Talanta 270 (2024) 125553
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Talanta
journal homepage: www.elsevier.com/locate/talanta
Rapid detection of Salmonella typhimurium by photonic PCR-LFIS dual
mode visualization
Jianxin Gao 1, Yuru Jiao 1, Jianhua Zhou **, Hongyan Zhang *
Shandong Provincial Key Laboratory of Animal Resistance Biology, Key Laboratory of Food Nutrition and Safety of Shandong Normal University, College of Life Science,
Shandong Normal University, Jinan, 250014, PR China
A R T I C L E I N F O
A B S T R A C T
Handling Editor: A Campiglia
Salmonella spp., as one of the foodborne pathogens, is a severe threat to global public health. Rapid screening of
salmonella spp. in contaminated food with low infective doses is the key to preventing food poisoning. In this
study, a fast visualization method for detecting Salmonella typhimurium (S. typhimurium) was developed based on
photonic PCR and AuNPs lateral-flow immunochromatography strip (LFIS). In addition, quantitative detection of
target bacteria could be achieved by utilizing the photothermal effect of AuNPs, and the sensitivity could be
improved by amplifying the photothermal signal. On the optimized conditions, the developed photonic PCR-LFIS
assay was highly sensitive, with a detection limit as low as 19 cfu mL− 1 of bacteria in pure culture after laser
irradiation, and highly specific, exhibiting no cross-reaction with Salmonella enteritidis, Listeria monocytogenes,
Escherichia coli, and Staphylococcus aureus. Notably, S. typhimurium could be detected in pork, egg white, and milk
without pre-treatment, with the recovery rates of the three samples between 81 % and 109 %. In conclusion, the
photonic PCR-LFIS assay realizes sensitive, simple, and rapid detection of S. typhimurium.
Keywords:
Salmonella typhimurium
Photonic PCR
Lateral-flow immunochromatography strips
Nucleic acid test
1. Introduction
Salmonella spp is a common zoonotic pathogen of the Enterobac­
teriaceae family, which is infected orally through contaminated food or
water [1–3]. Salmonella typhimurium (S. typhimurium) has substantial
toxicity and is one of the primary pathogens causing acute gastroen­
teritis [4]. It is widely distributed in nature and has strong survival
ability. It is easy to contaminate food and seriously threaten food safety
and human health [5]. Therefore, to accurately detect and effectively
control the contamination degree of S. typhimurium in food, it is
particularly urgent to develop a fast, accurate, sensitive, and reliable
detection method.
Detection methods for pathogenic bacteria are rapidly developing.
However, the most commonly used and reliable method is still nucleic
acid testing, and in the past few decades, PCR has become the gold
standard for detecting nucleic acid [6,7]. However, traditional PCR’s
limitations are becoming more and more prominent, such as the need to
undergo
a
long
thermal
cycle
process
like
denaturation-annealing-extension, relying on colossal equipment, and
difficulty used in grassroots and remote areas widely [8–10]. They have
been challenging to meet the urgent needs of some emergencies for rapid
on-site detection of microorganisms. It is imperative to resolve this
bottleneck problem to enable the widespread use of PCR detection
technology in food safety.
Son et al. proposed the concept of photonic PCR for the first time in
2015, mainly referring to the emerging PCR using photothermal mate­
rials to provide heat for PCR [11]. The temperature in the ultrafast
photon polymerase reaction process can be controlled by the intensity of
incident light or the nature and concentration of photothermal nano­
materials, reaching tens to hundreds of times the heating speed of
traditional PCR. Therefore, the whole amplification process can be
completed in a very short time [12,13]. In addition, the operation of
photonic PCR is simple and has broad application prospects in the field
of nucleic acid detection. From that time on, the photonic thermocycling
method based on the photothermal effects of specific nanomaterials [e.
g., gold nanoparticles (AuNPs), Aunanofilm, and titanium dioxide] has
attracted particular attention due to its noncontact energy conversion
[14–17]. Previous studies enhanced the plasmonic properties of the
nanomaterials by changing their size, shape, and other factors related to
localized surface plasmon resonance effect [18–20]. Although
* Corresponding author.
