storage capacity and charge transfer abilities, which endow them with free radical scavenging property.

4, 20

Meanwhile, under blue laser or white

light irradiation, GQDs could generate 1O2, exhibiting pro-oxidant properties. 2


10, 21

Compared with

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cytotoxic carbon nanotubes or graphene oxide, small sized GQDs, featuring superior biocompatibility and photoluminescence property, have become one of most promising and marketable antioxidant or pro-oxidant in organism. However, the anti- and pro-oxidant activities of GQDs are far from meeting the requirements of application until now since the surface functional groups and lattice defects are limit in unmodified GQDs. And only parts of the defects are active for producing or scavenging free radicals. 21 Heteroatom doping is an effective method to modify the defect level of GQDs and regulate their physical and chemical properties. The heteroatom dopants could create positive or negative charges on adjacent carbon atoms in the graphitic lattice. And the corresponded electronic density and charge transfer ability of GQDs could be varied, which lead to the increase of fluorescent in the intensity or catalytic activity.

22-23

Furthermore, the polarized carbon atoms could enhance the antioxidant

performance. 24 Besides, related research also pointed out that ROS-generating ability of GQDs was closely related to the ketonic carbonyl groups.

25

It seems that if high level of defects can be

introduced into the GQDs by doping and the oxygen-containing functional groups can be optimized to generate carbonyl groups, enhanced anti- and pro-oxidant properties could be expected. However, the related research had been rarely reported. Here, we realized the regulation of surface functional group (i.e. C=O/COOH group) in the synthesis of Cl-GQDs. Cl was chosen as the dopant due to its relatively large atom radium and high electronegativity compared to carbon atom, which favor the electronic interaction between Cl-GQDs and free radicals. Although Cl-GQDs have been prepared and their fluorescent and electron transfer properties in photovoltaic detector have been investigated elsewhere 26-28, their preparation processes are normally energy-intensive, highly risky, thus hardly commercially available (~450 $/ 100 mg). 3



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Therefore, in this work, an electrochemical approach was proposed to synthesize Cl-GQDs and a widely-used artificial sweetener (i.e. sucralose) was employed to provide C and Cl source. This method is not only facile and economic, but also can realize the regulation of surface functional groups (i.e. C=O/COOH) and Cl-doping concentration during the preparation simultaneously. Through optimizing the amount of Cl dopant and surface C=O/COOH, the as-prepared Cl-GQDs exhibited higher activity for different free radicals scavenging than the undoped ones. Meanwhile, they could also produce ROS more efficiently under light irradiation. As an antibacterial agent, the ratio of antibiosis thereof could reach to 96.6%. We hope our work can be helpful for controlled synthesis Cl-GQDs and design anti- and pro-oxidant materials with high activity. 2. Experimental 2.1 Preparation of Cl-GQDs Cl-GQDs were prepared by an electrochemical method using a CHI 660D working station. Two platinum wires were used as working and countering electrode, respectively. 1 g sucralose (Shanghai Yuanye Bio-Technology Co., Ltd., China, 98% in purity) was dissolved in 10 mL NaOH (4 M) aqueous solution, which provided the C and Cl sources. The amount of oxygen-containing functional group and Cl dopant were adjusted by changing the voltage and electrolysis time in the synthesis procedure. Cl-GQDs-5v and Cl-GQDs-7.5v were obtained by a constant potential method with 5 v and 7.5 v voltage supply for 45 min. Cl-GQDs-5v-2h was obtained by the similar method with 5 v voltage supply for 2 h. The Cl-GQDs were collected by filtering the electrolyte with a cellulose filtration membrane (0.22 μm) and dialyzing with a cellulose ester membrane bag (retained molecular weight: 3500 Da) for 6 days. Besides, the compared GQDs were prepared by constant-voltage scanning procedure as reported in our previous work. 21 4


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2.2 Material characterization Transmission electron microscopy (TEM) observation was carried out using an H-7650B electron microscope at 120 kV. UV-Vis absorption and photoluminescence (PL) spectra were measured using a TU-1900 spectrophotometer and a fluorimeter (Hitachi F-7000), respectively. X-ray photoelectron spectroscopy (XPS) was performed on an ESCALAB 250Xi electron spectrometer with an Al monochromatic Ka radiation (hυ=1486.6 eV) source. The energies of all the spectra were calibrated with respect to the C 1s peak at 284.5 eV. Electron-spin resonance (ESR) measurements were carried out by using an ESR spectrometer (A300, Bruker). The spin trap 2,2,6,6-Tetramethylpiperidine (TEMP) was selected to detect singlet oxygen. 200 μL of the sample solutions containing 20 μL TEMP and exposure to a 450 W xenon lamp (1000 W/m2) for 10 min. The control group was conducted in almost the same strategy except the light irradiation. Cyclic voltammetry (CV) curves were carried out on a CHI 660D electrochemical working station (Chenhua Instrument, Shanghai, China) with a three-electrode system. Cl-GQDs modified glassy carbon electrode (GCE) was used as working electrode. Pt plate and Ag/AgCl electrodes were used as the counter and reference electrode, respectively. GCE was polished with alumina powders and ultra-sonication in ethanol and deionized water before the experiment. 50 μL Cl-GQDs (200 μg/mL) solutions were spread on GCE and dry naturally in air. All the electrochemical measurements were recorded in 0.1 M KCl solution containing 0.5 mM K3[Fe(CN)6] and 0.5 mM K4Fe(CN)6. 2.3 Radical scavenging assays and antioxidant activity DPPH radical (DPPH•) scavenging assay. 1,1-Diphenyl-2-picrylhydrazyl radical (Shanghai 5



