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Yellow Fluorescent Nitrogen and Bromine Co-doped Graphene

Quantum Dots for Bioimaging
Lin Gong, Ji Sun, Peng Zheng, Yousong Liu,* and Guangcheng Yang*
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ABSTRACT: Currently, the large-scale commercial/industrial application of

graphene quantum dots (GQDs) is generally limited by their low production and
lack of diverse photoluminescence (PL) properties such as GQDs with long-
wavelength emissions and high quantum yields. Herein, for the first time, a facile
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deflagration method was developed for the ultrafast and gram-scale synthesis of N
and Br co-doped GQDs (NBr-GQDs) with bright yellow PL emissions. NBr-GQDs
exhibited an excitation-independent emission property with a central PL wavelength of ∼579 nm. The results of theoretical
calculations revealed that N and Br co-doping may reduce the band gap between the excited singlet states and decrease the
intersystem crossing effect of excited electrons from the singlet to the triplet state, thus considerably improving the quantum yield
(as high as 52%). Moreover, a series of experiments were performed, and their results showed that the synthesized NBr-GQDs
achieved excellent pH tolerance, long PL lifetime, and low cytotoxicity. Using HeLa cells as specimens, it was demonstrated that
NBr-GQDs could successfully enter the HeLa cytoplasm and achieve high-quality fluorescent labeling, indicating their great
potential in the bioimaging field.
KEYWORDS: graphene quantum dots, co-doping, high quantum yields, bioimaging, deflagration

1. INTRODUCTION accompanied by only green or blue PL emissions with

Usually, graphene quantum dots (GQDs) refer to the zero- relatively low QYs, limiting their practical applications.9 In
dimensional graphene nanosheets with sizes <10 nm.1 Such bottom-up methods, carbon-containing molecular precursors
nanosheets offer attractive properties such as good photo- are converted to GQDs via appropriate chemical/physical
luminescence (PL) performance, low toxicity, excellent treatments, including pyrolysis,20 ultraviolet irradiation,21 and
biocompatibility, and high catalytic activity.2,3 Thus, GQDs solvothermal treatment.22 Although the preparation processes
show a broad application potential in sensing, bioimaging, of the bottom-up methods are usually complex and the
production yield is generally low, such methods are suitable for
photo-/electro-catalysis, and other fields, mostly owing to their
regulating and modifying GQDs (such as heteroatom doping)
quantum confinement and edge effects.4,5 However, primarily
in the synthesis processes.23 Thus, the morphology controll-
because of the following aspects and certain deficiencies, the
ability and the QY of modified GQDs can be considerably
large-scale industrialization and commercialization of GQDs
improved.24 In summary, developing a facile and mass
are limited: (1) pristine GQDs obtained using industrial-scale
production method that can exploit the advantages of the
synthesis usually exhibit low quantum yields (QYs) of 0.8−
aforementioned two synthesis strategies and avoid their
9.1%.6 (2) Although the gram-scale synthesis of GQDs with
disadvantages for synthesizing high-quality GQDs is a
green or blue PL emissions has been realized,7,8 that of GQDs
challenging task and urgently required.
with long-wavelength fluorescence emissions (such as yellow
Since the realization of N-doped GQDs,25 modifying GQDs
or red light emissions) and high QYs is relatively limited.9
by heteroatom doping has become an effective method for
The current strategies for synthesizing GQDs can be
improving the QY and tuning the PL wavelength. Various
categorized as top-down and bottom-up methods.10,11 Top-
elements, such as N,26 B,27 S,28,29 P,30 and F,31,32 have been
down synthesis methods primarily include oxidative cleavage in
reported to be capable of adjusting the band gap and optical/
addition to hydrothermal,12 microwave,13 and electrochemical
electronic properties of doped GQDs.22 In addition to single-
methods14 and are usually used to synthesize GQDs by simply
cutting various large-sized carbonaceous materials, such as
graphene oxide,15 graphene sheets,16 and carbon nanotubes,17 Received: July 16, 2021
to quantum sizes.18 Although top-down methods are easy to Accepted: July 27, 2021
perform, they show a low cutting efficiency (generally <5 wt Published: August 9, 2021
%) and require high time consumption and harsh reaction
environments.19 Furthermore, GQDs obtained using top-down
methods show a heterogeneous morphology and are usually

© 2021 American Chemical Society https://doi.org/10.1021/acsanm.1c02004

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ACS Applied Nano Materials
Figure 1. Schematic of the NBr-GQD synthesis process.
