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- Metal-free polymeric carbon nitride photocatalytic bactericide: Precursor-controlled killing activity of E. coli
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- Environmental Advances 4 (2021) 100067
Contents lists available at ScienceDirect
Environmental Advances
journal homepage: www.elsevier.com/locate/envadv
Metal-free polymeric carbon nitride photocatalytic bactericide:
precursor-controlled killing activity of E. coli
Shan Ding a,b, Yan Li a,b,c, Tao Sun a,b,c, Bin Xue a,b,c,∗
a
Department of Chemistry, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China
b
Quality Supervision, Inspection and Testing Center for Cold Storage and Refrigeration Equipment (Shanghai), Ministry of Agriculture, Shanghai 201306, China
c
National Experimental Teaching Demonstration Center for Food Science and Engineering (Shanghai Ocean University), Shanghai 201306, China
a r t i c l e i n f o a b s t r a c t
Keywords: The photocatalytic sterilization activity of polymeric carbon nitride is closely related to its microstructure. In
Polymeric carbon nitride this study, four kinds of polymeric carbon nitride were prepared with melamine, dicyandiamine, thiourea and
Precursor urea as precursors respectively. These polymeric carbon nitrides were similar in crystallinity and bonding, but
Microstructure
differ significantly in texture, optical and photoelectrochemical properties. These changes resulted in different
Photocatalysis
performances of polymeric carbon nitrides in their photocatalytic activities to kill E. coli. The polymeric carbon
Antibacterial
nitride prepared from urea exhibited significantly better photocatalytic antibacterial activity than other control
samples. The advantage of the activity should be attributed to the synergy of many favorable factors, such as the
shape of flake, large specific surface area, open pore structure, high valence band potential, low photogenerated
carrier recombination rate, large photocurrent density and low electron transfer impedance. This study showed
that urea-derived polymeric carbon nitride is very promising for the preparation advanced materials with higher
photocatalytic sterilization activity.
1. Introduction Semiconductor-based photocatalysis is a promising new antibacte-
rial technology (Xu et al., 2019)(Dong, et al., 2020). Under ultravio-
With continuous development of society, the amount of sewage dis- let or visible light irradiation, the separation of photogenerated carri-
charge continues to increase (Patel, et al., 2019;(Wang et al., 2019) ers occurs over the semiconductor photocatalyst. (Dong, et al., 2020;
Guo, et al., 2020). Pathogenic bacteria, including Escherichia coli, Lis- Shen, et al., 2020). These photogenerated electrons and holes then re-
teria, and Staphylococcus aureus, are very common pollutants in sewage act with oxygen and water to produce reactive oxygen species (ROS)
(He, et al., 2021; Zhao, et al., 2019). Because of their biological charac- such as superoxide anions and hydroxyl radicals, thereby killing bacte-
teristics such as fast reproduction (Yuan et al., 2020) (Yuan, et al., 2020), ria ((Zhang, 2020)Zhao, et al., 2020; Liu, et al., 2020). Importantly,
large numbers (An, et al., 2021), and easy survival (Zhang, et al., 2020), the photocatalytic sterilization technology has unique advantages in
the pathogenic bacteria have a great impact on the ecological environ- overcoming bacterial resistance (Ding, et al., 2019). Among many semi-
ment and human health (Bradley, 2019; Zhang et al., 2019). In addition, conductor photocatalysts, polymeric carbon nitride (PCN) has attracted
the risk of contamination by pathogenic bacteria always exists during extensive attention because of its facile preparation, low cost, stable
storage and transportation of food (Shaharoona, et al., 2019). The con- physical and chemical properties and environmental friendliness (Sai-
sumption of food contaminated with pathogenic bacteria by humans or Anand, et al., 2018;(Li et al., 2019)(Dong et al., 2020)(Li et al., 2020)
organisms will disrupt the balance of intestinal flora and cause some Miao, et al., 2019). Moreover, PCN does not contain metal elements,
food-borne diseases (Wang, et al., 2019; Ganguly, et al., 2018). For a has good biocompatibility and visible light response, which also make
long time, various organic antibacterial substances represented by an- it a more competitive photocatalytic antibacterial material (Wang, et al.,
tibiotics have played an important role in killing pathogenic bacteria 2017; (Li, 2020)(Li, 2021)).