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Jinsui Bio-Technology Co., Ltd., China, 97% in purity), as a stable nitrogen-centered free radical, was used to evaluate the free radicals scavenging performance of Cl-GQDs. 1 mL ethanol solution containing 100 μM DPPH• was mixed with 1 mL Cl-GQDs (0-300 μg/mL) aqueous solution after incubated in the dark for 1 h. The scavenging efficiency was measured according to the decrease of absorption intensity at 520 nm. KMnO4 reduction assay. KMnO4 (Sinopharm Chemical Reagent Co., Ltd., China, 99.5% in purity) could also evaluate the antioxidant activity of GQDs following the protocol by Ruiz. 5 2 mL acidified (pH=3) KMnO4 solutions (100 mM) containing 100 μg Cl-GQDs were incubated in the dark for 30 min. After reduction by antioxidants, KMnO4 solutions changed from purple to colorless. The remaining concentration of KMnO4 was monitored by UV-Vis absorption spectroscopy at 515 nm. Hydroxy radical scavenging assay. •OH could be produced by a photochemical reaction of TiO2 nanoparticles (P25, Degussa AG Co., Ltd.). Terephthalic acid could capture •OH and transform it into 2-hydroxy terephthalic acid (λex: 315 nm and λem: 430 nm), which could be used as a fluorescence probe to determine the concentration of •OH. Therefore, in this paper, 2 mL solutions containing 25 mM PBS, 0.5 mM Terephthalic acid, 100 μg TiO2 and 100 μg Cl-GQDs were irradiated by UV light (8 W, 365 nm) for 1 h. Finally, the concentration of •OH could be monitored by the intensity of PL spectrum (430 nm). Dye protect assay. Rhodamine B (RhB, Sinopharm Chemical Reagent Co., Ltd., China) was used as a model target molecule for oxidant attack. 2 mL solutions containing 25 mM PBS, 50 μg/mL TiO2 (P25), 10 μM RhB and 100 μg/mL Cl-GQDs were irradiated by UV light (8 W,365 nm) for 3 h with magnetic stirring. The concentration of the remaining RhB was monitored by its 6


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absorption spectrum (552 nm). 2.4 Pro-oxidant assay Ascorbic acid oxidation assay. Pro-oxidant assay was conducted according to the protocol by Chong 4, in which ascorbic acid (AA, Xilong Scientific Co., Ltd., China, 99.7% in purity) could be oxidized by the photo-excited GQDs under the excitation light of a 450 W xenon lamp (1000 W/m2). Briefly, 1 mL AA solution (100 μM) was mixed with 1 mL Cl-GQDs (100 μg/mL) aqueous solution under light irradiation for 30 min. Then the remaining AA could be monitored by the absorption intensity (λmax=265 nm). The pro-oxidant performance of Cl-GQDs was evaluate by the peak intensity of AA. Antibacterial assay. Escherichia coli (ATCC 25922) was cultured overnight in Luria-Bertani (LB) agar medium at 37 °C to stationary phase. Then, the bacterial cells were centrifuged at 3000 rpm for 5 minutes, washed twice and subsequently diluted with 0.9% sterile saline (OD600 = 0.7). After that, 200 μL bacterial suspension was diluted to 5 mL sterile saline, in which Cl-GQDs-7.5v were added until their concentration reaches 50 μg/mL. Control experiment was conducted under almost the same conditions except that no Cl-GQDs-7.5v was added. The two as-prepared bacterial suspensions were exposed to the simulated sunlight (1000 W/m2) for 2 h, centrifuged at 3000 rpm for 5 min and subsequently redispersed in the sterile saline. Bacterial suspensions containing Cl-GQDs-7.5v in dark was conducted in the same strategy. After that, 100 μL of 100-fold serial dilutions bacterial suspensions were coated on a LB agar plate respectively and incubated at 37 °C overnight to observe the formation of colonies. 3. Results and discussion 3.1 GQDs characterization 7



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Cl-GQDs were prepared through the electrochemical treatment of sucralose, as illustrated in Fig 1a. TEM and HRTEM measurements were performed to investigate the morphology of Cl-GQDs. Fig. 1 b, c and d show that the as-prepared Cl-GQDs could be uniformly dispersed, which was similar to the undoped GQDs previously reported.

18

From HRTEM result of Cl-GQDs in Fig. 1e, a

clear lattice fringe of 0.24 nm matches with the (1120) facet of graphite. This suggests that the doped chlorine atoms do not influence the graphite nature and the surface morphology of Cl-GQDs.

