Sensors MDPI

1
1 Type of the Paper (Review)
2 Emerging Applications of Nanobiosensors in Pathogen

3 Detection in Water and Food
4 Hiram Martin Valenzuela-Amaro† 1,2, Alberto Aguayo-Acosta † 1,2, Edgar Ricardo Meléndez-Sánchez 1,2, Orlando de
5 la Rosa 1,2, Perla Guadalupe Vázquez-Ortega3, Mariel Araceli Oyervides-Muñoz1,2, Juan Eduardo Sosa-Hernández1, 2
6 * Roberto Parra-Saldivar1,2*
7 1
Tecnologico de Monterrey, Institute of Advanced Materials for Sustainable Manufacturing, Monterrey, 64849,
8 Mexico
9 2
Tecnologico de Monterrey, School of Engineering and Sciences, Monterrey, 64849, Mexico
10 3
Tecnologico Nacional de México/Instituto Tecnológico de Durango. Blvd. Felipe Pescador 1830-Ote. Col.
11 Nueva Vizcaya. C.P. 34080, Durango, Dgo., México.
12 * Correspondence: Juan Eduardo Sosa-Hernández (eduardo.sosa@tec.mx); Roberto Parra-Saldivar
13 (r.parra@tec.mx)
14
15 Abstract: Food and waterborne illness are still a major concern in the health and food safety areas. every year there are almost
16 420,000 deaths related to foodborne illness and 2.2 million of deaths related to waterborne illness worldwide, the major concern
17 pathogenic agents for these diseases are bacteria such as: Salmonella, Shiga-toxin producer E. coli, Campylobacter, Listeria
18 monocytogenes among other, in the other side major concern waterborne pathogens are Vibrio cholerae, leptospirosis, Schistosoma
19 mansoni, S. japonicum. Despite the major efforts for the control of food and water quality, safety and prevent the presence of
20 pathogens on this kind of sources, many foodborne and waterborne illness cases still occur globally. Due to the mentioned it is
21 required the development of novel, faster and more functional real-time surveillance methods for the detection of pathogenic
22 microorganisms in these sources. Methods based in biosensor devices emerged has a novel tool for faster detection of pathogens in
23 food and water, to displace the time-consuming pathogen detection methods, that usually takes a few days to obtain a precise
24 result and in many cases these methods do not generate considerable data. The biosensor devices can be summarized as a device
25 that uses biochemical reactions mediated by isolated enzymes, antibodies, tissues, DNA, or aptamers to detect the presence of
26 pathogens usually using electrical, thermal, or optical signals in response of the presence particular pathogen biomarkers, such as
27 specific genetic material sequence. The application of Nano and Molecular technologies permits
28 Citation: To be added by editorial the identification of pathogens in a faster and high sensibility process, available to discriminate at
29 staff during production. very low concentration of the pathogen for this objective the application of nanoparticles of gold,
30 Received: date silver, iron, and magnetics nanoparticles has been used to improve the function of the biosensor
31 Revised: date devices. In this review are summarized a principal application of nanomaterials and biosensor-
32 Accepted: date based devices for the detection of pathogens in food and water samples. It has been observed that
33 Published: date the application of nanomaterials has been improving the biosensor devices performance, also in
34 combination the nanomaterials used in biosensors offer unique advantages for pathogen detection.
35 Their small size and high specific surface area allow for more effective interaction with pathogenic
Copyright: © 2023 by the authors.
Submitted for possible open access
publication under the terms and
conditions of the Creative Commons
Attribution (CC BY) license
(https://creativecommons.org/license
s/by/4.0/).
3 Biosensors 2023, 13, x. https://doi.org/10.3390/xxxxx www.mdpi.com/journal/biosensors

4 Biosensors 2023, 13, x FOR PEER REVIEW 2 of 37
5
36 agents, enhancing the sensitivity and selectivity of the biosensors. Additionally, their ability to be functionalized with specific
37 molecules such as antibodies or nucleic acids facilitates the specific detection of the target pathogens.
38 Keywords: Nanobiosensors, Nanomaterials, Foodborne diseases, Waterborne diseases, Food

39 safety.
