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Photothermal Electrospun Nanofibers Containing Polydopamine-


Coated Halloysite Nanotubes as Antibacterial Air Filters
Oyku Demirel, Sarp Kolgesiz, Sena Yuce, Serap Hayat Soytaş, Derya Y. Koseoglu-Imer,
and Hayriye Unal*
Cite This: ACS Appl. Nano Mater. 2022, 5, 18127−18137 Read Online

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ABSTRACT: Antibacterial air filter media offer an important


solution to indoor air pollution from bioaerosols, which pose a
serious threat to global public health. In this study, we introduced an
Downloaded via SABANCI UNIV on March 9, 2023 at 17:38:19 (UTC).

antibacterial air filter based on nanofibers functionalized with a


photothermal agent, which deactivates bacteria upon near-infrared
(NIR) irradiation. Halloysite nanotube (HNT) clay nanoparticles
coated with polydopamine (PDA), which heat up when exposed to
NIR light, were utilized as photothermal agents to be incorporated
into polyacrylonitrile (PAN) nanofibers. The resulting PAN/HNT-
PDA nanofibers reached 102 °C after 2 min of NIR irradiation and
physically destroyed Staphylococcus aureus (S. aureus) cells that were
in contact with the nanofibers. In a simulated air filtration test
system, photothermal nanofibers demonstrated a bioaerosol
filtration efficiency of 99.97% and a quality factor of 0.14 Pa−1. 107S. aureus cells captured on the nanofibers were killed via a 10
min NIR-light irradiation, whereas the light-activated antibacterial properties of the nanofibers were maintained over 5 bioaerosol
flow/NIR-treatment cycles. The photothermal agent-containing electrospun nanofibers presented here have a strong potential for
aerosol removal as light-activated antibacterial air filters.
KEYWORDS: photothermal agents, nanofiber, air filter, bioaerosol removal, light-activated antibacterial activity

■ INTRODUCTION
Indoor air pollution caused by the deterioration of air quality
fact that the microorganisms captured on the filters remain
alive and the air filters become a secondary source of pollution
via aerosol particles is an important environmental problem constitutes an important problem. The high humidity in air
filtration systems, along with the organic/inorganic particles
that can have significant health consequences.1 One of the
retained on the filter media, create a suitable environment for
important sources of indoor air pollution is bioaerosols, which
the growth of microorganisms, which not only decreases the
are composed of bacteria, fungi, fungal spores, viruses, pollen,
filter efficiency but also poses the risk of pathogens being
and their airborne constituents.2,3 Bioaerosols are found in
reintroduced into the air.11 Therefore, there is a substantial
homes, schools, commercial and office buildings, and other
need for antimicrobial electrospun air filters that enable the
indoor common spaces where people spend the majority of
inactivation of captured bioaerosol particles.
their time, raising concerns for human health as they create a
Antibacterial properties have been imparted to air filters via
variety of diseases. Some of the diseases include sick building
the coating of antibacterial agents onto the surfaces of
syndrome, respiratory sensitization, and infectious diseases
nanofibers by dip coating, aerosol-based processes, or the
such as Legionnaires’ disease and Covid-19.4
integration of the antimicrobial agents into the electrospinning
Conventional air filters that are used to control indoor air
precursor solutions.12−14 Silver- and titanium-based nano-
quality by removing micron-sized airborne particles can
particles,15−17 carbon nanotubes,18 and natural plant ex-
capture larger bioaerosol particles and play a significant role
tracts19−21 have been incorporated into electrospun nanofibers,
in minimizing the consequences of indoor air pollution.5
However, their effect on the removal of submicron bioaerosol
particles is negligible.6 Air filter media prepared from Received: September 12, 2022
nanofibers, on the other hand, are excellent candidates for Accepted: November 11, 2022
the removal of fine bioaerosol particles due to their nanoscale Published: November 23, 2022
pore sizes, large surface-to-volume ratios, and excellent physical
properties.7−10 While the inherent advantages of electrospun
nanofibers allow efficient capture of bioaerosol particles, the
© 2022 The Authors. Published by
American Chemical Society https://doi.org/10.1021/acsanm.2c04026
18127 ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