(Dong, et al., 2021; Hu, et al., 2021). Unfortunately, these antibacterial PCN is usually prepared by a thermal polycondensation route using
agents have encountered an unprecedented crisis due to the resistance various nitrogen-rich organic compounds under calcination conditions
of pathogenic bacteria (Anand, et al., 2019; Li, et al., 2018). Therefore, (Cheng, et al., 2019). The precursors strongly affect the physicochem-
humans urgently need to develop a new antibacterial strategy to kill ical properties of the prepared PCN, which results in the difference of
bacteria. their photocatalytic antibacterial activity. The correlation between the
∗
Corresponding author.
E-mail addresses: bxue@shou.edu.cn, nkxuebin@126.com (B. Xue).
https://doi.org/10.1016/j.envadv.2021.100067
Received 18 March 2021; Received in revised form 16 April 2021; Accepted 3 May 2021
2666-7657/© 2021 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
- S. Ding, Y. Li, T. Sun et al. Environmental Advances 4 (2021) 100067
Fig. 2. FT-IR spectra of photocatalysts.
transform infrared spectra of the samples were obtained in the wave-
length range of 4000~500 cm−1 on a FTIR-650 (Gangdong, Tianjin)
infrared spectrometer with KBr as a reference (Liu, et al., 2020). The
nitrogen adsorption-desorption performances of the samples were ob-
tained on a Micromeritics ASAP 2020 adsorption instrument. The shape
of the samples was observed by a thermal field emission scanning elec-
tron microscope (FE-SEM, Hitachi SU5000). The acceleration voltage is
5 kV. The UV-Vis diffuse reflectance spectra (UV-Vis DRS) were obtained
by an ultraviolet spectrophotometer (Hitachi U-3900) using BaSO4 as a
reference in the range of 200~800 nm (She, et al., 2019). The photo-
luminescence (PL) spectra of the samples were derived from a fluores-
cence spectrophotometer (Edinburg Instruments FS5) at room tempera-
ture, and the excitation wavelength is 370 nm (Wang, et al., 2019). A
CHI660D (Chenhua, Shanghai) electrochemical workstation with a stan-
dard three-electrode system was used to evaluate the photoelectrochem-
ical properties of the samples. The reference electrode is AgCl/Ag (sat-
Fig. 1. (a) XRD patterns and (b) Enlarged view of (002) planes of photocata-
urated KCl), the counter electrode is a platinum plate, and the working
lysts.
electrode is a indium tin oxide (ITO) conductive glass. The slurry made
by mixing samples, Nafion and ethanol was evenly dipped and coated
structure and antibacterial activity of PCN obtained from different pre- on a 1 × 1 cm conductive glass, dried at 80°C for 12 hours and then cal-
cursors is crucial for promoting the application of PCN-based photocat- cined at 350°C for 1 hour under a nitrogen atmosphere. The light source
alytic antibacterial materials. However, as far as we know, systematic is a 5 W LED lamp with characteristic wavelength of 420 nm, and the
studies on this aspect are lacking. In this study, we selected four com- electrolyte is a 0.2 mol L−1 Na2 SO4 aqueous solution. The bias voltage
mon precursors, including melamine, dicyandiamine, thiourea and urea, used in the photocurrent response test is 0.35 V. The frequency range is
to prepare PCN. The crystallinity, chemical structure, texture, optical 0.1~100,000 Hz in electrochemical impedance spectroscopy (EIS) test.
properties, energy band structure and photoelectrochemical properties
2.3. Photocatalytic antibacterial activity test
of these PCN were investigated. Meanwhile, the photocatalytic bacteri-
cidal activities of E. coli over the PCN were tested and the corresponding
The typical strain of Gram-negative bacteria E.coli was selected as
structure-activity relationship was discussed.
the model strain for antibacterial activity test. E.coli (K12D31) stored
in -80°C refrigerator was first taken out, and then part of E.coli was
2. Material and methods dipped with inoculation ring to make plate lines. The obtained plate was
cultured at 37°C for 24 hours, and then single colonies were picked out
2.1. Preparation of PCN and placed in Luria-Bertani liquid medium at 37°C for 150 rpm for 12
hours. The culture medium was then absorbed into the prepared Luria-
10 g of different precursors including melamine, dicyandiamine, Bertani liquid medium at 37°C and 250 rpm for 3 hours (Xu, et al., 2017).