40
41
42
43
44 Graphical abstract
45
46 1. Introduction
47 Every year contaminated food is responsible for 420,000 deaths and 600 million
48 cases of foodborne illnesses caused by spoiled food [1]. This is not just a problem in
49 underdeveloped countries, also developed countries has several troubles related to
50 foodborne pathogens, Only in US there are more than 9.4 million deaths per year due to
7
51 the ingestion of pathogenic bacteria in food (Riu & Giussani, 2020), only in 2010, 420,000
52 people (one-third of them being children under the age of five) died from illnesses
53 related to salmonellosis and Escherichia coli infection [2]. Foodborne illnesses arise from
54 the presence of pathogens, toxins, and contaminants in food products. These illnesses
55 are typically associated with gastrointestinal symptoms such as diarrhea, vomiting,
56 abdominal pain, and fever. However, certain foodborne illnesses can have a significant
57 impact on human health, leading to neurological, hepatic, and renal complications, and
58 in some cases, they can be life-threatening if not appropriately addressed [3,4]. In recent
59 years the majority of reported foodborne illness outbreaks are caused by pathogens such
60 as: Norovirus [4], Campylobacter [5], Salmonella [4,5], Listeria monocytogenes [6], and
61 Shiga toxin-producing Escherichia coli [7]. Also, other pathogens that are occasionally
62 reported to cause illness include Staphylococcus aureus [8], species of Clostridium [9],
63 Bacillus cereus [10], Yersinia enterocolitica [11].
64 Similarly, to food pathogen, the presence of pathogens in water is a major concern
65 problem for health safety and biosafety [12], in fact it is estimated that 663 million
66 people consume untreated water obtained from different sources (surface and
67 groundwater) [13]. Diseases caused by the ingestion of contaminated water cause more
68 than 2.2 million deaths per year and more cases of diseases such as diarrhea,
69 gastrointestinal and systematic diseases are related to this cause [14], the major
70 pathogens related are: Salmonella, Shigella, Campylobacter, Staphylococcus aureus, and E.
71 coli [15,16], however the virus and parasite related diseases has become an incoming
72 problem [17], some parasite and pathogens linked to waterborne outbreaks include
73 Vibrio cholerae, leptospirosis, Schistosoma mansoni, S. japonicum, [15,18,19].
74 Monitoring the presence of pathogens such as viruses, bacteria and parasites in
75 water is very important as a measure to prevent diseases, derived from in drinking
76 contaminated water, also to surveillance the quality of water, these can be achieved
77 using protocol such as a wastewater-based epidemiology protocols, which allow the
78 detection of these pathogens [20,21], and can be applied to verify the quality of the
79 water that is discarded and how it has to be treated so as not to cause adverse effects on
80 the environment and to ensure water sustainability for future generations.
81 Pathogen detection methods has a crucial role in this quality preservation activity
82 and ensure food and water safety, however actual monitoring methods are time-
83 consuming process that usually takes a few days to obtain a precise result, and in some
84 cases they do not generate considerable data, limiting a real time pathogen monitoring
85 [22]. In fact, for the identification of pathogenic agents such as bacteria and viruses,
86 however, gold standards methodologies are traditional techniques: viable plate counts,
87 flow cytometry and staining methods, among others [23] [24,25]. Nevertheless, the
88 detection time is one of the major limitations of this technique, in fact, the necessary to
89 growth the pathogen in laboratory conditions is a limitans of this protocols, that can take
9
90 several days to get a result, hindering the response time for the control of pathogens
91 [24]. Among other fast techniques used for pathogen detection involve, polymerase
92 chain reaction techniques (PCR) [20,26,27], immunological methods [28] next-
93 generation sequencing [29], whole-genome sequencing [30], flow cytometry [31], and
94 the inclusions of the use of biosensors and nanoparticles (NPs ) in recent years [32–34].
95 The last-mentioned methods help to perform faster monitoring (real-time
96 surveillance systems), reducing response times to the presence of pathogens in water
97 bodies [35], the use of biosensors improved with NPs, allowing a better performance of
98 the device by making it faster, more specific and portable, among other improvements in
99 its characteristics [36]. In fact, the nature of the NPs is a subject of study as they show
100 diverse detection capabilities, when applied under the assumption of being part of a
101 pathogen detection system [37].
102 Due the above mentioned and the necessity of increasing of concern of other kind of
103 pathogens, it is becoming necessary the development of rapid methods for the detection
104 of pathogenic bacteria, virus and parasite [38]. Unfortunately, and despite recent
105 advances in new pathogen detection approaches, their applicability is still limited, this is
106 why technologies capable of obtaining better results in a fast and affordable way have
107 been studied and developed new technologies that are "rapid, sensitive and specific" for
108 the detection of pathogens is a priority assignment to ensure health security and prevent
109 food and water borne outbreaks, for this purpose the development of biosensor-devices
110 emerge as a novel solution [39].
111 In order to improve the pathogen detection method, this is why multiple
112 methodologies and technologies have been developed to allow for rapid and accurate
113 pathogen detection [40]. The tools offered by molecular biology have emerged as an
114 alternative for faster analysis [41], e.g., quantitative polymerase chain reaction (qPCR)
115 [42], conventional polymerase chain reaction (PCR) [43] digital droplet PCR (ddPCR)
116 (Chen et al., 2021), fluorescence in situ hybridization (FISH) [43], surface plasmon
117 resonance imaging (SPR) [45], enzyme-linked immunosorbent assay (ELISA) [46],
118 surface-enhanced Raman spectroscopy (SERS) [47], these technique has been applied
119 has a pathogen detection methodologies in different matrices such as food and water
120 [4,24].