atom doping, co-doping seems to provide additional attractive
optical or other properties to GQDs owing to the enhanced
coupling effect between different doping atoms.31 For example,
Luo et al. used aqueous ammonia and sulfur as precursors to
prepare N and S co-doped GQDs (NS-GQDs) using a
hydrothermal method.33 Compared with N-doped GQDs, NS-
GQDs showed a considerably improved QY (41%) and an
obvious blue PL emission shift (54 nm). Nevertheless, an in-
depth understanding of the modulating mechanism of the
intrinsic properties of co-doped GQDs is still required.
In this study, for the ultrafast and gram-scale synthesis of N
and Br co-doped GQDs (NBr-GQDs), a one-step deflagration
method was developed. The synthesized NBr-GQDs exhibited
a bright yellow PL emission with the maximum QY of 52%.
Theoretical calculations were performed, showing that N and
Br co-doping can tune the band gap and improve the PL
performance of GQDs. Furthermore, the low cytotoxicity and
stable PL intensity (in a wide pH range) of the fabricated NBr-
GQDs exhibited considerable application potential in bioimag-
ing.
2. EXPERIMENTAL SECTION
2.1. Chemicals. Reaction precursors, including hexabromoben-
zene (C6Br6) and sodium azide (NaN3), were purchased from Sigma-
Aldrich (Shanghai, China). For biological experiments, HeLa cells,
Dulbecco’s modified Eagle’s medium (DMEM), the alamarBlue
reagent, phosphate-buffered saline (PBS), and 4′,6-diamidino-2-
phenylindole dihydrochloride (DAPI) were obtained from Shiyanjia
Lab (www.shiyanjia.com). Deionized water (18.24 MΩ·cm) was used
throughout the experiments.
2.2. Synthesis of NBr-GQDs. For synthesizing NBr-GQDs, 3 g of
C6Br6 and a certain amount of NaN3 were mixed in a quartz mortar
with a molar ratio of 1:6 (C6Br6/NaN3). Then, 3 mL of ethanol was
added to the abovementioned mixture, and this mixture was physically
ground until dry to obtain a uniform reaction precursor mixture. The
obtained mixture was placed in a 100 mL stainless-steel reactor with a
temperature control system (Figure S1) and rapidly heated to 450 °C
to initiate the ultrafast deflagration reaction (in an Ar atmosphere).
After cooling naturally to room temperature, the reaction products
were purified overnight using dialysis bags (size: 50 mm, 500 Da).
Finally, NBr-GQDs were successfully obtained by vacuum drying (80
°C, 12 h).
2.3. Cell Viability Tests. All experiments were repeated at least
three times. First, HeLa cells were obtained and cultured in DMEM at
37 °C (5% CO2 atmosphere). Then, they were seeded in a 96-well
plate at a concentration of 104 cells/well for 24 h. Next, they were
treated with different NBr-GQD concentrations (0−200 μg/mL) and
incubated for another 24 h. Subsequently, alamarBlue assays were
performed as toxicity texts. Briefly, 10% alamarBlue by volume was
added to the aforementioned cells for 2 h to change their color from
blue to pink. The absorbance values of the samples were recorded
using a microplate reader (800 TS, BioTek) at 570 nm.
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2.4. Bioimaging Experiments. The culture conditions of HeLa
cells are the same as those described in Section 2.3. First, the HeLa
cells were seeded and incubated in a 35 mm-sized laser confocal cell
culture dish with a density of 105 cells/dish for 12 h. Thereafter, 100
μg/mL NBr-GQDs were used to treat the cells for another 4 h. As the
control, DAPI was then used to stain the nuclei for 15 min. Finally,
the above samples were washed with PBS three times, after which
fluorescent bioimages were obtained using confocal laser scanning
microscopy at an excitation wavelength of 405 nm (SP8, Leica).