resulting in antibacterial air filters. Bioaerosol particles that are deionized water to remove the residual dopamine. HNT-PDA
captured on the air filter medium are inactivated via the nanohybrids in powder form were dried at 70 °C for 24 h.
biochemical toxicity provided by the incorporated antibacterial The nanohybrids’ PDA content was determined by thermogravi-
agents. Antibacterial air filters, that can physically inactivate the metric analysis (TGA) [Shimadzu Corp. DTG-60H (TGA/DTA)].
TGA was carried out under nitrogen flow with a scan range of 30−
captured microorganisms, thus having a killing mechanism to 1000 °C and a heating rate of 10 °C/min. Calculations were done to
which pathogens cannot develop resistance, have not been determine the weight percent of PDA by comparing the weight loss of
reported. HNT and HNT-PDA nanohybrid between 30 and 1000 °C.
Incorporation of photothermal agents, which generate local The morphology of the HNT-PDA nanohybrids was evaluated
temperature elevations when irradiated with near infrared using the Zeiss LEO Supra 35VP scanning electron microscope
(NIR) light, has been demonstrated to result in antimicrobial (SEM). Images were collected at 3 kV using the secondary electron
materials and surfaces which can physically disrupt micro- detector after the samples were coated with Au−Pd.
organisms via light-activated heat generation.22−24 Composite The time−temperature profiles of the HNT-PDA nanohybrids
nanofibers comprising photothermal agents have also been were constructed to examine their photothermal properties. 0.5 g of
HNT-PDA nanohybrids in powder form was placed in a Teflon
shown to kill bacteria and viruses in membrane distillation,
holder under the infrared incandescent light bulb at 200 mW/cm2
cancer therapy, and biomedical applications,25−27 but their (Philips, Incandescent 230-250V BR125) light source, and temper-
utilization as antibacterial air filters was not demonstrated atures were recorded using a FLIR E6xt thermal camera. Measure-
before. ments were made on three different samples; mean and standard error
This study focused on the development of a photothermal values were reported.
agent containing antibacterial air filters which can kill retained Preparation of the PAN/HNT-PDA Nanofibers. The electro-
microorganisms by NIR-light activation. NIR-light irradiation spinning solutions consisted of PAN (7 wt % in DMF) and 10, 30,
activates the photothermal agents, resulting in a temperature and 50 wt % HNT-PDA nanohybrids. HNT-PDA nanohybrids were
increase at the nanofiber’s surface, which kills the bacteria via dispersed in DMF by ultrasonication for 20 min at 50% amplitude
hyperthermic effects. In our previous research, halloysite with a 5 s pulse on and a 2 s pulse off in an ice bath. Then, PAN was
added into the prepared dispersion and stirred with a magnetic bar at
nanotubes (HNT), which are hollow nontoxic28 tubular clay 500 rpm for 2 days at room temperature. In addition, an
nanoparticles widely utilized as functional green nanofillers in electrospinning solution composed of PAN (7 wt % in DMF) and
composites,29−31 were coated with photothermal polydop- 50 wt % neat HNTs was prepared to obtain PAN/HNT_50
amine (PDA), a sticky protein imitation found in mussels, to nanofibers.
create nontoxic clay-based photothermal nanohybrids (HNT- PAN/HNT-PDA nanofibers were produced utilizing an electro-
PDA) with strong light-to-heat conversion properties.32 Here, spinning system (Inovenso starter kit) that included a syringe pump, a
HNT-PDA nanohybrids were incorporated into polymeric vertical metal plate collector, and a DC voltage power supply. PAN/
electrospun nanofibers to obtain air filter membranes imparted HNT-PDA electrospinning solutions were transferred into a 5 mL
with photothermal properties, which heat up and kill bacteria syringe with a diameter of 13.10 mm, fitted with a stainless-steel
needle. The electrically grounded 15 × 15 cm metal plate wrapped
upon NIR light irradiation. The light-activated antibacterial with aluminum foil was placed 20 cm ahead of the needle tip. The
properties along with aerosol filtration properties of the applied voltage and the solution flow rate were set to 12 kV and 1
photothermal agent containing nanofibers were investigated. mL/h, respectively.
As the first example of antibacterial nanofibrous air filters, Characterization of the PAN/HNT-PDA Nanofibers. The
which can physically deactivate retained bacteria upon light- actual HNT and HNT-PDA content of the nanofibers were measured
stimulus, the membranes presented in this study have a strong by TGA (Shimadzu Corp. DTG-60H (TGA/DTA)). TGA was
potential to provide a solution to the problems associated with performed with a scan range of 30−1000 °C and a heating rate of 10
bioaerosol-based air pollution. °C/min under nitrogen flow. The weight-loss differences between
PAN nanofiber and PAN/HNT-PDA nanofiber at 30 to 1000 °C