121 The Biosensors devices are composed as follows; biorecognition element, a
122 transducer, amplifier, and processor. The biorecognition element recognizes the analyte
123 of interest, the transducer generates a signal from the recognition of the analyte into a
124 measurable signal which is then processed by a processor and amplifier to obtain a
125 signal output [48,49]. In summary is a bioanalytical device that detect specific
126 biomarkers using biochemical reactions [50] mediated by isolated enzymes, antibodies,
127 tissues, organelles, or whole cells to detect biomarkers related to the presence of
11
128 pathogen, using electrical, thermal, or optical signals [51], correlating the presence of
129 specific pathogen in a mentioned matrixes and signal emission [32].
130 The application of biosensor have garnered attention in the field of pathogen
131 detection due to their precision, decent selectivity, and short analysis times [25].
132 However, these methodologies also have certain disadvantages (use of expensive
133 enzymes and equipment), not to mention the extensive laboratory work involved.
134 Therefore, there is a need to develop fast, highly specific, and sensitive techniques for
135 pathogen detection [35]. Currently, biosensor technology has greater possibilities for
136 application due to its unique sensitivity, low detection limit, and simple operation
137 compared to traditional techniques [52].
138 In recent years, the development of biosensors has been focused on the
139 miniaturization of the devices without affecting the detection efficacy. To achieve this
140 priority NPs are employed for the miniaturization of the biosensor through the
141 development of the nano-scale platform, indeed, in the different sections of the
142 biosensor, NPs are used as signal transducers to convert a biomolecular interaction into
143 an electrical, optical, or magnetic signal [53]. This functionality inside of biosensor is
144 because of unique properties at nanometric scales (surface area, small size, affinity for
145 some biomolecules, catalytic activity, and autofluorescence) [54,55].
146 The nanobiosensors are composed of three parts: biorecognition probe, transducer,
147 and amplifier (fig. 1) [56]. NPs are often used as transducers which combine a
148 biochemical, electrical, magnetic or optical signal [53] these signals can be read simply
149 and effectively (fig.1) shows the structure of a biosensor using NPs functionalized with
150 biorecognition and as transducer. [57]
151
Figure 1. General structure of nanobiosensor with differents agents of biorecognition

13
152 Nanomaterials have been identified as ideal candidates to enhance biosensors in

153 terms of sensitivity and the reduction of detection limits, enhances detection capabilities,
154 being highly specific and making it one of the best alternatives for early diagnosis [37];
155 [36]. Through the detection of electrochemical signals, the specificity of signal
156 recognition is results of the adequate selection of ligands, and functionality, directly
157 conjugated with the NPs that help to attracts biomarkers of interest, also NPs convert
158 signals from one form to another or act as detectors of the generated signals [58],[59].
159 The classification based on the type of bio-recognition immobilized on the
160 nanomaterial [60] is divided into: enzymes [61], antibodies [62], antigens [63], DNA-
161 RNA [64], organelle [65], cell membrane [66], and phage particle [67]. The conversion of
162 this signal can be achieved in different ways, and this can be classified according to the
163 type of conversion used [68]. The classification of conversion systems can include optical
164 systems. [69] electrochemical nanobiosensors [70] thermoelectric [71] and piezoelectric
165 [72]. The classification based on the type of bio-recognition immobilized on the
166 nanomaterial [60] is divided into: enzymes [61], antibodies [62], antigens [63], DNA-
167 RNA [64], organelle [65], cell membrane [66], and phage particle [67]. The conversion of
168 this signal can be achieved in different ways, and this can be classified according to the
169 type of conversion used [68]. The classification of conversion systems can include optical
170 systems. [69] electrochemical nanobiosensors [70] thermoelectric [71] and piezoelectric
171 [72].
172 2. Biofunctionalization of Nanostructured Surfaces for Interaction with

173 Biorecognition Agents
174 It is essential for the biomaterial surface to be biocompatible in order to allow
175 protein adsorption without altering the natural structure of the bioactive molecule [73].
176 Bioconjugation involves the interaction of chemical or functional groups between NPs
177 and biomolecules [74,75]. Also, it is important to mention the properties that can affect
178 the efficiency of the connection with the biomarkers are: the optimal distance between
179 biorecognition molecules and the nanostructure, the pH of the storage buffer used, as
180 well as potential modifications to the biological and antigenic properties of biomolecules
181 after conjugation, developing different approaches for nanostructures conjugation
182 [76,77], by custom functional groups (such as primary amines, carboxylates, cis-diols,
183 and sulfhydryls) on nanosurfaces.[54,78].