2.5. Characterization. Transmission electron microscopy (TEM,
Tecnai G2 F20, FEI), X-ray diffraction analysis (XRD, X′Pert PRO
MPD, PANalytical), Raman spectroscopy (DXR, Thermo Fisher), X-
ray electron spectroscopy (XPS, Thermo ESCALAB 250XI, Thermo
Fisher), and atomic force microscopy (AFM, Dimension Edge,
Bruker) were used to analyze the morphology and molecular structure
of the synthesized NBr-GQDs. The optical properties of NBr-GQDs,
such as the PL emission, fluorescence lifetime, and absolute QY, were
determined using a steady/transient fluorescence spectrometer
(FLS1000, Edinburgh), and an ultraviolet−visible (UV−vis)
absorption curve was obtained using a UV−vis spectrometer (UV-
3600, SHIMADZU). Bioimaging experiments were performed using
confocal laser scanning microscopy (SP8, Leica).
3. RESULTS AND DISCUSSION
3.1. Preparation and Structural Characterization of
NBr-GQDs. Figure 1 describes the process of synthesizing
NBr-GQDs. A mixture of NaN3 and C6Br6 was first placed in a
stainless-steel reactor with a temperature control system. Then,
the temperature was rapidly increased to 450 °C to trigger an
ultrafast deflagration reaction. To understand the reaction, a
self-built device, which includes a laser igniter (1064 nm, 8 W),
a thermocouple thermometer, and a high-speed camera, was
used to record the temperature changes and durations during
the reaction process. The images obtained using the high-
speed camera showed that the entire reaction lasted only for
170 ms (Figure S2). When the reaction was induced, NaN3
rapidly decomposed into active sodium (Na) and N-free
radicals,34 accompanied by a large amount of heat release.
Thus, the reaction temperature increased to >1100 °C in just
∼100 ms, which then quickly returned to room temperature
(Figure S3). At such high temperatures, certain amounts of
active Na could capture Br atoms and cut C6Br6 into smaller
fragments. Furthermore, the N radicals and residual Br could
act as heteroatom precursors in the short-term carbon lattice
regrowth process to achieve co-doping in NBr-GQDs because
the ultrarapid decrease in temperature hindered the continued
lattice growth. XRD analysis of the unpurified product
demonstrated the presence of NaBr and Na2CO3 in the
product (Figure S4), further indicating the reaction mechanism
in which the active Na could capture the Br atoms from the
C6Br6 molecules. The Na2CO3 formation was attributed to the
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Figure 2. TEM (a,b) and high-resolution TEM (c) images of NBr-GQDs. (d) AFM image of NBr-GQDs (inset: height analysis). XRD (e), Raman
(f), and XPS N 1s (g) and Br 3d (h) characterization of NBr-GQDs.

Figure 3. (a) PL spectra of NBr-GQDs; (b) UV−vis absorption curve and excitation spectra of NBr-GQDs; (c) PL intensity of the NBr-GQDs in
various pH aqueous environments; and (d) PL decay curve and the fitting curve analysis of NBr-GQDs.

exposure of a part of the excess Na in the product to air. In
terms of the sample product yield, 3.1 g of the purified product
could be obtained from 5.12 g of the reaction precursors,
indicating a gram-scale synthesis with a yield of approximately
60%. Moreover, the product output could be facilely increased
when sufficient amounts of precursors were added. In
summary, this synthesis strategy could easily achieve a fast,
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facile, and gram-scale production of high-quality GQDs, thus
showing an attractive industrial application potential.