thiourea or urea were taken in a capped crucible, heated up to 550°C in It can make E. coli reach the index phase.
static air, and kept for 2 hours. The obtained samples were recorded as The above medium was centrifuged in a centrifuge tube at 8000 rpm
PCN-M, PCN-D, PCN-T or PCN-U, respectively. for 5 min to obtain the bacteria. After being washed with sterile nor-
mal saline, the bacteria were resuspended with sterile normal saline to
2.2. Characterization obtain the E.coli suspension with the concentration of 6.0 × 107 CFU
mL−1 . The photocatalyst solution with a concentration of 0.7 mg mL−1
The X-ray diffraction (XRD) patterns of the samples were collected on was prepared in advance by ultrasonication of a mixture of PCN and wa-
a Bruker D8 ADVANCE diffractometer with a Cu-K𝛼 monochromated ra- ter for 30 min. The suspension was added to the photocatalyst solution
diation source (𝜆 = 0.1540562 nm). The X-Ray tube voltage and current and stirred in the dark for 30 minutes. A 5 W LED lamp (𝜆 = 420 nm)
are 40 kV, and 40 mA, respectively (Wang, et al., 2019). The Fourier was suspended at a distance of 5 centimeters from the liquid surface as
2
- S. Ding, Y. Li, T. Sun et al. Environmental Advances 4 (2021) 100067
Fig. 3. FESEM images of photocatalysts: (a) PCN-M (b) PCN-D (c) PCN-T and (d) PCN-U.
a light source. After the light source was turned on, the samples were
taken every 30 minures under a constant stirring. After concentration
gradient dilution with sterile normal saline, 0.1 mL sample was pipet-
ted and coated on a plate. After cultivation at 37°C for 24 hours, the
plate counting was performed.
At the same time, the contrast experiments were carried out in the
two cases of only catalyst without light source and only light source
without catalyst. Each experiment was made in triplicate, and the uten-
sils and media involved in the experiments were all sterilized before
used.
2.4. E.coli sample preparation for SEM observation
The mixture of E.coli and photocatalyst after photocatalysis was cen-
trifuged for 5 minutes at 8000 rpm. Individual E.coli was collected di-
rectly and washed using phosphate buffer solution (PBS) for three times.
The samples were then fixed with 2.5% glutaraldehyde solution, washed
with phosphate buffer solution for three times, and centrifuged. Then
E.coli were dehydrated, dried and sprayed with 30, 50, 70, 80, 90 and
100 % ethanol solution, and then the morphology of E.coli was observed
by FE-SEM (Zeng, et al., 2019).
3. Results and discussion
3.1. Characterization of photocatalysts
The XRD patterns of PCN prepared from four precursors are shown in
Fig. 1a. It can be clearly seen that the four photocatalysts have character-
istic peaks at ~13.2 ° and ~27.2 °, indicating the presence of graphite-
like carbon nitride. These two characteristic peaks correspond to (100)
and (002) crystal planes, which can be attributed to the repeated ar-
rangement of triazine ring units in the plane and the accumulation of
conjugated aromatic systems between the layers, respectively (Li, et al.,
2020; Li, et al., 2019). Fig. 1b shows that the positions of the (002) crys-
tal planes of PCN prepared from different precursors are slightly differ-
Fig. 4. (a) Nitrogen adsorption isotherms (b) Pore size distribution curves of ent. For PCN-M, PCN-D, PCN-T and PCN-U, these peaks are located at
photocatalysts.
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- S. Ding, Y. Li, T. Sun et al. Environmental Advances 4 (2021) 100067
Fig. 6. (a) Photocurrent responses and (b) EIS of photocatalysts.