184 Therefore, the adsorption of bioactive molecules into biosensor and nanobiosensor
185 devices can be classified into the following categories: (i) non-covalent immobilization
186 strategies, those techniques are based in electrostatic interaction, hydrophobic
187 adsorption, and coordination bond formation between biorecognition molecules and the
188 surface of nanomaterials (fig. 2) [75,79], (ii) covalent immobilization strategies,
189 involving chemical bonds, chemically activate and modify biorecognition molecules,
15
190 achieving a stable binding. They enhance sensitivity and selectivity in pathogen
191 detection, ensuring a robust interaction [80], and finally (iii) combined techniques
192 [76,81].
193
194
195 Figure 2. Different techniques of bioconjugation in nanomaterials
196 2.1 Biorecognition section of bionsensor device: Enzymes applications

197 Enzymatic reactions in biodetection processes involve the following steps: Firstly,
198 enzymes recognize and bind to the target molecule in the environment / solution, often
199 through specific binding sites or active sites on the enzyme, enzymes are typically
200 immobilized on the surface, electrode or substrate, of the sensor in order to provide the
201 best conditions to react with a specific target molecule and produce a detectable signal
202 [82]. Subsequently, enzymes catalyze chemical reactions and produce detectable signals.
203 Enzymatic activity can be used as a signal through variations in the concentration of
204 protons, entrance or exit of gases, heat emission (Dziąbowska et al., 2018). Finally, the
205 signal generated is detected and quantified using detection techniques (electrochemical
206 and fluorescence techniques) [82,83]. In fact, a biosensor-based in enzymes immobilized
207 on Au-NP was used to detect the microbial pathogen , Campylobacter jejuni in chicken
208 breast samples, in this biosensor the nuclease enzymes and deoxyribozymes was
209 immobilized to detect the presence of the pathogen for the reaction of the scission
210 enzymatic generating a heteroduplex of DNA-RNA, which finally induce a detectable
211 signal based in a fluorescence detection model with a LOD of 10 pM [84]
17
212 To enhance the biosensor recognition capacities, the immobilization and

213 stabilization of the enzyme are a normal process, in fact, for the immobilization of
214 enzymes on nanostructures, different techniques are commonly applied, such as
215 covalent binding, crosslinking, and self-assembled monolayers [85]. However, using
216 enzymes as biorecognition agents has certain disadvantages in in situ applications.
217 Enzymatic activity can be influenced by environmental conditions such as temperature
218 and pH, which affect the stability of the biosensor [86].
219
220 2.2 Antibody applications
221 Antibodies (immunoglobulins) are proteins produced by cells of the immune
222 system called B lymphocytes [87]. They consist of a basic structure composed of four
223 polypeptide chains: two identical heavy chains and two identical light chains with their
224 typical "Y" shape [87,88]. Antibodies are among the many biological molecules that
225 have gained importance due to their high specificity and in vivo uniqueness, for the
226 detection of pathogen biomarker [89]. The monoclonal antibodies, have been designed
227 to precisely target antigens or receptors [90]. The antibodies used as a part of biosensor
228 device are derived from animals and commonly are immobilized . This is the case with
229 Majdi et al., (2019) for the immovilized an antibody with NP or nanomaterial includes
230 adsorption by weak interaction such as electrostatic, hydrophobic or van de Waals forces
231 [92], in the other hand the preferred method for immobilizing antibodies onto NPs and
232 other surfaces is through covalent bonding, specifically using carbodiimide chemistry
233 and maleimide conjugation. This approach allows for longer lasting and reusable
234 devices, as well as better control over antibody orientation, resulting in enhanced
235 detection capabilities [92,93].
236 These type of antibody-functionalized biosensor has been used for the biodetection
237 of different pathogens, in the case of Guo et al., (2020) developed a method that utilizes
238 NPs etching. These techniques allow for specific detection of Salmonella Typhimurium.
239 Using a catalase-modified antibodies bind to the bacteria and catalyze the conversion of
240 H2O2 to H2O. In the absence of Salmonella Typhimurium, the catalase-modified
241 antibodies do not bind to the bacteria, resulting in a significant accumulation of residual
242 H2O2. HRP triggers the production of •OH, causing a color change in the Au nanowires
243 from dark blue to pink. The linear detection range is between 18 UFC mL−1 to 1.8 × 10^5
244 CFU mL−1, with a detection limit of 35 CFU mL−1 [94]. However, antibody-
245 functionalized biosensors have limitations including lack of specificity, long-term
246 stability, high production cost, challenges in antibody immobilization, potential cross-
247 reactivity, limited antibody availability, and batch-to-batch variability [32].