■ EXPERIMENTAL SECTION
Chemicals. HNTs were purchased from Eczacıbaşı ESAN
were calculated to determine the weight percent of the HNT-PDA
nanohybrid in the nanofiber.
The surface morphology and diameter of nanofibers were evaluated
(Turkey). Dopamine (3-hydroxytyramine hydro-chloride) was using Zeiss LEO Supra 35VP SEM. Images were collected at 2 kV
provided by Acros Organics Inc. Ultrapure Tris base (Tris- using the secondary electron detector after the samples were coated
(hydroxymethyl)aminomethane) was purchased from MP Biomed- with Au−Pd. The diameter distribution diagrams of the fibers were
icals, LLC. Polyacrylonitrile (PAN) (Mw = 150 kDa) was provided by computed using the ImageJ application by measuring the fiber
Sigma-Aldrich. N,N-Dimethylformamide 99.8% was purchased from diameter at 100 different spots in the SEM images.
Sigma-Aldrich. Tryptic soy broth (TSB) and agar powder were The tensile strength, Young’s modulus, and elongation at break (%)
procured from Medimark (Italy). Deionized (DI) water was used in of the nanofibers were calculated using the TA-XT Plus Texture
all experiments. Staphylococcus aureus (S. aureus) (ATCC 29213) Analyzer (Stable Micro System, U.K.) equipped with a 50 kg load cell
bacteria were used for the antibacterial activity tests. The organic and Tensile Grips A/TG (Stable Micro System, U.K.). Nanofibers
model, aerosol bis(2-ethylhexyl) sebacate (DEHS) ≥ 97.0% (GC), with thicknesses in the range of 0.01−0.025 mm were cut into 20 mm
and the inorganic model, aerosol sodium chloride (NaCl), were × 50 mm dimensions. Before the experiment, the height and force
purchased from Sigma-Aldrich. calibration of the instrument was completed. The distance between
Preparation and Characterization of HNT-PDA Nano- the grips was set to 50 mm, the test speed was set to 0.5 mm/s and
hybrids. The preparation of HNT-PDA nanohybrids was described the breaking distance was set to 10 mm. For each nanofiber, 5
in our prior work in detail.33 Briefly, neat HNTs were dispersed in different samples were prepared and tested. The statistical analysis of
deionized water at a concentration of 10 mg/mL by ultrasonication the data was completed with one-way ANOVA (Tukey) analysis
(QSonica, Q700, Newtown, CT, USA) at 50% amplitude with a 5 s (Origin Lab Corporation, USA) at p < 0.05.
pulse on and a 2 s pulse off in an ice bath for 20 min. Dopamine was Photothermal Properties of the PAN/HNT-PDA Nanofibers.
added to the HNT dispersion at a concentration of 8 mg/mL. The The time-temperature profiles of the nanofibers were constructed to
pH of the dispersion was adjusted to 8.5 by adding the Tris base, and examine their photothermal properties. The nanofiber was cut into 1
the dispersion was continuously stirred for 24 h at 30 °C. The × 1 cm dimensions and placed in a Teflon holder under the selected
dispersion was centrifuged at 11,000 rpm and washed six times with light source, and temperatures were recorded using a FLIR E6xt

18128 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

Figure 1. (a) Schematic representation of the HNT-PDA synthesis and SEM images of neat HNTs and HNT-PDA nanohybrids, (b) TGA of
HNTs and HNT-PDA nanohybrids, and (c) time-temperature profiles of neat HNTs and HNT-PDA nanohybrids under irradiation from an
infrared incandescent lamp at 200 mW/cm2 light density.

thermal camera. The following light sources and light densities were activated antibacterial properties of the nanofibers, one sample was
utilized: (i) an 808 nm laser module (STEMINC, SMM22808E1200) treated with NIR light for varying periods of time (2, 5, 10 min), while
(Doral, FL USA) at 800 mW/cm2, (ii) an infrared incandescent light the control sample was kept in the dark for the same amount of time.
bulb at 100 mW/cm2 (Philips, Incandescent 230-250V BR125), (iii) Bacteria on the nanofiber samples were transferred into 1 mL of Tris
an infrared incandescent light bulb at 200 mW/cm2 (Philips, buffer by vortexing for 2 min. Bacterial suspensions were serially
Incandescent 230-250V BR125) (iv) a solar simulator (Oriel LCS- diluted, plated on TSB agar plates, and incubated at 37 °C for 24 h.
100) at 1 sun (100 mW/cm2), and (v) a solar simulator (Oriel LCS- Colony counting was performed, and the viability of S. aureus on the
100) at 2 sun (200 mW/cm2). Time-temperature profiles were nanofiber samples before and after NIR light-treatment was reported
constructed with data obtained from three different spots on each as log10 CFU/mL. Mean and standard error values from three
nanofiber; mean and standard error values were reported. different experiments were reported.
Light-Activated Antibacterial Properties of the PAN/HNT- Air Filtration Properties of the PAN/HNT-PDA Nanofibers.
PDA Nanofibers. S. aureus (ATCC 29213) cells were cultured in 3 The filtration performance tests were carried out using a custom-
mL of TSB growth medium for 24 h at 37 °C in an incubator with made, continuous flow air filtration test system constructed with an
shaking at 200 rpm. The bacteria that had grown were centrifuged, aerosol generator (TSI Six-Jet Atomizer 9306), a diffusion dryer (TSI
washed twice with sterile Tris buffer (pH 7.5) and resuspended at a 3062-NC), an optical particle sizer (OPS) (TSI 3330), a differential
concentration of 108 CFU/mL in Tris buffer. 1 × 1 cm nanofibers pressure gauge, and a custom-made stainless-steel filter module with a
were cut and placed in wells of Teflon molds with a radius of 1 cm quartz top onto which the nanofiber membranes of 10 cm diameter
and a height of 0.5 cm. The nanofiber surface has been completely can be inserted. An aqueous neutralized monodisperse NaCl solution
covered with 100 μL of the bacterial suspension. To ensure that the at 1 g/L concentration and DEHS solution in distilled water at 0.5 g/
bacteria were not killed by the light alone, the same amount of the L concentration were loaded into the aerosol generator that is
bacterial suspension was added to an empty well as a control. connected to a compressed air line at 10 psi. Generated aerosol passed
Additionally, PAN/HNT_50 composite nanofibers were utilized as a through the diffusion dryer and entered the filter module at an air flow
control to demonstrate that PDA-induced light-to-heat conversion rate of 0.5 L/min and a velocity of 0.02 m/s. Particle quantities
basically caused the physical death of the bacteria. For each of the downstream and upstream of the filter were determined with the OPS
nanofibers, two samples were prepared. To examine the NIR light- after operating the system for 50 min.