** Corresponding author.
E-mail addresses: zhoujh16@sdnu.edu.cn (J. Zhou), zhanghongyan@sdnu.edu.cn (H. Zhang).
1
The authors contributed equally.
https://doi.org/10.1016/j.talanta.2023.125553
Received 13 September 2023; Received in revised form 6 December 2023; Accepted 11 December 2023
Available online 15 December 2023
0039-9140/© 2023 Elsevier B.V. All rights reserved.
J. Gao et al.
Talanta 270 (2024) 125553
Fig. 1. Schematic diagram of rapid detection based on photonic PCR-LFIS. (A) Bacteria capture and photonic PCR, (B) Composition of immunofiltration strip, (C)
Positive results, (D) Negative results.
modification of nanoparticles effectively improves photothermal effi­
ciency, detecting reaction products is another challenge because it re­
quires a fluorescence spectrometer or other large equipment. Its
application to point-of-care testing (POCT) is limited [16,21,22].
In our previous work, the magnetic and photothermal effects of
Fe3O4 nanomaterials were used to enrich and isolate strains in complex
food substrates, carry out photonic PCR, and realize the detection of
pathogenic bacteria without pre-treatment [23]. However, the final
result still needs the help of a fluorescence spectrophotometer, which
needs better intuitiveness and relatively low sensitivity. Therefore, in
order to obtain the detection results of photonic PCR in a more intuitive,
sensitive, and effective manner, based on the successful construction of
photonic PCR, which was combined with lateral-flow immunochroma­
tographic strips (LFIS) to establish a visual detection method for
S. typhimurium in this study. The photothermal effect of AuNPs was used
to realize the quantitative detection of target bacteria, and the sensi­
tivity of the strip detection method could be improved through the
photothermal signal.
Table S1.
2.2. Photonic PCR
The photonic PCR reaction was performed as described in our pre­
vious work [23]. Under near-infrared laser irradiation, Fe3O4 magnetic
nanoparticles function as photothermal materials to facilitate the
completion of the PCR process. S. typhimurium genomic DNA was used as
a template. The PCR reaction mixture of this method was 12.5 μL of 2 ×
rapid Taq master mix, 1 μL each for primers, and then the total volume
was brought up to 25 μL with sterile ultrapure water. Finally, 3 μL
mineral oil was added to prevent the evaporation of water during pho­
tonic PCR [20,22]. The temperature changes were recorded using the
thermal sensor. The amplified products were diluted and then detected
by lateral chromatographic strips.
2.3. Optimization of coupling conditions between AuNPs and probe
AuNP particles with diameters of 15 ± 3 nm were prepared following
the methods described by Liu et al. with minor modifications [24].
Briefly, 1 mL of 1 % chloroauric acid was added to 100 mL of ultrapure
water and heated to boiling at 280 ◦ C. After boiling for 3 min, 3 mL of 1
% sodium citrate solution was added. The solution was then heated and
stirred evenly for 10 min. At this point, the solution appears as a clear
and bright wine-red color. The prepared AuNPs were characterized by
UV/visible absorption spectroscopy (UV-VIS) and Transmission Electron
Microscope (TEM).
In order to improve the antibody binding efficiency, AuNPs must be
concentrated 5 times. One mg⋅mL− 1 anti-digoxin antibody was slowly
added to the concentrated AuNPs solution (100 μL), incubated at room
temperature for 1 h by shaking, and then blocked at room temperature
2. Materials and methods
2.1. Bacterial strains and primers
A total of 2 Salmonella strains and 3 other bacterial strains were used
to determine the specificity of photonic PCR. Stock cultures were stored
at − 80 ◦ C in 0.8 mL of Luria-Bertani broth (Beijing Land Bridge Tech­
nology Co., Ltd., Beijing, China) and 0.2 mL of 80 % glycerol. The primer
pair SF: 5′-TCCGC AAAGG ATGAA GTTC- 3’ (2539–2557) and SR: 5′ACTCC TGGTG TTTCT CGATT- 3’ (2636–2617) was designed in the
present study to amplify a 116 bp sequence from the invasion protein A
gene (invA) of S. typhimurium. The bacterial strains used are listed in
2
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Talanta 270 (2024) 125553
Fig. 2. Characterization of AuNPs and AuNPs@Ab (A) Characterization of AuNPs and AuNPs@Ab by UV–Vis spectrum, (B) Zeta potential of AuNPs and AuNPs@Ab,
(C) TEM image of AuNPs, (D) TEM image of AuNPs@Ab.