The morphology and structure of the fabricated NBr-GQDs
were examined using multiple characterizations. TEM images
showed the successful synthesis of uniform NBr-GQDs (Figure
2a,b) with an average particle size of ∼3.5 nm (Figure S5),
proving that the reported synthesis method could maintain a
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Figure 4. Energy-level distributions for the singlet (S) and triplet (T) states of the GQDs, edge N-GQDs, and NBr-GQDs.
consistent size and morphology of products even in gram-scale
preparation. Clear lattice fringes were observed with a lattice
plane distance of 0.24 nm (Figure 2c), corresponding to typical
graphitized carbon structures.35 Moreover, the AFM character-
ization revealed that the sample thickness was <2 nm (Figure
2d, inset). Note that additional fine structures of NBr-GQDs
were examined using XRD, Raman, and XPS analyses. Figure
2e shows a broad XRD peak located at ∼25°, attributed to the
(002) diffraction of graphitic carbon, which is consistent with
the results characterized by high-resolution TEM.36 Two
typical Raman vibration peaks were observed at ∼1330 and
1591 cm−1 (Figure 2f), corresponding to the G and D bands
with an intensity ratio (ID/IG) of 1.27. Compared with pristine
graphene (the ID/IG value is usually widely reported to be close
to 1), such a high ID/IG value indicates that the heteroatoms
were successfully doped into the products.37 The full-scan XPS
spectrum of NBr-GQDs revealed the presence of N, Br, and O
elements in the prepared sample (Figure S6). Moreover, the N
1s XPS characterization (Figure 2g) demonstrated that N
atoms were doped in the products in the form of pyridinic N
(398.4 eV) and pyrrolic N (399.5 eV), which usually tend to
exist at the edge of carbon skeletons as edge N.38 In terms of
Br doping, only a C−Br bond was observed by using Br 3d
XPS analysis (Figure 2h). Furthermore, two fitting peaks were
found at 70.4 and 71.4 eV, corresponding to C−Br 3d3/2 and
C−Br 3d5/2, respectively.39 One Br atom prefers to bond with
one C in graphene for completing the octet, which usually
sticks out from the graphene planes because of its considerably
larger size compared with that of C.40
3.2. PL Properties. The PL property is an attractive feature
of GQDs. Figure 3a shows that the PL curves of NBr-GQDs
were excited at different wavelengths. The central wavelength
of all the emissions showed a negligible shift, and the PL
intensities showed an obvious change. When the excitation
wavelength was increased from 320 to 420 nm, the PL
intensity first increased and then decreased, with the strongest
PL intensity appearing at excitation wavelengths of 320−360
nm with a central wavelength of ∼579 nm. The excitation-
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independent emission property indicates the high-level size
homogeneity and molecular structure of the synthesized NBr-
GQDs. The coexistence of the heterogeneous size and
molecular structure of GQDs (even slight differences in
GQDs) results in the excitation-independent emission
property of the PL, owing to the differences in their energy
gaps.41 The UV−vis absorption curve of NBr-GQDs (Figure
3b) shows that only a single absorption peak appeared at 232
nm with a long and smooth trail, corresponding to the π−π*
electronic transitions of the sp2 hybrid carbon cores.42
However, the n−π* electronic transition peak of the oxygen-
containing group at the edge of the graphite cores, which
usually appears at ∼360 nm,43 was not observed, thus
demonstrating the low oxidation degree of NBr-GQDs. As
confirmed using O 1s XPS analysis (Figure S7), only 3 at. %
oxygen atoms were introduced into NBr-GQDs. The XPS peak
at 531.8 eV was attributed to the adsorbed hydroxyl.44 It is
inferred that the co-doping of edge N and large Br atoms
around the carbon cores may inhibit the introduction of
certain oxygen-containing functional groups.
To confirm the influence of pH on NBr-GQDs, their PL
properties were evaluated in different pH aqueous solutions.
The PL intensity of many GQDs usually decreases
substantially in strong acidic or alkaline aqueous environments,
primarily because the protonation of oxygen-containing groups
(particularly carboxyl) at the edges of GQD sheets induces the
disruption of their surface charges.1,45 However, in this work,
the prepared NBr-GQDs showed high pH tolerance when
tested in a wide pH range of solutions (Figure 3c and its inset).