Fig. 1 (a) Schematic illustration of the preparation of Cl-GQDs. TEM images of Cl-GQDs-5v (b), Cl-GQDs-7.5v (c) and Cl-GQDs-5v-2h (d). (e) HRTEM image of Cl-GQDs-5v. The UV-vis spectrum of Cl-GQDs, shown in Fig. S1, displays a typical absorption band at ca. 268 nm and a small absorption tail that extended to 350 nm attributing to the π-π* transition of the C=C and the n-π* transition of oxygen-containing groups, respectively. The light-yellow Cl-GQDs aqueous solution emitted strong blue-green fluorescence under irradiated at 365 nm (Fig. 2a, inset). With heteroatoms doping, Cl-GQDs exhibited stronger PL intensity compared with GQDs in the same concentration, which could be ascribed to the interplay between the dopants and the carbon 8


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atoms in the graphene lattice. 23, 29 The FT-IR spectra of the Cl-GQDs (Fig. 2b) shows peaks at 588, 710 and 788 cm-1 owing to C-Cl stretching vibration, which confirms the successful incorporation of chlorine atoms into GQDs. The other peaks at 1048, 1720, 3430 cm-1 are ascribed to C-O-C, C=O, -OH stretching vibration, respectively. Furthermore, the Raman spectra (in Fig. S2) revealed that a large number of defects were produced in the Cl-GQDs, given by the Cl doping.

Fig. 2 (a) PL spectra of the Cl-GQDs-5v, Cl-GQDs-7.5v, Cl-GQDs-5v-2h and GQDs dispersed in water at room temperature. The inserts show the photograph (left) and fluorescence images of the Cl-GQDs-7.5v solutions under UV light of 365 nm (right). FT-IR spectra (b) and XPS survey spectra (c) of the Cl-GQDs-5v, Cl-GQDs-7.5v, Cl-GQDs-5v-2h and GQDs. (d) Cl 2p high-resolution XPS spectrum of Cl-GQDs-7.5v. XPS measurements further confirm the successful doping of Cl atoms in Cl-GQDs-5v, Cl-GQDs-7.5v Cl-GQDs-5v-2h from Fig. 2c, in which a pronounced Cl 2p peak at ca. 199 eV is observed along with the C 1s (ca. 284 eV) and O 1s (ca. 530 eV) main peaks. During the synthesis 9



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process, we prepared Cl-GQDs with tunable amounts of Cl by changing the voltage or electrolysis time. Cl contents in Cl-GQDs-5v, Cl-GQDs-7.5v, and Cl-GQDs-5v-2h are 0.89%, 1.32% and 0.62%, respectively (Table S1). In addition, the high-resolution C 1s spectrum of each sample (Fig. S3) indicates that the C=O/COOH content rises with the increase of voltage or the duration of the electrolysis. 3.2 Antioxidant activity 3.2.1 DPPH radical scavenging assay

Fig. 3 DPPH• scavenging assay. (a) DPPH• remaining ratio after incubated with Cl-GQDs-5v, Cl-GQDs-7.5v, Cl-GQDs-5v-2h and GQDs in the dark for 30 min. (b) Absorption spectra of 2 mL DPPH• solutions (50 μM) containing 0-300 μg Cl-GQDs-7.5v after incubation in the dark for 1 h. Error bars represent the standard deviation. The antioxidant activity of Cl-GQDs was first investigated by using DPPH• as model radical. As a relatively stable free radical, DPPH• has been commonly used to assess the antioxidant activity of compounds. A stable DPPH-H complex could be formed when an antioxidant was added and the color immediately changed from deep purple to pale yellow/colorless. Fig. 3a shows the DPPH• remaining ratio of each GQDs after incubation in the dark for 30 min. Compare with undoped GQDs, all of the Cl-GQDs samples show higher antioxidant activity. Meanwhile, the antioxidant activity is dependent on the Cl doping content, From Cl-GQDs-5v-2h (Cl content is 0.62%), Cl-GQDs-5v (Cl 10


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content is 0.89%) to Cl-GQDs-7.5v (Cl content is 1.35%), the antioxidant activity was gradually improved. In addition, from the variation of the intensity of the characteristic peaks in DPPH • absorption spectra, as shown in Fig. 3b, the antioxidant activity of Cl-GQDs-7.5v is also related to their concentration. Furthermore, compared with other carbon nanomaterials from the literatures, such as GO and pC60 or modified CNT

6, 30,

Cl-GQDs-7.5v exhibit a higher reaction rate and a

superior antioxidant activity. The DPPH• scavenging mechanism is discussed in detail later. 3.2.2 KMnO4 reduction and hydroxyl radical scavenging assay KMnO4 reduction assay was further conducted to evaluate the antioxidant activity of Cl-GQDs. Mn7+ in acidified KMnO4 solutions could be reduced to Mn2+ after antioxidants were added, which companies with a decreased absorbance at 515 nm. 31 The antioxidant property of each sample could be estimated compared with the characteristic absorption peak of KMnO4 solutions without any antioxidant. Fig. 4a shows the KMnO4 remaining ratio with different antioxidants after 1 h reaction in dark. It could be noticed that the KMnO4 was slightly reduced by GQDs according to the absorption spectra, but KMnO4 solutions with all Cl-GQDs exhibited more significant reduction, which indicated that Cl doping played an important role in the KMnO4 reduction assay. On the other hand, similar to the DPPH• assay, the order of the reducing capacity is: Cl-GQDs-7.5v >Cl-GQDs-5v > Cl-GQDs-5v-2h. These results further confirmed that content of Cl atoms in Cl-GQDs also very important to their antioxidant property. Our previous studies confirmed that Fe2+ could be chelated with GQDs and thus depressed the Fenton reaction.