248
249 2.3 DNA applications
19
250 Nucleic acid-based biosensors, such as DNA, stand out as biorecognition elements
251 due to their simplicity, speed, and high specificity. For this reason, they are widely used
252 for the detection of pathogens and other substances of interest in various biodetection
253 applications [77]. These characteristics make DNA a powerful and versatile tool in the
254 field of biodetection [95,96]. These molecular probes can be used in different ways and
255 methods, such as DNAzyme [97], DNA hairpin [98], DNA hybridization [99], and DNA
256 origami [100]. It is widely recognized that DNA and its assembly structure can be
257 applied to detect specific targets, including nucleic acids, proteins, metal ions, and small
258 biological molecules. Common bioreceptors in this category include deoxyribonucleic
259 acid (DNA), ribonucleic acid (RNA), and peptide nucleic acids (PNA) [101].
260 These biomarkers have been functionalized with nanomaterials to enhance their
261 selectivity and durability in pathogen biodetection. An application of pathogenic
262 bacteria detection in milk, was development using a combination of photo-induced
263 electron transfer (PET) between a G-quadruplex DNAzyme and silver nanocluster-
264 labeled DNA, along with exponential circular amplification based on hairpin probe,
265 achieving an ultra-low detection limit of 8 cfu·mL−1 for S. Typhimurium. This strategy
266 represents a promising platform for highly sensitive and specific detection of pathogenic
267 bacteria in food analysis [102]. In another study a fluorescent DNA hairpin template
268 was develop by designing two hairpin probes with Au-NPs for the detection of
269 Staphylococcus aureus 16S rRNA. HP1 was biofunctionalized with thiol groups and a
270 fluorescent chromophore, and a thiol group was attached to the NP surface. The
271 addition of HP2 causes the target sequence to walk along the surface of the Au-NPs,
272 thus opening the hairpin structure of HP2 and enabling the recycling of the target
273 sequence. They achieved a LOD of 7.73 CFU mL-1 with an FM of 4.36x10-5,
274 demonstrating a novel and efficient method for the detection of S. aureus [103].
275
276 2.4 Aptamer applications
277 Aptamers are short sequences of RNA or DNA (oligonucleotides) capable of folding
278 into unique three-dimensional structures and binding to targets such as proteins, lipids,
279 ions, small-molecular-weight metabolites, and even whole cells with high specificity and
280 affinity [104]. To produce aptamers, the SELEX (Systematic Evolution of Ligands by
281 Exponential Enrichment) process is utilized. In this process, aptamers are generated
282 through in vitro synthesis of combinatorial libraries with diverse sequences [35].
283 Through an iterative selection process, aptamers with higher affinity for the desired
284 target are enriched and amplified, while those with lower affinity are discarded. This
285 enables the generation of highly specific and high-affinity aptamers for various
286 biomolecular targets [105]. The analytes of aptamer-based biosensors can vary between
287 size, and complexity as it can detect specific molecules such as proteins or more complex
288 analytes such as whole cells. Aptamers modify its structure once reacting with a specific
289 analyte and the conformational change can be transduced by different types of signals
21
290 such as optical or electrochemical (Sharifi et al. 2020; Bakhshandeh et al. 2022;
291 Sadanandan et al. 2023).
292 Some of the applications of aptamer-based sensor were developed for the detection
293 of S. aureus, E. coli and Campylobacter jejuni pathogen biomarkers [35] another example
294 was the results for S. aures detection protocolos where they designed an ultra-sensitive
295 magnetic fluorescence aptasensor based on fluorescence resonance energy transfer, the
296 aptamers on the surface of Fe3O4 and modified carbon dots (CDs). CDs were used as the
297 fluorescence donor and Fe3O4 as the "off-on" sensor receptor. Due to the strong affinity of
298 the aptamers for bacteria, the presence of target bacteria led to the disassembly of the
299 Fe3O4/CDs aptasensor, resulting in the recovery of CD fluorescence whit a range of
300 detection exhibited between 50x10^7 CFU mL-1 and 8 CFU mL-1 [106].
301 Other example is the application for Escherichia coli detection using graphene oxide
302 (GO)-modified Au-NPs, enhanced with aptamers E8 aptamer for E. coli detection. The
303 detection limit was found to be 10 cells mL-1 in water and coconut water-enriched
304 samples. Furthermore, the aptamer-based nanosensor exhibited selectivity towards its
305 target without any cross-reactivity with other bacteria. The color change from red to
306 blue, based on aggregation, can be easily visualized by naked eye [107], other protocol
307 for E. coli detection in water, was the nanobiosensor using QDs functionalized with
308 aptamer II and coated with magnetic NPs. Fluorescence values were recorded for 100,
309 200, 300, 400, and 500 CFU, each with CdTe-MPA QDs at 100 μg/mL, resulting in digital
310 signals of 29.3 mV, 34.18 mV, 39.06 mV, 43.94 mV, and 48.82 mV respectively,
311 demonstrate that CdTe-MPA QDs conjugated with aptamer II were capable of
312 selectively capture and detect E. coli [108].