18129 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

Figure 2. (a) Preparation of the PAN/HNT-PDA nanofibers; (b) visual appearance of the PAN and PAN/HNT-PDA_50 nanofibers.

Filtration efficiency (η, %) and quality factor (QF) were calculated were not reacted with dopamine monomer indicated that the
with eqs 1 and 2, respectively, by determining the differential pressure HNT-PDA nanohybrids contained 8 wt % PDA (Figure 1b).
(ΔP) at the inlet and outlet of the filter module and measuring the The time-temperature profile of the HNT-PDA nanohybrids
total number of particles both inlet (Cin) and outlet (Cout) using the
OPS.
under irradiation from an NIR lamp revealed that the
nanohybrids can be heated to 212 °C under 2 min irradiation,
Cout whereas the neat HNTs did not heat up under the same
(%) = 1
Cin (1) conditions (Figure 1c). The PDA coating on the HNTs
introduced photothermal properties and allowed them to be
ln(1 ) used as natural, nontoxic, low-cost additives, that can impart
QF (kPa 1) =
P (2) light-to-heat conversion properties to nanofibers.
Bioaerosol Removal and Antibacterial Properties of the HNT-PDA integrated PAN nanofibers were produced by
PAN/HNT-PDA Nanofibers. The bioaerosol removal and anti- the electrospinning method (Figure 2a). The weight ratio of
bacterial properties of the nanofibers were investigated via the the PAN and the HNT-PDA was varied to determine the
following procedure: S. aureus cells were cultured in 3 mL of TSB
optimum formulation that allows nanofiber formation with a
growth medium for 24 h at 37 °C with shaking at 200 rpm, washed
twice with sterile Tris buffer (pH 7.5) and resuspended in Tris buffer uniform HNT-PDA distribution and the highest NIR-light-
at a concentration of 108 CFU/mL. The prepared bacterial induced temperature elevations. By dispersing HNT-PDA
suspension was diluted in 50 mL of deionized water to generate a nanohybrids in DMF and mixing them with PAN in various
bacterial suspension at a concentration of 2.0 × 108 CFU/mL, which proportions, an electrospinning solution with the required
was transferred into the chamber of the aerosol generator. After the viscosity for electrospinning was obtained. The electrospinning
nanofiber was placed in the filter module, the system parameters were solution did not present any phase separations and
set to a flow rate of 0.5 L/min and a velocity of 0.02 m/s. After the
precipitations, demonstrating appropriate compatibility be-
system was operated for 50 min, the nanofiber sample on the filter
module was irradiated with the near-infrared incandescent light bulb tween PAN and HNT-PDA nanohybrids. Electrospinning of
at 200 mW/cm2 via the quartz top of the filter module for 0, 2, 4, and the dispersion resulted in a gray-colored nanofiber mat,
10 min. Light-treated nanofiber filters were aseptically removed from confirming the successful incorporation of the black-colored
the filtration module and placed in 10 mL of Tris to transfer the HNT-PDA nanoparticles, whereas the control PAN nanofiber
bacteria retained on the air filters into the buffer. After vortexing for 2 was white-cream in color (Figure 2b).
min, bacterial suspensions were serially diluted and plated on TSB The presence of the HNT-PDA nanohybrids in the
agar plates. Plates were incubated at 37 °C for 24 h. Colony counting nanofiber mat was further verified using TGA (Figure S1
was performed, and the viability was expressed as log10 CFU/mL.
To investigate the reusability of the nanofibers, nanofiber samples and Table 1). The decomposition onset temperature (Tonset) of
were exposed to S. aureus aerosols in the filtration system as detailed the PAN nanofiber was shifted to lower temperatures when 50
above for 50 min and irradiated with NIR light for 10 min. This cycle
was repeated three times without replacing the nanofiber sample. Table 1. Thermal Properties of the PAN/HNT-PDA
Following the three-aerosol exposure/irradiation cycles, the nanofiber Nanofibers; the HNT-PDA Content of the Nanofibers
sample was aseptically removed, and the viability of the bacteria on Calculated from the % Char at 1000 °C Values
the filter was determined with the procedure explained above.