32

Furthermore, we confirmed that there was no •OH generated from Cl-GQDs

through a PL test by using terephthalic acid as fluorescence probe under UV light irradiation (365 nm). Hence, we employed a photochemical reaction of TiO2 nanoparticles to produce •OH. 11



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Terephthalic acid could capture the •OH and transformed into a fluorescence 2-hydroxy terephthalic acid. The remaining ratio of •OH was evaluated by the PL intensity. As illustrated in Fig. 4b, the PL intensity of terephthalic acid solution containing TiO2 nanoparticles and GQDs decreased to various degrees after UV light irradiation (365 nm). Specifically, the PL intensity of solution with GQDs have decreased slightly (58%), whereas Cl-doped GQDs have decreased dramatically (83%, 91% and 78% for Cl-GQDs-5v-2h, Cl-GQDs-5v and Cl-GQDs-7.5v, respectively), indicating the Cl-GQDs with more Cl possess higher •OH scavenging efficiencies.

Fig. 4 KMnO4 reduction and hydroxyl radical scavenging assays. (a) KMnO4 remaining ratio after incubated with Cl-GQDs-5v, Cl-GQDs-7.5v, Cl-GQDs-5v-2h and GQDs in the dark for 1 h (pH=3). (b) Hydroxyl radical remaining ratio after incubated with Cl-GQDs-5v, Cl-GQDs-7.5v, Cl-GQDs-5v-2h and GQDs under light irradiation for 1 h.

Fig. 5 Dye protect assay. (a) RhB (10 μM) remaining ratio after photocatalytic degradation with or without antioxidant protection. (b) Photo of the solutions after photocatalytic experiment. 3.2.3 Dye protection assay 12


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Furthermore, Cl-GQDs were selected to investigate their potential to prevent the degradation of organic dye from oxidation pressure. In our case, TiO2 nanoparticles were selected again to produce ROS by a photochemical reaction. Once antioxidants were added, the degradation of RhB by ROS was suppressed. And the antioxidant property of Cl-GQDs could be evaluated by the remaining ratio of RhB, which was detected by the absorption spectra. As shown in Fig. 5a, the remaining ratio of RhB (84.4%) is the highest in the solution containing with Cl-GQDs-7.5v among all samples. The dye-protection efficiency of Cl-GQDs-7.5v is 7 times higher than that of the undoped one. 3.3 Pro-oxidant activity

Fig.6 (a) AA remaining ratio after light irradiation for 30 min. (b) O 1s high-resolution XPS spectra of Cl-GQDs-5v, Cl-GQDs-7.5v and Cl-GQDs-5v-2h. (c) Cell viability measurements of E. coli treated with Cl-GQDs. (d) Photographs of LB agar plates contain E. coli bacterial cells with Cl-GQDs-7.5v in dark or exposure to light. Bacterial suspension without Cl-GQDs-7.5v was used as control. 13



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It is reported that ROS could be produced through energy transfer between GQDs and oxygen molecules.

8, 33

And AA was used as an antioxidant to evaluate the ROS production efficiency of

Cl-GQDs. The pro-oxidant activity of Cl-GQDs was detected by the loss ratio of AA from the change of characteristic absorption peak (265 nm). Fig. 6a indicates that the ROS generation of the Cl-GQDs is 3 times more efficient than that of the GQDs. This could be also ascribed to the large number of defective sites in the doped Cl atoms and the corresponding promoted electronic interaction with oxygen. In addition, ROS generation ability is involved with the functional groups such as carbonyl and carboxyl species.

25

Carbonyl bonds is an active site to produce ROS, whose

content in Cl-GQDs-7.5v is higher than that in Cl-GQDs-5v-2h and Cl-GQDs-5v (Fig. 6b). Therefore, the high Cl and carbonyl bond content endow Cl-GQDs-7.5v with the strongest ROS generating ability. Furthermore, ROS are harmful to lipids and proteins of bacteria.

33-35

Several studies reported

Ag or adenine modified GQDs could be used to kill bacteria, but these GQDs based materials still suffered from inefficient antibacterial performance and complex preparation processes.

36-37

Biljana

et al. reported that GQDs could kill bacterial under a blue light laser irradiation, but using laser to kill bacteria is impractical in industrial applications and there were still bacteria survival at the end. 9 In our case, we assessed the antibacterial performance of the Cl-GQDs against E. coli bacteria. First, E. coli suspension with Cl-GQDs-7.5v (50 μg/mL) was exposed to a simulated sunlight for 2 h. And then the bacteria cells were coated on a LB agar plate and counted after overnight incubation. Fig. 6c and d indicate that the Cl-GQDs-7.5v could result in a high antibacterial ratio (> 96.6%) under a simulated sunlight illumination, while the antibacterial ratio was only 15.3% in the dark conditions. The obtained results indicate the Cl-GQDs-7.5v possesses high antibacterial ability under a 14


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simulated sunlight irradiation. 3.4 Discussion It is known that carbon atoms in graphene plane of GQDs are covalently bonded through three electrons with each other and form a strong lattice, but the fourth valence electron on each carbon atom is delocalized. In addition, this delocalized electron could be localized at the edge or defect sites of the GQDs.