for 1 h with 10 μL 6 % BSA. The AuNPs immune probe (AuNPs@Ab) was
obtained and stored at 4 ◦ C away from light.
and after irradiation. The test strip that did not contain S. typhimurium
was taken as the blank, and the temperature change ΔT0 before and after
laser irradiation of the test strip was calculated. Finally, the actual
temperature change value ΔT = ΔT1-ΔT0 generated by AuNPs was
calculated. The standard curve was established by using ΔT and the
concentration of bacteria to realize the quantitative detection of
S. typhimurium.
2.4. Assembly of paper-based lateral-flow strip
The lateral-flow strips consisted of plastic backing, an NC membrane,
a sample pad, and an absorption pad (Fig. 1B). To assemble the test strip,
streptavidin and goat anti-mouse antibodies were coated on the nitrate
cellulose membrane at 5 mm intervals using the film scribing instrument
as the test line (T line) and control line (C line), respectively. To
assemble the test strip, the NC membrane was placed in the center of the
plastic backing, and then the sample pad and the absorption pad were
placed on both sides, ensuring that they overlapped the NC membrane
by 1–2 mm. The assembled strips were dried at 37 ◦ C for 1 h, cut into a
width of about 4 mm, and stored in a sealed box containing desiccants at
4 ◦ C.
2.6. Detection of S. typhimurium in food samples
The pork (1 g), egg white (1 g) or milk (1 mL) was verified to be free
of S. typhimurium according to the National Standard GB 4789.4-2016
(People’s Republic of China, 2016), were purchased from a local su­
permarket, mixed with 9 mL of ultrapure water and homogenized well.
S. typhimurium solution cultured to logarithmic stage was harvested by
centrifugation at 6000 rpm for 10 min at 4 ◦ C [25]. The final pellet was
added to pork, egg white, or milk using 10-fold serial dilutions to ach­
ieve different concentrations: 102 cfu mL− 1, 104 cfu mL− 1 and 106 cfu
mL− 1. And then, S. typhimurium was captured using immune-Fe3O4
complexes in actual samples. The obtained liquid was used as the sub­
sequent photonic PCR assay template. Each food sample was tested 3
times.
2.5. Visual and photothermal detection of S. typhimurium
The AuNPs@Ab was mixed with PCR products and added to PBS to
achieve a total volume of 60 μL. The probe was incubated in a shaker for
10 min at room temperature and then added to the sample pad. After the
upward migration through the T and C lines, the color development of
the T and C lines was observed 10 min later, and the visual detection of
S. typhimurium was realized according to the color of the T lines.
The initial temperature T0 at the T line was recorded by the thermal
imager after the test strip was dried. Then, a laser with a wavelength of
532 nm illuminated the test line, and the temperature was recorded as T.
The temperature change at the test line ΔT1 = T-T0 is calculated before
2.7. Statistical analysis
Statistical analysis was performed using GraphPad Prism. Differ­
ences between groups were analyzed using Student’s t-test and one-way
analysis of variance (ANOVA). P value < 0.05 indicates a significant
difference, and the significant difference was indicated by *.