■ RESULTS AND DISCUSSION


HNT-PDA nanohybrids were utilized as the photothermal sample name
Tonset
(°C)
% char at
1000 °C
HNT-
PDAtheoretical
(wt %)
HNT-
PDAexperimental
(%)
agents to be incorporated into nanofibers.33 Oxidative PAN 292 2.0
polymerization of dopamine in the presence of HNT PAN/HNT_50 276 38.7 50 50.6
substrates resulted in PDA-coated clay nanoparticles, which PAN/HNT-PDA_10 284 12.2 10 15.9
preserved their nanotubular structure (Figure 1a). TGA of the PAN/HNT-PDA_30 300 29.1 30 38.0
HNT-PDA nanohybrids in comparison to neat HNTs, that PAN/HNT-PDA_50 332 43.0 50 56.2

18130 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

Figure 3. SEM images at 5k (top raw) and 50k (middle raw) magnification and nanofiber diameter distributions (bottom row) of PAN (a), PAN/
HNT-PDA_10 (b), PAN/HNT-PDA_30 (c), and PAN/HNT-PDA_50 (d) nanofibers.

wt % neat HNTs were incorporated, demonstrating a observed. These structures potentially consisted of nano-
destabilizing effect, potentially due to the aggregation of hybrids that were not completely dispersed in the electro-
HNTs at high concentrations. On the other hand, when HNT- spinning solution and remained agglomerated, resulting in
PDA nanohybrids were incorporated into PAN at the same expanded fibers when present. Bead formation was observed in
concentration, the PAN/HNT-PDA nanofibers presented nanofibers with an HNT-PDA content greater than 30 wt %.
decomposition temperatures 40 °C higher than those from The type of anionic or cationic agents integrated into the
the PAN nanofibers, indicating improved thermal stability in electrospinning solution has been shown to have a
PAN/HNT-PDA composite nanofibers. The carbonization of considerable impact on the properties of the solution.34 The
the PDA on the HNT-PDA nanohybrids starting at 220 °C has difference in the electrical conductivity of the polymer and the
potentially created a synergistic effect with PAN, which HNT-PDA nanohybrids might have caused the bead
resulted in more stable PAN/HNT-PDA nanofibers. As the formation. Studies in the literature have proven that bead
control PAN nanofiber was entirely decomposed at 1000 °C, formation in nanofibers has a positive effect on efficiency and
the remaining weight of the PAN/HNT-PDA nanofibers at low airflow resistance in air filters.35,36 Bead-on-string
this temperature allowed us to determine the amount of the structures for use in the production of PAN nanofiber air
HNT-PDA nanohybrids integrated into the nanofibers. The filters have been attempted and were shown to be effective at
experimental HNT-PDA nanohybrid content of the nanofibers holding onto ultra-fine particulate matter.37 Thus, the PAN/
were calculated by dividing the % char at 1000 °C of the HNT-PDA nanofibers with the higher HNT-PDA photo-
nanofiber by the weight loss of the PAN nanofiber and the thermal agent content can be effectively utilized as air filters.
weight loss of HNT-PDA nanohybrids at the same temper- When the size distributions of nanofibers containing the
ature and are given in Table 1. The fact that the total weight HNT-PDA photothermal agents were analyzed, it has been
loss of the composite nanofibers decreased proportionally to seen that the nanofiber diameters varied in the range of 200−
the amount of the theoretically integrated HNT-PDA 250 nm, whereas the diameter distributions of neat PAN
nanohybrids proved that the HNT-PDA nanohybrids were nanofibers were mainly observed between 200 and 500 nm.
successfully integrated into the nanofibers. Furthermore, the The addition of HNT-PDA nanoparticles likely changes the
experimental HNT-PDA nanohybrid content largely coincided properties of the electrospinning solution, promoting better
with the theoretical HNT-PDA nanohybrid content, which charge distribution and resulting in thinner fibers. Similarly, the
emphasizes that the PAN and HNT-PDA nanohybrids were reduction in the fiber diameter with the addition of PDA
compatible and that all HNT-PDA nanohybrids present in the nanoparticles has been previously reported in the production
electrospinning solution were integrated into the composite of electrospun polycaprolactone fibers.38 The fiber diameter
nanofibers. distributions obtained from PAN/HNT-PDA nanofibers are
The images acquired from the SEM analysis of the PAN/ similar to other PAN air filter studies.39−41 In general, a
HNT-PDA fiber mats demonstrated that the nanofiber reduction in fiber diameter leads to a reduction in the overall
formation was successful (Figure 3). As the amount of the pore size distribution of the nanofiber, which increases the
HNT-PDA nanohybrids integrated into the nanofiber uptake of small diameter particles, especially in air filtration
increased, agglomerated fragments and bead structures were applications.42
18131 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

Figure 4. SEM images of PAN/HNT-PDA (a,b) and PAN (c) nanofibers.