9

As mentioned before, a lot of sp3 C exist in Cl-GQDs, which lead to the

unbalance distribution of the density of electron inside the hexagonal carbon ring. 38 Moreover, there is significant difference between in electronegativity of chlorine dopant (3.16) (2.55).

40

39

and carbon atom

And the covalently doped electron donating chlorine atoms create net negative charges on

adjacent carbon atoms in graphitic lattice, which further modulate the electronic density and enhance the chemical activity of Cl-GQDs, facilitating the electronic interaction between Cl-GQDs and radicals.

41-44

Similar to many heteroatoms doped carbon-based materials (such as CNT, graphene

and GQDs) 45-48, Cl-GQDs possess an excellent electron transfer property, which is important for the superior antioxidant and pro-oxidant abilities. The DPPH• scavenging mechanism was further elucidated by the XPS analysis on Cl-GQDs-5v after the reaction with DPPH•. First, the appearance of N in the XPS survey spectra (Fig. S5) after the reaction demonstrated that the formation of adduct is an important mechanism for DPPH• scavenging. Moreover, the C 1s spectra demonstrate that most of the surface C-O bonds are reduced, especially the C-Cl bonds almost disappeared in Cl-GQDs-5v after the scavenging experiment (Fig. 7a). This indicated both Cl and O are the reactive center of Cl-GQDs.

15



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Fig. 7 (a) C 1s spectra of the Cl-GQDs-5v before and after reaction with DPPH•. (b) CV curves of Cl-GQDs samples modified on GCE electrodes in 0.1 M KCl solutions containing 0.5 mM K3[Fe(CN)6] and 0.5 mM K4Fe(CN)6. (c) ESR spectra obtained from samples containing Cl-GQDs-7.5v and TEMP with (black) or without (red) light irradiation. (d) Schematic illustration of the 1O2 generation mechanism. To evaluate the influence of Cl in GQDs, CV measurements were conducted by using a 0.1 M KCl solution containing 0.5 mM K3[Fe(CN)6] and 0.5 mM K4Fe(CN)6 as the electrolyte. Cl-GQDs act as an insulating layer on the GCE electrode and hinder the electron transfer between ferricyanide ions and GCE.

49

Fig. 7b showed a typical redox reaction at the electrode surface with the

Cl-GQDs-7.5v exhibiting the highest peak current value than others. Besides, the peak current value decreases with the decreasing Cl doping level, which further indicated that the charge transfer ability of GQDs was closely related to the doped Cl. Hence, the high-value electronegativity of the Cl promoted the electronic interaction between Cl-GQDs and DPPH• and Cl-GQDs-7.5v with the 16


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highest Cl content possess the highest DPPH• scavenging efficiency. Similar to DPPH• scavenging, the experimental results of KMnO4 and •OH scavenging assays both demonstrated that the doped Cl atoms promoted the charge transfer between Cl-GQDs and Mn7+/•OH. And the Cl-GQDs with the maximum Cl content exhibited the strongest reduction property and superior antioxidant ability. The ROS generation from GQDs under light irradiation was confirmed by ESR spectroscopy. TEMP was selected as a spin trap for singlet oxygen, which could selectively react with 1O2. 8 After the 1O2 was trapped, a stable product 2,2,6,6-tetramethylpiperidine-1-oxyl was produced, leading to a characteristic EPR signal. Fig. 7c illustrated a strong ESR signal of TEMP with Cl-GQDs-7.5v solution under irradiation. In addition, no ESR signal was observed for the control sample in dark. These results demonstrated 1O2 could be generated by Cl-GQDs-7.5v under irradiation which agreed well with previous reports.

8

Following photoexcitation, 1O2 was produced by energy transfer from

the excited triplet state of the Cl-GQDs to the ground-state oxygen (Fig. 7d). And no O2•- or •OH was generated by GQDs under irradiation. 8, 33 Compared with GQDs, the higher level of defects induced from the highly electronegative Cl atoms facilitated the energy transfer between Cl-GQDs and O2 and thus enhance their pro-oxidant property. 4. Conclusions In summary, we successfully synthesized Cl-GQDs by a facile electrochemical method. And the Cl-GQDs exhibited efficiently free radicals scavenging ability, which could be ascribed to the high content of defect sites induced by doping with Cl atoms. These Cl-GQDs could scavenge the strong oxidizing ROS and protect dye from degradation. The scavenging performance of Cl-GQDs was about 7 times higher than that of the undoped one. Furthermore, ROS could also be produced by

17



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Cl-GQDs under a visible light irradiation. The ROS producing capability was about 3 times higher than that of the undoped one. The highly ROS producing ability could be also attributed to the defect induced by Cl doping and their highly C=O bonds content, which endowed them with an enhanced antibacterial performance. Associated content The Supporting Information is available free of charge on the ACS Publications website at DOI: UV-vis absorption spectra, Raman spectra, C 1s high-resolution XPS spectra, Loss ratio of AA in dark, XPS survey spectrum of Cl-GQDs-5v after reaction with DPPH• and Table S1 (PDF) Acknowledgments This work was supported by National Natural Science Foundation of China (Grant No. 21674011), Beijing Municipal Natural Science Foundation (2172040), and Fundamental Research Funds for the Central Universities (FRF-GF-17-B11). Notes and references (1) Zhou, Z.; Song, J.; Nie, L.; Chen, X. Reactive Oxygen Species Generating Systems Meeting Challenges of Photodynamic Cancer Therapy. Chem. Soc. Rev. 2016, 45, 6597-6626. (2) Finkel, T. Signal Transduction by Reactive Oxygen Species. J. Cell Biol. 2011, 194, 7-15. (3) Zhao, S.; Lan, M.; Zhu, X.; Xue, H.; Ng, T. W.; Meng, X.; Lee, C. S.; Wang, P.; Zhang, W. Green Synthesis of Bifunctional Fluorescent Carbon Dots from Garlic for Cellular Imaging and Free Radical Scavenging. Acs Appl. Mater. Inter. 2015, 7, 17054-17060. (4) Chong, Y.; Ge, C.; Fang, G.; Tian, X.; Ma, X.; Wen, T.; Wamer, W. G.; Chen, C.; Chai, Z.; Yin,