3
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Talanta 270 (2024) 125553
Fig. 3. Optimization of (A) photonic PCR product quantity, (B) coating concentration of streptavidin on the T-line, (C) laser irradiation time under different
S. typhimurium concentrations.
3. Results and discussion
3.3. Optimization of detection conditions
3.1. Operating principle of the photonic PCR-LFIS
In order to avoid excess antigens, it is necessary to optimize the
quantity of the photonic PCR products. The PCR product was diluted
10–70 times and added to the test strip. As shown in Fig. 3A, the color
rendering of the test strip was enhanced with the increase in the dilution
ratio of PCR products. The strip displayed satisfactory color reactions
when the dilution was 40 times. When diluted 10–30 times, it is pre­
sumed that the color weakness is caused by high antigen concentration
and severe interference with the PCR matrix. When diluted 60–70 times,
it is speculated that the color weakness is caused by low antigen con­
centration. Therefore, 40 times was selected as the optimal dilution of
PCR products.
Additionally, the coating concentration of streptavidin on the T-line
will directly affect the binding ratio of the gold-labelled protein, ulti­
mately affecting the color development of the test strip [27]. Therefore,
the coating concentration of streptavidin on the T-line is optimized. The
results in Fig. 3B demonstrated that with the increase of streptavidin
concentration, the color of the T-line on the membrane was gradually
enhanced. In contrast, the C-line’s color rendering was unaffected. When
the T-line concentration was 0.6 mg mL− 1 and 0.8 mg mL− 1, the T-line
color was weak, and false positives quickly appeared. When the T-line
concentration was 1 mg mL− 1, the T-line color rendering was signifi­
cantly enhanced, the sensitivity met the requirements, and the T-line
color rendering intensity did not change much compared with that when
the concentration was 1.2 mg mL− 1. So to obtain a test strip with stable
reactions and clear color development, 1 mg mL− 1 of streptavidin was
selected as the optimum concentration.
The photothermal properties of AuNPs can be used to amplify the
signal of detection, thus effectively improving the detection sensitivity,
and quantitative detection of S. typhimurium can be realized by calcu­
lating the temperature change after laser irradiation [28]. The temper­
ature of the T-line will continue to rise when the laser irradiates it.
However, when the lost and stimulated heat by the laser irradiation
reaches a dynamic balance, the temperature of the T-line will not
change. In addition, the length of irradiation time also affects the
detection sensitivity. When the irradiation time is too short, the T-line
temperature changes little, and the sensitivity is low. While the irradi­
ation time is too long, it will cause a waste of energy. Thus, optimizing
the laser irradiation time is necessary. The T-line was irradiated with a
532 nm laser, and the temperature change was recorded. As shown in
Fig. 3C, the T-line temperature continued to rise with laser irradiation.
When the laser irradiation time was about 20 s, the rate of temperature
The principle of the Photonic PCR-LFIS is illustrated in Fig. 1. Mag­
netic Fe3O4 nanoparticles functionalized with anti-S. typhimurium anti­
bodies were used to capture S. typhimurium from the food samples
selectively. The material’s magnetic properties were then used to
separate and enrich the target bacteria from the food matrix, thereby
eliminating the adverse effects of the complex food matrix on the
amplification of photonic PCR. The target DNA fragments labelled biotin
and digoxin were amplified by photonic PCR using the photothermal
effect of Fe3O4 nanoparticles. The PCR-amplified product was diluted 10
times with PBS (pH 8.0) and specifically captured to AuNPs@Ab by an
anti-digoxin antibody. The target DNA-AuNPs@Ab were dripped onto
the sample pad and flowed through the T line (coated with streptavidin)
and the C line (coated with goat anti-mouse antibody) by capillary
forces. The complex was captured by streptavidin immobilized on the
test line, which led to an increase in the number of target DNAAuNPs@Ab and the development of a visual band on the test line.
Excess AuNPs@Ab were captured on line C by anti-digoxin-goat antimouse antibody. As shown in Fig. 1B, in the presence of the target
bacteria, the AuNPs@Ab was fixed on the surface of the test strip based
on the sandwich-type reaction principle, and the color of the T-line and
C-line was displayed (positive). As shown in Fig. 1C, PCR was not
completed when there were no target bacteria, so only the C line showed
color (negative). Finally, visual and photothermal detection of
S. typhimurium were realized by observing the color of the T-line and
recording the temperature change before and after laser irradiation.