313 Aptamers exhibit significant advantages for the application in pathogen detection,
314 including lower molecular weight, easier and more cost-effective production methods,
315 and good chemical stability [35], also their ability to be generated against a wide range
316 of targets, ranging from small molecules to large proteins, even whole live cells such as
317 bacteria [109], leading to their utilization in various nanobiosensor technologies for
318 pathogen detection. Different technologies are employed in these sensors, including
319 surface plasmon resonance (SPR), electrochemistry, piezoelectric effect, and
320 chemiluminescence [68].
321 For example, SPR sensors utilize the reflection of light on a modified metal surface
322 to detect changes in refractive index due to analyte binding. This enables precise and
323 sensitive detection of the target analytes [68]. In the case of electrochemical sensors, the
324 analyte interaction is translated into an electrical signal, providing a quantitative means
325 of detection and enabling real-time measurements [110]. Piezoelectric sensors, on the
326 other hand, leverage the piezoelectric effect to convert the mechanical energy generated
327 by analyte interaction into electrical energy, allowing highly sensitive and accurate
328 detection [111]. Furthermore, chemiluminescence is another technology used in
329 biosensors, where the analyte interaction triggers a chemical reaction that generates
23
330 light. This emitted chemiluminescent light can be measured to detect and quantify the
331 analyte, providing highly sensitive and specific detection [112].
332
333 Functionalizing nanomaterials with aptamers have allowed combining various
334 signal transduction strategies (including colorimetric, electrochemical, and fluorescence
335 methods) for detecting foodborne pathogens. This versatility in detection provides the
336 ability to utilize different approaches according to the specific needs of each application,
337 enhancing the sensitivity and selectivity of detection systems. Thus, aptamers become a
338 powerful and promising tool in the fight against food contamination and the protection
339 of public health [113]. These technologies enable the detection and quantification of
340 substances in biological samples, providing versatile and efficient options for
341 applications in fields such as medical diagnosis, food safety, and environmental
Figure 3. Combination of different nanomaterials and sensors for the detection of pathogens
342 monitoring (fig 3).
343 3. Nanomaterials for the detection of pathogens in water and food

344
345 The precise detection of pathogens in water and food is of vital importance to
346 ensure sanitary safety. In this context, nanomaterials play a crucial role by offering
347 innovative and sensitive solutions. The exploration of nanomaterials in combination
348 with highly efficient aptamers is revolutionizing the detection of pathogens in water and
25
349 food. This fusion of nanotechnology and aptamers opens new possibilities for more
350 effective control and quicker responses to potential public health risks. The following
351 table summarizes the last five years of nanobiosensor production for the detection of
352 viruses, bacteria, and parasites using aptamers in complex matrices.
353
354 Table 1 NPs application for detection of pathogenic bacteria in food and water matrices
Nanomateria Pathogen Matrix LOD Signal Bioconjugate Reference

l d material
Au-NPs S. aureus Tap- 101 to 104 Fluorescence Aptamer [114]
water CFU
mL-1.
Au-NPs E. coli Tap 10 cell Fluorescence - [115]
S. water mL-1 in
Typhimurium and lake tap
water water
and 100
in lake
Au- P. aeruginosa Water 1 cell LSPR Aptamer [116]
N.triangles
AuNPs Staphylococcus Luria 1.5x107 Colorimetric Aptamer [117]
aureus bertani cells/mL
media
AuNPs Ochratoxin A Peanut, 28.18 Colorimetric Aptamer [118]
soybean, pg/mL
and corn
AuNPs E. coli Flour 2.5 ng/µ Colorimetric Probe [119]
L
Graphene E. coli Bacterial 1x103 Colorimetric Antibody [120]
oxide coated S. suspensio CFU
AuNPs Typhimurium n
Ag-NPs S. aureus Water 1,0 Electrochemical Aptamer [121]

ufc/mL
Ag-NPs E. coli Water 150 Electrochemical Aptamer [122]
CFU/ml
Chitosan- Glipopolysacc Bacterial 248 Electrochemical - [123]
AgNPs haride suspensi CFU/mL
27
on
AgNPs S. aureus Bacterial 1 Electrochemical Aptamer [124]
suspensi CFU/mL
on and
human
serum
AgNPs E. coli Pork, 2 Photoelectroch Peptide [125]
cabbage CFU/mL emical Magainin
and milk
Au-NPs and E. coli Water 9,34 Electrochemical Aptamer [126]
oxide of CFU mL
graphene -1
NPs
Multiwalled E. coli Water 0,8 Electrochemical Antibody [127]
carbon CFU/mL
nanotubes
Graphene Salmonella Water 102–108 Colorimetric Antibody [128]
and carbon enteritidis cfu mL-
nanotubes 1
FeO-NPS and E. coli Water 1 × 102 Fluorescence Aptamer [108]
Quantum dots CFU
Quantum S. aureus, S. Water 16-28 Colorimetric Aptamers [129]
dots typhimurium CFU/mL
SiNPs E. coli Bacterial 103 Electrochemical Polyclonalanti [130].