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Page 19 of 25 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


J. J. Crossover between Anti- and Pro-Oxidant Activities of Graphene Quantum Dots in the Absence or Presence of Light. ACS Nano 2016, 10, 8690-8699. (5) Ruiz, V.; Yate, L.; Garcia, I.; Cabanero, G.; Grande, H. J. Tuning the Antioxidant Activity of Graphene Quantum Dots: Protective Nanomaterials against Dye Decoloration. Carbon 2017, 116, 366-374. (6) Qiu, Y.; Wang, Z.; Owens, A. C.; Kulaots, I.; Chen, Y.; Kane, A. B.; Hurt, R. H. Antioxidant Chemistry of Graphene-Based Materials and Its Role in Oxidation Protection Technology. Nanoscale 2014, 6, 11744-11755. (7) Poprac, P.; Jomova, K.; Simunkova, M.; Kollar, V.; Rhodes, C. J.; Valko, M. Targeting Free Radicals in Oxidative Stress-Related Human Diseases. Trends Pharmacol. Sci. 2017, 38, 592-607. (8) Ge, J.; Lan, M.; Zhou, B.; Liu, W.; Guo, L.; Wang, H.; Jia, Q.; Niu, G.; Huang, X.; Zhou, H.; Meng, X.; Wang, P.; Lee, C. S.; Zhang, W.; Han, X. A Graphene Quantum Dot Photodynamic Therapy Agent with High Singlet Oxygen Generation. Nat. Commun. 2014, 5, 4596-4604. (9) Ristic, B. Z.; Milenkovic, M. M.; Dakic, I. R.; Todorovic-Markovic, B. M.; Milosavljevic, M. S.; Budimir, M. D.; Paunovic, V. G.; Dramicanin, M. D.; Markovic, Z. M.; Trajkovic, V. S. Photodynamic Antibacterial Effect of Graphene Quantum Dots. Biomaterials 2014, 35, 4428-4435. (10) Liu, S.; Zeng, T. H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R.; Kong, J.; Chen, Y. Antibacterial Activity of Graphite, Graphite Oxide, Graphene Oxide, and Reduced Graphene Oxide: Membrane and Oxidative Stress. ACS Nano 2011, 5, 6971-6980. (11) Bitner, B. R.; Marcano, D. C.; Berlin, J. M.; Fabian, R. H.; Cherian, L.; Culver, J. C.; Dickinson, M. E.; Robertson, C. S.; Pautler, R. G.; Kent, T. A.; Tour, J. M. Antioxidant Carbon Particles Improve Cerebrovascular Dysfunction Following Traumatic Brain Injury. ACS Nano 2012, 19



Page 20 of 25

6, 8007-8014. (12) Galano, A. Carbon Nanotubes as Free-Radical Scavengers. J. Phys. Chem. C 2008, 112, 8922-8927. (13) Martinez, A.; Galano, A. Free Radical Scavenging Activity of Ultrashort Single-Walled Carbon Nanotubes with Different Structures through Electron Transfer Reactions. J. Phys. Chem. C 2010, 114, 8184-8191. (14) Wright, J. S.; Johnson, E. R.; DiLabio, G. A. Predicting the Activity of Phenolic Antioxidants: Theoretical Method, Analysis of Substituent Effects, and Application to Major Families of Antioxidants. J. Am. Chem. Soc. 2001, 123, 1173-1183. (15) Morita, Y.; Suzuki, S.; Sato, K.; Takui, T. Synthetic Organic Spin Chemistry for Structurally Well-Defined Open-Shell Graphene Fragments. Nat. Chem. 2011, 3, 197-204. (16) Liu, X.; Sen, S.; Liu, J.; Kulaots, I.; Geohegan, D.; Kane, A.; Puretzky, A. A.; Rouleau, C. M.; More, K. L.; Palmore, G. T.; Hurt, R. H. Antioxidant Deactivation on Graphenic Nanocarbon Surfaces. Small 2011, 7, 2775-2785. (17) Pasquini, L. M.; Sekol, R. C.; Taylor, A. D.; Pfefferle, L. D.; Zimmerman, J. B. Realizing Comparable Oxidative and Cytotoxic Potential of Single- and Multiwalled Carbon Nanotubes through Annealing. Environ. Sci. Technol. 2013, 47, 8775-8783. (18) Li, Y.; Hu, Y.; Zhao, Y.; Shi, G. Q.; Deng, L. E.; Hou, Y. B.; Qu, L. T. An Electrochemical Avenue to Green-Luminescent Graphene Quantum Dots as Potential Electron-Acceptors for Photovoltaics. Adv. Mater. 2011, 23, 776-780. (19) Wang, L.; Wang, Y.; Xu, T.; Liao, H.; Yao, C.; Liu, Y.; Li, Z.; Chen, Z.; Pan, D.; Sun, L.; Wu, M. Gram-Scale Synthesis of Single-Crystalline Graphene Quantum Dots with Superior Optical 20