The distribution of the HNTs in the nanofibers was also agglomeration of the HNT-PDA nanohybrids, which created
investigated with SEM at higher magnifications (Figure 4). local small vacancies on the fiber matrix, directly affecting the
While PAN nanofibers presented fine, uniform nanostructures, mechanical properties. Overall, the presence of the HNT-PDA
the HNT-PDA nanohybrids were easily visible within the nanohybrids inside the nanofibers improved the mechanical
PAN/HNT-PDA nanofibers, either as individually oriented properties because of the high aspect ratio of the nanohybrids
along the flow direction of the nanofibers or within aggregated and their nucleating effect on the nanofibers, and durable
structures incorporated into the nanofibers. composite nanofibers that are suitable for air filter applications
The mechanical properties of the composite nanofibers in were obtained.
comparison to neat PAN nanofibers were demonstrated in The light-activated heating properties of the composite
Figures 5 and S2. The elongation at break and the tensile nanofibers and whether they can be heated to temperatures
that can disrupt bacteria under NIR-light irradiation were
studied. The time-temperature profiles of HNT-PDA contain-
ing nanofibers were constructed by monitoring the NIR lamp
irradiation-triggered temperature elevations. As shown in
Figure 6, the irradiation of the neat PAN and PAN/HNT

Figure 6. Time-temperature profiles of PAN, PAN/HNT, and PAN/


HNT-PDA nanofibers with varying HNT-PDA content under NIR
irradiation from an incandescent light bulb at 200 mW/cm2 light
density.

nanofibers under the NIR light source did not cause any
temperature elevations in 2 min, whereas the HNT-PDA-
containing nanofibers were heated significantly under the same
conditions due to the photothermal character of the HNT-
Figure 5. Mechanical properties of PAN and PAN/HNT-PDA PDA nanohybrids. The degree of light-triggered temperature
nanofibers. (a) Elongation at break, (b) tensile strength, and (c) elevations was observed to be in direct proportion to the
Young’s modulus. HNT-PDA photothermal agent loading rates of the composite
nanofibers. The temperature of PAN/HNT-PDA_50 nano-
strength of the composite nanofibers were slightly improved fibers with the highest content of photothermal agents by
compared to neat PAN nanofibers. However, the Young’s weight reached 102 °C when irradiated with a NIR lamp for 2
modulus of the samples did not significantly change at min. Thus, it has been shown that the photothermal effect of
increasing HNT-PDA concentrations inside the nanofibers. the HNT-PDA nanohybrids was transferred to the composite
While the tensile strength of the nanofibers increased at 10 and nanofibers and that the degree of the light-triggered heating of
30 wt % HNT-PDA content, it did not further increase above the nanofibers can be adjusted by changing the amount of the
30 wt % HNT-PDA content, potentially due to the integrated photothermal agent. The temperature elevations
18132 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

Figure 7. (a) Schematic representation of the in vitro antibacterial tests, (b) viability of S. aureus suspension on PAN and PAN/HNT-PDA_50
nanofibers after 0, 2, 4, and 10 min NIR irradiation at 200 mW/cm2 light density.

Table 2. Air Filtration Performance of PAN, PAN/HNT_50, and PAN/HNT-PDA_50 Nanofibers


sample Name inner particle number (#/cm3) outer particle number (#/cm3) η (%) ΔP (Pa) QF (Pa−1)
inorganic aerosol (NaCl) PAN 3745 0.053 99.9976 10 1.06
PAN/HNT_50 3625 0.037 99.9990 60 0.19
PAN/HNT-PDA_50 3450 0.042 99.9988 60 0.19
organic aerosol (DEHS) PAN 2452 0.012 99.9995 10 1.22
PAN/HNT_50 2832 0.030 99.9989 60 0.19
PAN/HNT-PDA_50 2620 0.036 99.9986 50 0.22
bacterial aerosol (S. aureus) PAN 3400 3.46 99.8981 10 0.69
PAN/HNT_50 3798 1.96 99.9484 60 0.13
PAN/HNT-PDA_50 3866 1.05 99.9729 60 0.14

caused by the irradiation of nanofibers under different light HNT-PDA nanofibers and kept in the dark for the same period
sources, including a NIR laser module and a solar simulator of time as the irradiated nanofibers remained alive, which
were also investigated, and it was demonstrated that the PAN/ implied that there is no eradication of bacteria by environ-
HNT-PDA nanofibers can be remotely heated by NIR mental factors and that PAN/HNT-PDA nanofibers do not
irradiation at different light densities (Figure S3). have any antibacterial activity in the absence of NIR light.
The utilization of the PAN/HNT-PDA composite nano- Consequently, PAN/HNT-PDA composite nanofibers were
fibers present unique light-to-heat conversion properties as shown to have remarkable light-activated antibacterial proper-
membranes that can kill bacteria via light-activated heating was ties in in vitro testing and strong potential for use as air filter
investigated. The nanofibers with the highest amount of membranes that can be purified from microorganisms by NIR
photothermal agent (PAN/HNT-PDA_50), which was shown irradiation.
to present the highest light-activated temperature elevations The aerosol filtration performance of the PAN/HNT-
was tested in terms of its antibacterial properties. The viability PDA_50 nanofibers was studied in comparison to neat PAN
of an aqueous suspension of S. aureus dropped on the PAN/
nanofibers to determine the effect of the HNT-PDA
HNT-PDA_50 nanofibers was examined after NIR irradiation
nanohybrids on the air filtration properties. The aerosol
of the nanofiber mat for different durations (Figure 7).
filtration performance of the nanofibers was tested using the
Irradiation of the neat PAN nanofibers that did not contain the
photothermal HNT-PDA nanohybrids resulted in insignificant filtration test system schematized in Figure S4. Aerosols of
bacterial fatalities that are independent of the irradiation neutralized monodisperse NaCl, DEHS, and S. aureus bacteria
duration. On the other hand, the number of viable S. aureus were utilized as models that simulate inorganic, organic, and
dropped on the PAN/HNT-PDA_50 decreased significantly bio aerosols in the indoor air, respectively.
with increasing NIR-irradiation times, and all of the The filtration performance of the PAN/HNT-PDA_50
approximately 108 bacteria were killed when the composite nanofibers, which presented strong light-to-heat conversion
nanofibers were exposed to irradiation for 10 min. The fact properties and excellent light-activated bacteria-killing poten-
that suspensions of S. aureus that were exposed to the same tial was investigated in the air filtration test system. Filtration
irradiation conditions did not present any killing confirmed efficiency, pressure drop, and quality factor values for the neat
that the bacteria were killed by light-activated heating of the PAN, PAN/HNT_50, and PAN/HNT-PDA_50 nanofibers
HNT-PDA photothermal agents in the nanofibers and not obtained after inorganic (NaCl) and organic (DEHS) aerosol
directly by light. Similarly, bacteria dropped on the PAN/ flow for 50 min are tabulated in Table 2.
18133 https://doi.org/10.1021/acsanm.2c04026
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ACS Applied Nano Materials www.acsanm.org Article