3.2. Characterization of AuNPs@Ab
Results of Fig. 2A showed that the peak of AuNPs@Ab was shifted
from 520 nm to 525 nm compared with AuNPs, which was evidence of
the conjugation between Au and antibodies [26]. Besides, the a Zeta
potential of AuNPs and AuNPs@Ab was measured by Zeta potential
analyzer. Compared with AuNPs, the Zeta potential of AuNPs@Ab was
significantly increased from − 50 mV to − 35 mV (Fig. 2B). The TEM
image in Fig. 2C showed that gold nanoparticles were spherical and
uniformly distributed at about 20 nm. Compared with AuNPs, there was
an extra layer of 1–2 nm film-like substance in the AuNPs@Ab (Fig. 2D).
These results indicated that antibodies were successfully adsorbed on
the surface of gold nanoparticles.
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Talanta 270 (2024) 125553
Fig. 4. (A) The photonic PCR-LFIS of different concentrations of S. typhimurium, (B) Photothermal detection of different concentrations of S. typhimurium, (C)
Specificity assessment of the photonic PCR-LFIS in the presence of different common bacteria, (D) Photothermal specificity of different common bacteria under laser
irradiation (****，P ≤ 0.0001), (E) Stability assessment of test strip at 4 ◦ C, (F) Stability assessment of test strip at 37 ◦ C.
rise became slower. Moreover, when the laser irradiation time reached
about 40 s, the T-line temperature peaked and remained unchanged.
Therefore, 30 s was chosen as the best laser irradiation time to obtain
higher sensitivity and save detection time.
With an excellent photothermal effect, AuNP molecules will be
excited and produce much heat under a 532 nm laser irradiation [29].
Therefore, the T-line region of the test strip was irradiated by laser with
a wavelength of 532 nm, and the quantitative detection of
S. typhimurium on the test strip was realized by photothermal detection.
As shown in Fig. 4B, the temperature of the T-line increased significantly
after irradiation. Moreover, ΔT (The temperature change before and
after laser irradiation) has an excellent linear relationship with bacterial
concentration. The regression equation between ΔT and bacterial con­
centration is obtained by establishing a standard curve: Y = 2.586X +
2.508, R2 = 0.9573. When the concentration of S. typhimurium is low, the
color change cannot be identified by the naked eye when the AuNPs test
strip method is used for visual detection. Still, the T-line has captured a
certain amount of DNA@Ab-AuNPs@Ab complex, which can be detec­
ted by the photothermal detection method. The detection limit of pho­
tothermal detection is about 19 cfu mL− 1, and the sensitivity is 10 times
3.4. Performance investigation of the photonic PCR-LFIS
Under the optimal conditions, S. typhimurium of 102,103, 104, 105,
10 and 107 cfu mL− 1 as templates, photonic PCR amplification was
performed according to Jiao et al. and sterile ultra-pure water as control
[23]. The photonic PCR product was diluted and mixed with the AuN­
Ps@Ab for incubation and then dropped onto the sample pad of the test
strip for visual detection. As shown in Fig. 4A, the color rendering ability
of the T-line was enhanced with the increase in bacterial concentration,
and it could still be observed by the naked eye when the bacterial
concentration was 102 cfu mL− 1.
6
5
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Talanta 270 (2024) 125553
Fig. 5. The analytical performance of photonic PCR lateral-flow immunochromatography strip for detection of S. typhimurium spiked in actual samples (A) Pork
samples, (B) Egg white samples, (C) Milk samples.
109 % (Table 1), and the coefficient of variation within the group is less
than or equal to 16.9 %, indicating that the established photonic PCRLFIS assay has a good application in the food sample detection.
Table 1
Spiked recoveries.