Page 21 of 25 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


Properties. Nat. Commun. 2014, 5, 5357-5366. (20) Yoo, E.; Okata, T.; Akita, T.; Kohyama, M.; Nakamura, J.; Honma, I. Enhanced Electrocatalytic Activity of Pt Subnanoclusters on Graphene Nanosheet Surface. Nano. Lett. 2009, 9, 2255-2259. (21) Wang, Y.; Kong, W.; Wang, L.; Zhang, J. Z.; Li, Y.; Liu, X.; Li, Y. Optimizing Oxygen Functional Groups in Graphene Quantum Dots for Improved Antioxidant Mechanism. Phys. Chem. Chem. Phys. 2019, 21, 1336-1343. (22) Liu, Q.; Guo, B.; Rao, Z.; Zhang, B.; Gong, J. R. Strong Two-Photon-Induced Fluorescence from Photostable, Biocompatible Nitrogen-Doped Graphene Quantum Dots for Cellular and Deep-Tissue Imaging. Nano Lett. 2013, 13, 2436-2441. (23) Qu, D.; Zheng, M.; Du, P.; Zhou, Y.; Zhang, L.; Li, D.; Tan, H.; Zhao, Z.; Xie, Z.; Sun, Z. Highly Luminescent S, N Co-Doped Graphene Quantum Dots with Broad Visible Absorption Bands for Visible Light Photocatalysts. Nanoscale 2013, 5, 12272-12277. (24) Li, Y.; Li, S.; Wang, Y.; Wang, J.; Liu, H.; Liu, X.; Wang, L.; Liu, X.; Xue, W.; Ma, N. Electrochemical Synthesis of Phosphorus-Doped Graphene Quantum Dots for Free Radical Scavenging. Phys. Chem. Chem. Phys. 2017, 19, 11631-11638. (25) Zhou, Y.; Sun, H.; Wang, F.; Ren, J.; Qu, X. How Functional Groups Influence the Ros Generation and Cytotoxicity of Graphene Quantum Dots. Chem. Commun. 2017, 53, 10588-10591. (26) Zhao, J.; Tang, L.; Xiang, J.; Ji, R.; Yuan, J.; Zhao, J.; Yu, R.; Tai, Y.; Song, L. Chlorine Doped Graphene Quantum Dots: Preparation, Properties, and Photovoltaic Detectors. Appl. Phys. Lett. 2014, 105, 111116-111120. (27) Li, X. M.; Lau, S. P.; Tang, L. B.; Ji, R. B.; Yang, P. Z. Multicolour Light Emission from Chlorine-Doped Graphene Quantum Dots. J. Mater. Chem. C 2013, 1, 7308-7313. 21



Page 22 of 25

(28) Zhao, J. H.; Tang, L. B.; Xiang, J. Z.; Ji, R. B.; Hu, Y. B.; Yuan, J.; Zhao, J.; Tai, Y. J.; Cai, Y. H. Fabrication and Properties of a High-Performance Chlorine Doped Graphene Quantum Dot Based Photovoltaic Detector. RSC Adv. 2015, 5, 29222-29229. (29) Ananthanarayanan, A.; Wang, Y.; Routh, P.; Sk, M. A.; Than, A.; Lin, M.; Zhang, J.; Chen, J.; Sun, H.; Chen, P. Nitrogen and Phosphorus Co-Doped Graphene Quantum Dots: Synthesis from Adenosine Triphosphate, Optical Properties, and Cellular Imaging. Nanoscale 2015, 7, 8159-8165. (30) Shieh, Y. T.; Wang, W. W. Radical Scavenging Efficiencies of Modified and Microwave-Treated Multiwalled Carbon Nanotubes. Carbon 2014, 79, 354-362. (31) Das, B.; Dadhich, P.; Pal, P.; Srivas, P. K.; Bankoti, K.; Dhara, S. Carbon Nanodots from Date Molasses: New Nanolights for the in Vitro Scavenging of Reactive Oxygen Species. J. Mater. Chem. B. 2014, 2, 6839-6847. (32) Li, Y.; Liu, H.; Liu, X. Q.; Li, S.; Wang, L.; Ma, N.; Qiu, D. Free-Radical-Assisted Rapid Synthesis of Graphene Quantum Dots and Their Oxidizability Studies. Langmuir 2016, 32, 8641-8649. (33) Chong, Y.; Ge, C.; Fang, G.; Wu, R.; Zhang, H.; Chai, Z.; Chen, C.; Yin, J. J. Light-Enhanced Antibacterial Activity of Graphene Oxide, Mainly Via Accelerated Electron Transfer. Environ. Sci. Technol. 2017, 51, 10154-10161. (34) Hui, L.; Huang, J.; Chen, G.; Zhu, Y.; Yang, L. Antibacterial Property of Graphene Quantum Dots (Both Source Material and Bacterial Shape Matter). ACS Appl. Mater. Inter. 2016, 8, 20-25. (35) Shi, L.; Chen, J. R.; Teng, L. J.; Wang, L.; Zhu, G. L.; Liu, S.; Luo, Z. T.; Shi, X. T.; Wang, Y. J.; Ren, L. The Antibacterial Applications of Graphene and Its Derivatives. Small 2016, 12, 4165-4184. 22