Fig. 5. (a) UV-Vis DRS and (b) PL spectra of photocatalysts.
much larger than that of the other three samples. The photograph in
Figure S1 also shows that PCN-U has the smallest bulk density. More-
over, the adsorption and desorption isotherms of all samples show the
27.3, 27.6, 27.5, 27.2 °, respectively. This may relate to the change in characteristics of type IV isotherm and H3 hysteresis loop in Fig. 4a
the stacking distance between the conjugated aromatic systems inside ((Yang, 2020); Wang, et al., 2018). This indicates that these photocata-
PCN (Aquino de Carvalho, et al., 2020). Overall, these PCN have no lysts have mesoporous pore structures and the pores may be caused by
obvious difference in crystal structure. slits. However, PCN-U shows its particularity in pore size distribution.
The chemical structures of photocatalysts were further analyzed by As shown in Fig. 4b, compared with the cases of the other three sam-
infrared spectroscopy. As shown in Fig. 2, the four samples have sim- ples, the average Barrett-Joyner-Halenda (BJH) pore size peak of PCN-
ilar FT-IR spectra. the broad absorption bands between 3000~3400 U is obviously moving in a larger direction. This indicates that a large
cm−1 are related to the N-H bond stretching vibration mode and the amount of released gas plays a significant role in expanding the pore
O-H bond breathing mode, which may be caused by the uncondensed size when urea is thermally polycondensed (Xu, et al., 2017). This phe-
amino groups and the H2 O molecules adsorbed on the surface of PCN nomenon is consistent with the results of FE-SEM. High specific surface
(Liu, et al., 2019). The multiple absorption peaks from 1200 to 1700 area (Cheng, et al., 2018) and relatively open pore structure can provide
cm−1 originate from the stretching vibration of C-N in the conjugated more accessible catalytic active sites, thereby improving the photocat-
aromatic system. The absorption peaks of 810 cm−1 correspond to the alytic antibacterial activity.
bending vibration mode of the triazine ring or heptazine ring (Qi, et al., The light absorption capacity of the photocatalysts were character-
2018). Infrared characterization results indicate that PCN prepared ized using UV-Vis DRS. As shown in Fig. 5a, all four photocatalysts have
from different precursors does not have significantly different functional visible light absorption, but the ranges of the optical absorption vary
groups. with the precursors. Specifically, the absorption edges of PCN-M and
The shape of photocatalysts was observed using FE-SEM. As shown PCN-D are both close to 490 nm. However, the absorption edge of PCN-
in Fig. 3, three samples of PCN-M, PCN-D and PCN-T are all piled up U is significantly blue-shifted to 476 nm, which may be attributed to its
with irregular blocks, while PCN-U is stacked with smaller and curled small size causing the quantum confinement effect. Meanwhile, PCN-T
sheet-like structures. Unlike the other three samples, PCN-U has a more shows an absorption edge of 500 nm, but it also has an additional ab-
open framework structure, which implies that its specific surface area sorption that can extend to 600 nm, which may be due to the presence of
may be larger. Nitrogen adsorption and desorption tests confirm this sulfur in the precursor that changes the band structure to some extent.
speculation. The Brunauer-Emmett-Teller (BET) specific surface areas These results are also consistent with the color difference of the samples
(SSABET ) of PCN-M, PCN-D, PCN-T and PCN-U are 13.7, 20.6, 13.3 and in Figure S1. Moreover, the bandgap energy (Eg ) of the photocatalysts
76.0 m2 g−1 , respectively. It is obvious that the SSABET of PCN-U is was converted from the Kubelka-Munk function. As shown Figure S2,
4
- S. Ding, Y. Li, T. Sun et al. Environmental Advances 4 (2021) 100067
Fig. 7. (a) Antibacterial activity of all photocatalysts
against E.coli under visible light irradiation and (b)
Photographs of untreated E.coli colonies and treated
with different photocatalysts for 2 h.
the Eg of PCN-M, PCN-D, PCN-T and PCN-U is 2.77, 2.76, 2.71 and 2.80 est, indicating that charge transfer is easier than the other three pho-
eV, respectively. The Mott-Schottky plots in Figure S3 show positive tocatalysts. The excellent photoelectrochemical performances of PCN-U
slopes, which indicates that all four photocatalysts have n-type semicon- may depend on its intrinsic structural properties and will play a positive
ductor characteristics. Therefore, the conduction band (CB) potential is role in its photocatalytic sterilization activity.
similar to the flat band potential (Li, et al., 2019; Wang, et al., 2018).