suspensio CFu/mL bodies
n
SiNPs E. coli Bacterial 8 Fluorescence Rhodamine B [131]
suspensio CFU/mL
n
SiNPs AFB1 from Peanut, 0.214 Fluorescence Aptamer [132]

filamentous maize pg/mL
fungi and
badam
MNPs S. aureus Milk, 2.5 ng/µ Colorimetric Probes [133]
Romaine L
lettuce,
ham,
29
sausage
Iron oxide Bacillus cereus Inoculate 12 Electrochemical Vancomycin [134]
MNPs assisted and Shigella d media cells/mL
AuNPs flexneri and
3
cells/mL
Iron core gold Salmonella Beverage 32 Fluorescence Antibody [55]
NPs enteritidis samples Salmonell
a/mL
MNPs Salmonella Abrir en 53 Abrir en tec Abrir en tec [135]
Typhimurium tec CFU/nL
Iron oxide Hepatitis E Clinical 56 RNA Fluorescence Antinody [136]
encapsulated virus samples copies/m Electrochemical
quantum dots Norovirus L
69 RNA
copies/m
L
QDs Salmonella Chicken 43 Fluorescence Antibody [137]
Typhimurium meats CFU/mL
QDs Salmonella Aquatic 10 Fluorescence Aptamer [138]
Typhimurium samples CFU/mL
and Vibrio
parahaemolyti
cus
102
CFU/mL
QDs nanobeds Salmonella Potable 10−1 Fluorescence Antibody [139]
Typhimurium water, CFU/mL
orange
juice,
lettuce,
and
chicken
355
356 3.1 Gold nanopartícles (Au-NPs)
357 Among the different types of NPs, metallic nanoparticles (MNPs) exhibit many
358 useful characteristics for their application in various fields of biotechnology, such as
359 high surface-to-volume ratio, conductivity, selectivity, and excellent optical and
360 chemical properties [140,141]. The application can vary depending on the metal used,
31
361 size, shape, surface properties, and functionalization of the MNPs (Patel et al., 2022). On
362 one hand, Au-NPs have been successfully used in pathogen detection because they can
363 easily be conjugated with recognition and biorecognition elements such as aptamers,
364 DNA, antibodies, carbohydrates, and proteins, which can enhance the reactivity and
365 selectivity of the NPs towards specific pathogens [33,143].
366 Au-NPs are one of the most stable MNPs, not to mention their unique
367 characteristics such as good chemical reactivity, conductivity, and high resistance, which
368 have attracted attention for their use in biosensor development [144]. The surface of Au-
369 NPs has been functionalized with various biocomponents [145]. These nanobiosensors
370 have a very low limit of detection (LOD) for different chemical and biological analytes,
371 not to mention their high stability against oxidation [144].
372 Their characteristics, such as stability, conjugation, amplification properties, and
373 their ability to serve as colorimetric biosensors [146–148], as are especially relevant in the
374 case of Au-NPs due to their localized surface plasmon resonance, which is a
375 phenomenon that gives unique optical properties to MNPs, particularly Au-NPs. This is
376 due to the interaction of electromagnetic waves with NPs of specific sizes and shapes,
377 resulting in differential absorption of the light spectrum and different colors exhibited
378 by the NPs [32,33]. These properties can be altered in the presence of different analytes,
379 making Au-NPs highly suitable for biosensor development.
380 3.2 Silver nanoparticles (Ag-NPs)
381 Ag-NPs stand out for their wide range of applications. These nanomaterials have
382 been incorporated into textiles, healthcare products, consumer goods, medical devices,
383 biodetection, among others [149]. These materials are highly attractive in the field of
384 diagnostics due to their high conductivity, catalytic activity, and plasmonic properties
385 that can be leveraged to enhance the performance of biosensors [150]. Sensitivity is a
386 crucial factor in biosensors for detecting low concentrations of an analyte. Ag-NPs have
387 been used to increase the electroactive surface area of electrodes, thereby enhancing the
388 electron transfer rate and improving biosensor sensitivity biosensor [149,150]. In a
389 biosensor, Ag-NPs have the characteristic of amplifying signals or improving the
390 detection of nucleic acids. Their plasmonic resonance absorption band below 500 nm
391 confers selective absorption in the visible and near-infrared spectrum [144]. In the
392 phenomenon of surface plasmon resonance (SPR), electrons on the surface of a metal are
393 excited by photons of specific wavelengths and incidence angles (Li, 2018; Varghese
394 Alex et al., 2020), This phenomenon is utilized to detect a target based on the refractive
395 index [151]. When bound to a biosensor, the biological recognition event between the
396 analyte and the biological recognition element results in a change in the SPR resonance
397 angle [153].