Page 23 of 25 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


(36) Habiba, K.; Bracho-Rincon, D. P.; Gonzalez-Feliciano, J. A.; Villalobos-Santos, J. C.; Makarov, V. I.; Ortiz, D.; Avalos, J. A.; Gonzalez, C. I.; Weiner, B. R.; Morell, G. Synergistic Antibacterial Activity of Pegylated Silver Graphene Quantum Dots Nanocomposites. Appl. Mater. Today 2015, 1, 80-87. (37) Luo, Z. M.; Yang, D. L.; Yang, C.; Wu, X. Y.; Hu, Y. L.; Zhang, Y.; Yuwen, L. H.; Yeow, E. K. L.; Weng, L. X.; Huang, W.; Wang, L. H. Graphene Quantum Dots Modified with Adenine for Efficient Two-Photon Bioimaging and White Light-Activated Antibacteria. Appl. Surf. Sci. 2018, 434, 155-162. (38) Nia, Z. K.; Chen, J. Y.; Tang, B.; Yuan, B.; Wang, X. G.; Li, J. L. Optimizing the Free Radical Content of Graphene Oxide by Controlling Its Reduction. Carbon 2017, 116, 703-712. (39) Zheng, J.; Liu, H. T.; Wu, B.; Di, C. A.; Guo, Y. L.; Wu, T.; Yu, G.; Liu, Y. Q.; Zhu, D. B. Production of Graphite Chloride and Bromide Using Microwave Sparks. Sci. Rep. 2012, 2, 662-668. (40) Zhang, M.; Dai, L. M. Carbon Nanomaterials as Metal-Free Catalysts in Next Generation Fuel Cells. Nano Energy 2012, 1, 514-517. (41) Gong, K.; Du, F.; Xia, Z.; Durstock, M.; Dai, L. Nitrogen-Doped Carbon Nanotube Arrays with High Electrocatalytic Activity for Oxygen Reduction. Science 2009, 323, 760-764. (42) Jeon, I. Y.; Choi, H. J.; Choi, M.; Seo, J. M.; Jung, S. M.; Kim, M. J.; Zhang, S.; Zhang, L.; Xia, Z.; Dai, L.; Park, N.; Baek, J. B. Facile, Scalable Synthesis of Edge-Halogenated Graphene Nanoplatelets as Efficient Metal-Free Eletrocatalysts for Oxygen Reduction Reaction. Sci. Rep. 2013, 3, 1810-1817. (43) Li, S.; Li, Y.; Cao, J.; Zhu, J.; Fan, L.; Li, X. Sulfur-Doped Graphene Quantum Dots as a Novel Fluorescent Probe for Highly Selective and Sensitive Detection of Fe3+. Anal. Chem. 2014, 86, 23



Page 24 of 25

10201-10207. (44) Li, Y.; Zhao, Y.; Cheng, H.; Hu, Y.; Shi, G.; Dai, L.; Qu, L. Nitrogen-Doped Graphene Quantum Dots with Oxygen-Rich Functional Groups. J. Am. Chem. Soc. 2012, 134, 15-18. (45) Qu, D.; Sun, Z. C.; Zheng, M.; Li, J.; Zhang, Y. Q.; Zhang, G. Q.; Zhao, H. F.; Liu, X. Y.; Xie, Z. G. Three Colors Emission from S,N Co-Doped Graphene Quantum Dots for Visible Light H2 Production and Bioimaging. Adv. Opt. Mater. 2015, 3, 360-367. (46) Zhang, J.; Wang, J.; Wu, Z. X.; Wang, S.; Wu, Y. M.; Liu, X. Heteroatom (Nitrogen/Sulfur)-Doped Graphene as an Efficient Electrocatalyst for Oxygen Reduction and Evolution Reactions. Catalysts 2018, 8, 475-484. (47) Yang, S. B.; Zhi, L. J.; Tang, K.; Feng, X. L.; Maier, J.; Mullen, K. Efficient Synthesis of Heteroatom (N or S)-Doped Graphene Based on Ultrathin Graphene Oxide-Porous Silica Sheets for Oxygen Reduction Reactions. Adv. Funct. Mater. 2012, 22, 3634-3640. (48) Li, J. C.; Hou, P. X.; Liu, C. Heteroatom-Doped Carbon Nanotube and Graphene-Based Electrocatalysts for Oxygen Reduction Reaction. Small 2017, 13, 1702002-1702015. (49) Krishnamoorthy, K.; Veerapandian, M.; Yun, K.; Kim, S. J. The Chemical and Structural Analysis of Graphene Oxide with Different Degrees of Oxidation. Carbon 2013, 53, 38-49.

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Chlorine doped graphene quantum dots synthesized by electrochemical method exhibits both extraordinary ROS scavenging performance in dark and superior ROS generating ability during sun exposure.


Chlorine-Doped Graphene Quantum Dots with Enhanced Anti- and

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