Figure 8. (a) Schematic illustration of the light-activated deactivation of the bioaerosol particles captured on the air filter membrane, (b) viability of
S. aureus particles on PAN, PAN/HNT, and PAN/HNT-PDA composite nanofibers after 0, 4, and 10 min irradiation with an NIR lamp at 200
mW/cm2. (c) Viability of S. aureus captured on the PAN/HNT-PDA_50 nanofiber after multiple bioaerosol flow/NIR-irradiation cycles.

The pressure drop (ΔP) of the PAN/HNT-PDA_50 demonstrated to have superior aerosol filtration capabilities
nanofiber filters under different aerosol flows was observed and achieved high QFs.
to be slightly higher than the ΔP of the neat PAN nanofibers The aerosol filtration test setup was also utilized to assess
due to the HNT-PDA photothermal agents integrated into the the efficiency of the PAN/HNT-PDA composite nanofibers as
fiber, but the ΔP values of the composite nanofibers were antibacterial air filters, which can deactivate the bioaerosol
below 60 Pa. The quality factor (QF) is also a standard particles trapped on the membrane upon NIR irradiation. The
parameter for assessing air filter performance.43,44 While QF light-activated antibacterial activity of the nanofibers was
values of the PAN/HNT-PDA nanofibers slightly decreased examined by exposing them to a 50 min of S. aureus aerosol
relative to the QF values for the neat PAN nanofiber under flow followed by NIR irradiation for various periods of time
organic, inorganic, and bio aerosol flow, the nanocomposite and determining the viability of the captured bacteria (Figure
nanofibers containing the HNT-PDA photothermal agents 8a). When the PAN and PAN/HNT_50 nanofibers were
presented acceptable QF values ranging between 0.14 and 0.69 exposed to NIR light, approximately 107 bacteria captured on
Pa−1. Despite having lower QF values than the PAN nanofiber, the nanofibers remained alive; independent of the duration of
the bead-on-string PAN/HNT-PDA_50 nanofibers still had the irradiation; no significant killing activity was observed. On
competitive QF values. For both PAN and PAN/HNT- the other hand, when the PAN/HNT-PDA_10, PAN/HNT-
PDA_50 nanofibers, the filtration efficiency was above 99.97%. PDA_30, and PAN/HNT-PDA_50 nanofibers with approx-
PAN/HNT nanofibers presented similar air filtration perform- imately the same number of bacteria on the surface were
ance as the PAN/HNT-PDA nanofibers, demonstrating that exposed to NIR light, significant killing activity was observed
the PDA coating on the HNTs did not affect the air filtration (Figure 8b). On the PAN/HNT-PDA_50 air filters, a 5 log
properties. SEM images of the PAN and PAN/HNT-PDA_50 reduction in the number of viable bacteria was observed after 4
nanofibers obtained after 50 min of NaCl and DEHS aerosol min of irradiation with NIR light. Irradiation of the same
flow have also clearly visualized the filtration performance of nanofiber for 10 min resulted in killing of all bacteria. In light
the air filters, showing particles captured on the surface and of the comparison between PAN/HNT_50 and PAN/HNT-
within the pores of the nanofibers (Figure S5). As a result, the PDA_50 composite nanofibers, the results indicated that the
composite nanofibers and PAN nanofibers developed were presence of the photothermal PDA coating on the HNTs
18134 https://doi.org/10.1021/acsanm.2c04026
ACS Appl. Nano Mater. 2022, 5, 18127−18137
ACS Applied Nano Materials www.acsanm.org Article