Combined with the Eg of the photocatalysts, the valence band (VB) po- 3.2. Antibacterial activity of photocatalyst
tentials of PCN-M, PCN-D, PCN-T, and PCN-U are about 1.52, 1.61, 1.66
and 1.72 eV, respectively. When the photogenerated holes are located in The photocatalytic antibacterial activity of the four photocatalysts
the high VB position, it means that these holes have stronger oxidation was evaluated by the survival rate of the common pathogenic bacteria
ability. Compared with other potocatalysts, the VB potential of PCN-U E.coli as a probe microorganism under visible light irradiation. To eval-
is the highest, which suggests that PCN-U may produce stronger ROS to uate whether the material and the light source itself have an effect on
kill bacteria during photocatalysis. The separation efficiency of photo- the survival rate of bacteria, dark control experiment was carried out
generated carriers of the four photocatalysts was explored by PL spec- without a light source and a light control experiment without a photo-
troscopy. In Fig. 5b, all photocatalysts show PL emission peaks of 460 catalyst. As shown in Fig. 7a, the survival rates of E. coli are close to
nm, which can be explained as the recombination of photogenerated 80 % in these two control experiments. The death of E. coli in these
electrons and holes. It is generally believed that the weaker PL emis- situations may be attributed to stress responses caused by light or in-
sion intensity means that the recombination is inhibited and the photo- organic materials (Zeng, et al., 2019; She, et al., 2019). Furthermore,
catalysis will be enhanced. Obviously, PL intensity of PCN-U among all the survival rates of E. coli have been substantially reduced during the
photocatalysts is the weakest, which strongly implies that PCN-U has photocatalysis. The survival rates of E. coli over PCN-M, PCN-D, PCN-T
strong photogenerated carrier separation efficiency (Sun, et al., 2020; and PCN-U after 2 h of light irradiation are 73.3, 63.5, 51.0 and 12.5
Yuan, et al., 2020). %, respectively. Undoubtedly, the photocatalysis effectively promotes
In order to further study the transfer behavior of photogenerated the killing of E. coli. The comparative photographs of the distribution
carries over the four photocatalysts under visible light irradiation, pho- of E. coli colonies before and after photocatalysis shown in Fig. 7b also
toelectrochemical tests were performed. As shown in the instantaneous intuitively reflect this effect. In addition, different photocatalysts also
photocurrent response spectra (Fig. 6a), the photocurrent average den- exhibit different bactericidal activity, PCN-U has the strongest bacteri-
sity of PCN-U is about 3, 2, and 1.5 times that of PCN-M, PCN-D and cidal ability under the same conditions. This sharp contrast shows that
PCN-T, respectively. It exhibits that the photoelectric conversion capa- different precursors lead to differences in the bactericidal performance
bility of PCN-U is significantly superior to other three photocatalysts. In of PCN. PCN prepared from different precursors has many differences
the electrochemical impedance spectra (EIS) of Fig. 6b, the sizes of the in morphology, specific surface area, pore size distribution, and opti-
arc radius reflect the different charge transfer resistance of the photocat- cal and photoelectrochemical properties. Experimental facts prove that
alysts. Among four photocatalysts, the arc radius of PCN-U is the small- the open porous structure composed of thin flake, strong photocatalytic
5
- S. Ding, Y. Li, T. Sun et al. Environmental Advances 4 (2021) 100067
Fig. 8. FESEM images of E. coli cells: (a)
untreated and (b) over PCN-U after 2 h of
light irradiation.
oxidation ability and good photoelectrochemical response performance Supplementary materials
synergistically promote the E. coli killing ability of PCN-U.
In order to further explore the effect of photocatalytic sterilization of Supplementary material associated with this article can be found, in
PCN-U, FE-SEM was used to visualize morphological changes of E. coli the online version, at doi:10.1016/j.envadv.2021.100067.
before and after photocatalysis. The E. coli cells without any treatment
exhibit a short rod-like morphology (Fig. 8a). However, as shown in
Fig. 8b, the rod-like cells have deformed and adhered after adding 0.7 References
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