Even under extreme acidic (pH = 2) or alkaline (pH = 13)
conditions, the PL intensity of NBr-GQDs only decreased by
<13%. Moreover, no obvious color difference was observed in
the emitted fluorescence of NBr-GQDs under different pH
conditions, demonstrating the high stability and wide
application potential of the synthesized NBr-GQDs even in
extreme chemical environments. The PL lifetime of NBr-
GQDs was examined, and the average lifetime was calculated
to be 7.8 ns, using Fluoracle software (Figure 3d).
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Figure 5. Viability tests of the HeLa cells treated with different concentrations of NBr-GQDs (a); laser confocal microscopy images of HeLa cells
without any treatment under a bright field (b) and a dark field (c); laser confocal microscopy images of the HeLa cells treated with DAPI only (d)
and NBr-GQDs (e,f).
Furthermore, a biexponential curve perfectly fitted the decay
measurement results with two lifetime components, consid-
erably attributed to the recombination process in the core
states (sp 2 carbon) and surface states (doped edge
heteroatoms), respectively.46 The N and Br co-doping
remarkably improved the QY of the NBr-GQDs. The absolute
QY of NBr-GQDs was found to be as high as 52%. Because the
radii of Br atoms are significantly larger than those of C atoms,
doping Br atoms into GQDs is relatively difficult. For the first
time, NBr-GQDs were synthesized in this study. For
comparison, some QYs of halogen atom-doped/co-doped
GQDs, such as Cl-doped GQDs (6.8%),47 N and Cl co-doped
GQDs (20%),48 F and N co-doped GQDs (22.98),49 and F-
doped GQDs (31%),50 reported in the literature were listed,
showing the competitive QY of the prepared NBr-GQDs. Also,
the QY improvement mechanism of NBr-GQDs was studied
below.
3.3. Explanation of the PL Mechanism. To understand
the PL mechanism of NBr-GQDs, density functional theory
(DFT) calculations were performed using the Gaussian 16
software package at the B3LYP/6-311g (d) level with a D3(BJ)
empirical dispersion correction. The electronic singlet state
(Si) and triplet state (Ti) of NBr-GQDs and their control were
obtained (Figure 4). After photoexcitation, the excited
electrons were generally found to be concentrated in the
highly excited states (S2, S3...). Because of the instability of the
excited electrons, an internal conversion occurred preferably
(Kasha’s rule), resulting in the vibrational relaxation of the
excited electrons from the highly excited states (S2, S3...) to the
S1 state. Then, fluorescence was observed, and the excited
electrons returned from the S1 state to the S0 ground state.
Compared with C atoms, N atoms exhibit considerably better
electronegativity (3.04 for N and 2.55 for C) but a similar
atomic radius, making it easier for N atoms to be doped into
GQDs and change the charge distribution of GQDs, thus
achieving different energy level structures.51 It can be observed
in Figure 4 that the energy differences of N-GQDs between S1,
S2, and S3 are lower than those of GQDs. Thus, the
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photoexcited electrons tend to return from the highly excited
singlet states (S2, S3...) to the S1 state owing to the vibrational
relaxation effect with low nonradiative energy losses (such as
heat). Additionally, most of the energy can be released in the
form of radiation energy from S1 to S0, thus improving the
fluorescence intensity. It is found that the energy level
differences between the excited singlet states are further
reduced when Br atoms are introduced. Moreover, Br atoms
contain more electrons in their outer layers than N atoms,
promoting the excitation of more electrons and thus enriching
the excited electrons in the excited singlet state, resulting in an
enhanced QY of NBr-GQDs.52 Furthermore, the doping of
large-sized Br atoms can partly transfer the sp2 hybrid structure
of GQDs to the sp3 hybrid structure,53 leading to a narrow
energy gap of NBr-GQDs resulting from the uneven orbital
distribution.54 This is why NBr-GQDs emit a bright yellow
fluorescence rather than the green or blue fluorescence usually
emitted by GQDs and N-GQDs. In addition to the
fluorescence emission, some excited electrons may move
from the excited Si state to the Ti state owing to the
intersystem-crossing effect, inducing phosphorescence emis-
sions (excited electrons returning from the T1 to T0 state).