Food samples
Added
Lg (cfu⋅mL− 1)
Found
Lg (cfu⋅mL− 1)
Recoveries (%)
Pork
2.00
4.00
6.00
2.00
4.00
6.00
2.00
4.00
6.00
2.16
4.38
4.86
1.94
4.21
5.76
2.10
3.41
5.85
108 ± 11.2
109 ± 2.54
81 ± 6.40
97.2 ± 7.29
105 ± 2.28
96.0 ± 8.68
105 ± 17.7
85.4 ± 7.91
97.5 ± 3.58
Egg white
Milk
4. Conclusion
The photonic PCR was combined with LFIS to rapidly detect
S. typhimurium in this study, which uses inexpensive capillary action
based on an overlapping paper membrane system and offers rapid visual
detection results. Besides, the detection signal is amplified, and quan­
titative detection is realized by the photothermal properties of AuNPs.
Moreover, the detection limit of this detection method can reach 19 cfu
mL− 1. The method showed excellent specificity, and the recovery of
bacteria spiked in tagged samples was between 81 % and 109 %.
Compared with reported methods for Salmonella detection based on
nucleic acid amplification (Table S2), photonic PCR-LFIS is more un­
complicated sensitive, has a broader detection range, and avoids the
need for specialized personnel or expensive instruments. Without any
sample pretreatment or technical expertise, this sensor can rapidly test
complex food samples, such as pork, eggs, and milk. The combination of
photonic PCR and LFIS is thus a promising on-site detection technology
to monitor Salmonella.
higher than that of the visual method.
In order to evaluate the specificity of the PCR-LFIS assay under
optimal conditions, common food-borne pathogens such as Salmonella
enteritidis, Listeria monocytogenes, Escherichia coli, and Staphylococcus
aureus were detected by photonic PCR and observed using LFIS method.
To better show the specificity of the method, the concentration of
S. typhimurium was 105 cfu mL− 1, and the concentration of other bacteria
was 106 cfu mL− 1. As shown in Fig. 4C, when five bacteria were added to
the sample pad, clear bands appeared on the control line. However, only
the S. typhimurium strains showed visible bands on the test line. After
laser irradiation, the temperature of the T-line region for detecting
S. typhimurium was significantly different from that of the other four
groups (Fig. 4D). The results show that the photonic PCR-LFIS visual
detection method has reasonable specificity for detecting Salmonella
bacteria.
The storage stability of the test strip affects the quality of the test.
The main factor that caused the stability reduction of the test strip was
protein inactivation, which was mainly related to temperature [30], so
4 ◦ C and 37 ◦ C were chosen for investigation (Fig. 4E and F). The sta­
bility of test strips stored at 4 ◦ C for 0, 3, 7, 14, and 30 days and 37 ◦ C for
0, 1, 2, and 3 days was investigated. The final detection efficiency
decreased slightly due to the decrease of streptavidin activity during
storage and other factors. After 30 days of storage at 4 ◦ C, the final
detection efficiency was 84 % of the initial detection efficiency. After
being stored at 37 ◦ C for three days, the detection efficiency was 86 %.
The above results show that the test strip has good storage stability.
Credit author statement
Yuru Jiao: Data curation, Formal analysis, Investigation, Validation.
Jianhua Zhou: Formal analysis, Writing – review & editing. Jianxin Gao:
Conceptualization, Formal analysis, Methodology, Writing – original
draft. Hongyan Zhang: Funding acquisition, Methodology, Project
administration, Resources, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgments
3.5. Application to food samples
This study received financial support from a project of the National
Natural Science Foundation of China (grant number U22A20550, Key
Program) and the Natural Science Foundation of Shandong Province
(grant number ZR2020KC031, Key Program).
In order to investigate the feasibility of the photonic PCR-LFIS for
food samples, S. typhimurium with concentrations of 102 cfu mL− 1, 104
cfu mL− 1 and 106 cfu mL− 1 were added to pork, egg white, and milk
samples for spiked detection, as shown in Fig. 5. Due to the complexity
of the food sample matrix, the ions, lipids, proteins and pH value of the
matrix will affect the detection efficiency of S. typhimurium. It can be
seen that the recovery rates of the three samples are between 81 % and
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Talanta 270 (2024) 125553
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