caused the killing of bacteria. The antibacterial properties of


PAN/HNT-PDA_50 nanofiber, which were proven in an in

*
ASSOCIATED CONTENT
sı Supporting Information
vitro test, were also confirmed in an aerosol filtration system, The Supporting Information is available free of charge at
where bioaerosol particles captured on the nanofiber were https://pubs.acs.org/doi/10.1021/acsanm.2c04026.
entirely deactivated remotely with NIR irradiation.
Bacteria attached to the PAN/HNT-PDA nanofiber surface Stress−strain curves of PAN and PAN/HNT-PDA
after being exposed to bioaerosol flow for 50 min were nanofibers, time−temperature profiles of PAN, PAN/
visualized before and after NIR irradiation of the nanofibers. HNT, and PAN/HNT-PDA nanofibers with varying
SEM images in Figure S6 clearly demonstrate that bacteria photothermal agent contents under different light
were entrapped on the nanofiber surface following the sources, and SEM images of PAN and PAN/HNT-
bioaerosol flow exposure. The bacteria attached to the PDA_50 composite nanofibers exposed to 50 min NaCl
nonirradiated nanofiber surface appeared to retain their and DEHS aerosol flow (PDF)
spherical shape and to be alive, whereas the majority of
bacteria on the irradiated PAN/HNT-PDA_50 surface
appeared to be dead, as evidenced by their radically disrupted
■ AUTHOR INFORMATION
Corresponding Author
morphology; thus, the lethal activity of the PAN/HNT- Hayriye Unal − SUNUM Nanotechnology Research Center,
PDA_50 nanofibers on S. aureus was observable. Sabanci University, Istanbul 34956, Turkey; orcid.org/
In terms of environmental damage and financial expenditure, 0000-0002-9090-2440; Email: hunal@sabanciuniv.edu
the reusability and sustainability of antibacterial air filters are
crucial. To investigate their reusability after NIR light Authors
treatment, the PAN/HNT-PDA_50 nanofibers were irradiated Oyku Demirel − Faculty of Engineering and Natural Sciences,
for 10 min after being exposed to bacterial aerosol for 50 min Sabanci University, Istanbul 34956, Turkey; SUNUM
in the aerosol filtration test system, and this procedure was Nanotechnology Research Center, Sabanci University,
repeated five times under the same conditions. Finally, the Istanbul 34956, Turkey
viability of bacteria before and after 5 aerosol flow/irradiation Sarp Kolgesiz − Faculty of Engineering and Natural Sciences,
cycles was evaluated. Figure 8c demonstrates that the killing Sabanci University, Istanbul 34956, Turkey; SUNUM
activity of the PAN/HNT-PDA nanofibers remained the same Nanotechnology Research Center, Sabanci University,
and that the nanofiber filter was able to deactivate all captured Istanbul 34956, Turkey
bacteria even after 5 cycles. This result demonstrated that the Sena Yuce − Faculty of Engineering and Natural Sciences,
composite nanofibers were stable, so that they could reach the Sabanci University, Istanbul 34956, Turkey; SUNUM
same temperature required to deactivate the bacteria after Nanotechnology Research Center, Sabanci University,
multiple cycles of light exposure and are suitable for reuse. Istanbul 34956, Turkey
Serap Hayat Soytaş − SUNUM Nanotechnology Research

■ CONCLUSIONS
The HNT-PDA photothermal agents, which were prepared by
Center, Sabanci University, Istanbul 34956, Turkey;
orcid.org/0000-0002-2114-8923
Derya Y. Koseoglu-Imer − Department of Environmental
coating the natural clay nanoparticles with PDA, have been Engineering, Istanbul Technical University, Maslak Campus,
integrated into electrospun nanofibers, resulting in antibacterial Istanbul 34467, Turkey
composite nanofiber mats that kill S. aureus bacteria via NIR Complete contact information is available at:
irradiation. The amount of the photothermal agent contained https://pubs.acs.org/10.1021/acsanm.2c04026
in the nanofibers proportionally increased the temperature
reached by the nanofibers upon NIR irradiation. The Author Contributions
temperature of the PAN/HNT-PDA nanofibers was observed The manuscript was written through the contributions of all
to rise above 100 °C in nearly 2 min. The integration of HNT- authors. All authors have given approval to the final version of
PDA photothermal agents did not adversely impact the aerosol the manuscript.
filtration properties of the composite nanofibers, but imparted Notes
light-activated antibacterial properties, which allowed deacti- The authors declare no competing financial interest.
vation of the bacteria captured by the nanofibers by light
activation. Even after being exposed to NIR light multiple
times, they exhibited reusability by reaching the same
temperature and deactivating the bacteria. To the best of our
■ ACKNOWLEDGMENTS
This work was supported by the Scientific and Technological
knowledge, the PAN/HNT-PDA nanofibers presented here Research Council of Turkey (TUBITAK) under the project
are the first examples of a photothermal air filter, which could number 119Y131.
provide a new dimension to the air filtration application field.
By utilizing the heat produced by a widely obtainable light
source, bacteria such as S. aureus, which are important
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