Based on the DFT results, the energy differences of NBr-
GQDs between excited S and T states increased, considerably
reducing the probability of the intersystem-crossing effect and
decreasing the phosphorescence intensity. Above all, N and Br
co-doping could increase the probability of enriching excited
electrons in the S1 state and decrease the intersystem-crossing
effect; therefore, most excited electrons could return from S1 to
S0, thus improving the QY of NBr-GQDs.
3.4. Cytotoxicity and Bioimaging Performance. A
series of experiments were performed to examine the
cytotoxicity and cell-bioimaging performance of NBr-GQDs
using HeLa cells as the specimens. Figure 5a shows the
viability of HeLa cells treated with different concentrations of
NBr-GQDs. When the NBr-GQDs’ concentration was
increased, the viability of HeLa cells decreased gradually and
slightly. However, when the NBr-GQDs’ concentration was as
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high as 200 μg/mL, ∼90% of the cells survived, indicating the
extremely low cytotoxicity of NBr-GQDs. In terms of the cell-
bioimaging performance, spindle-shaped HeLa cells without
any treatment could not be observed via confocal microscopy
imaging in a dark field (Figure 5b,c). Only blue fluorescent
HeLa nuclei were observed when DAPI was used (Figure 5d).
A bright yellow fluorescence clearly appeared in the HeLa
cytoplasm after the NBr-GQD treatment (Figure 5e,f). Overall,
the results showed that NBr-GQDs can successfully enter the
HeLa cytoplasm and achieve high-quality fluorescent labeling
or bioimaging, indicating their additional potential applications
in the bioimaging field.
4. CONCLUSIONS
In summary, a facile and gram-scale synthesis of NBr-GQDs
was realized using an ultrafast deflagration method. Because of
their high-level homogeneity in size and molecular structure,
NBr-GQDs showed an excitation-independent emission
property of PL at a central wavelength of 579 nm. Based on
the theoretical calculations, N and Br co-doping could
considerably adjust the energy-band structures to reduce the
intersystem crossing effect of the excited electrons and increase
the return probability of the electrons from the first singlet
state to the ground state, achieving a considerably improved
QY (52%). Furthermore, even in extreme pH environments,
the PL intensity of NBr-GQDs only decreased by <13%.
Moreover, in addition to their good pH tolerance, NBr-GQDs
exhibited very low cytotoxicity. After incubation for 24 h, HeLa
cells treated with 200 μg/mL NBr-GQDs still showed a
survival rate of >90%. The long fluorescence lifetime (7.8 ns)
and excellent cell-staining performance were experimentally
confirmed, showing the great application potential of NBr-
GQDs in the bioimaging field.
■ ASSOCIATED CONTENT
* Supporting Information
sı
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/acsanm.1c02004.
Photograph of the reaction device; XRD analysis of the
products without purification; high-speed photographs;
and reaction temperature change data (PDF)
■
AUTHOR INFORMATION
Corresponding Authors
Yousong Liu − Institute of Chemical Materials, China
Academy of Engineering Physics, Mianyang 621900, China;
Email: ysliu@caep.cn
Guangcheng Yang − Institute of Chemical Materials, China
Academy of Engineering Physics, Mianyang 621900, China;
orcid.org/0000-0002-6034-3860; Email: ygcheng@
caep.cn
Authors
Lin Gong − Institute of Chemical Materials, China Academy
of Engineering Physics, Mianyang 621900, China
Ji Sun − School of Emergency Science, Xihua University,
Chengdu 610039, China
Peng Zheng − National Special Superfine Power Engineering
Research Center, Nanjing University of Science and
Technology, Nanjing 210094 Jiangsu, China
Complete contact information is available at:
https://pubs.acs.org/10.1021/acsanm.1c02004
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Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
This work was supported by the National Natural Science
Foundation of China (nos. 11802276 and 11772307).
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