398 Conjugated polymers such as those that include silver nano particles are promising
399 materials for the addressing of current and emerging issues such as pandemic
400 monitoring [154], and pathogen detection both in food [125] and in water [121]
33
401
402 3.3 Carbon-based nanoparticles
403 Similar to Au-NPs, carbon-based NPs are useful for the implementation of
404 detection techniques for pathogen monitoring in water [155,156]. Carbon-based NPs
405 such as carbon nanotubes, graphene and carbon nanodots have great potential in
406 biosensing of pathogens because of their ability to be coated with different biomolecules
407 for association of molecular patterns from pathogens and generate a signal for specific
408 pathogens as functionalized NPs can mimic the specific surface structure of pathogens
409 [157]. Carbon NPs have been used in the fluorescence resonance energy transfer (FRET)
410 technique with quantum dots as donors modified with aptamers for the detection of
411 Vibrio parahaemolyticus and Salmonella typhimurium in the range of from 25 and 35 cfu/mL
412 and up to 50 to106 cfu/mL respectively [158]. Also, these NPs can be used in combination
413 with aptamers to amplify the sensitivity and specificity of the device.
414
415 3.4 Magnetic nanomaterials (MNPs)
416 Magnetic NPs possess their own versatility when used for biosensing pathogens,
417 because of their specific attributes particularly fast separation and concentration that
418 makes them an easy tool for pathogen detection [159]. MNPs have been used for
419 detecting pathogen by nucleic acid detection and quantification in devices for point of
420 care testing in the detection of hepatitis B virus (limit of detection of 50 IU/mL) and
421 SARS-CoV-2 (500 copies/mL) [160].
422 The magnetic NPs (MNPs) can conform a section of the transducer part of the
423 biosensor, or to be suspended in solution in direct contact with the analyte of interest
424 [161], when the MNPs are in contact with the sample, bind to the target molecule by
425 interaction of the label in the NPs (a functional group) and a protein, once the complex
426 of MNP and target is formed an external magnetic field attract it to the active detection
427 surface and after a wash of the not binding molecules targets are detected [162]
428 When talking about magnetic NPs s in biosensing, it is important to mention the
429 magnetic relaxation switching mechanism (MRS). This phenomenon describes the time
430 when cross-linking occurs between the MNPs in the binding and recognition of targets.
431 When these MNPs clusters are formed, a change in the transverse relaxation of the
432 sample is reflected as motional averaging or static dephasing according to the MNPs
433 cluster size and this change can be monitored by nuclear magnetic resonance (Min et al.,
434 2012).
435
436 3.5 Silica nanoparticles (Si-NPs)
437 Si-NPs have applications in biomedical field [164], they present good optical
438 properties and also have a good biocompatibility [165] NPs possesses the quality of
439 being mesoporous witch in combination with other metals result in attractive and
35
440 profitable characteristics for biosensing purposes [165] Its uniformity and easily pore
441 size change among the gating mechanism makes the very useful in biosensing for drugs
442 delivery, for example [166] another important characteristic of SiNPs is that there are
443 considered as a GRAS (generally recognized as safe) material by the FDA. [167,168].
444 The mesoporous nature of the silica NPs is a characteristic of big interest, this
445 feature can be employed to separate bacteria from complex samples even preserving its
446 viability, colloidal stabilization of magnetic NPs for the same purpose. Also, the silanol
447 functional groups from SiNPs make possible the use and design of various bio-
448 recognition systems that help to increase the sensibility and selectivity while reducing
449 detection time of different pathogens [168].
450
451 3.6 Quantum Dots (QD)
452 Quantum dots (QD) are colloidal nanocrystalline semiconductors that possess
453 properties such as quantum confinement effect, allowing them to emit and absorb light
454 at specific wavelengths [169]. Because of this, QDs exhibit excellent optical properties,
455 including a broad absorption spectrum, a narrow emission spectrum, and tunable
456 luminescence, which show great prospects in biodetection [170]
457 QD-based biosensors include and may not be limited to fluorescence,
458 bioluminescent, chemiluminescent and photoelectrochemical approaches [171]. Some of
459 the characteristics that make attractive the use of quantum dots for biosensing
460 applications are that the possess high quantum yield, better photobleaching resistance,
461 wide absorption spectrum, a narrow emission spectrum and their specificity with
462 biologic targets in comparison with common fluorophores and dyes (Pourmadadi et al.,
463 2023). Also, it is very remarkable that its surface is easily functionalized with biologic
464 components in order to integrate QD probes [171]. In the field of nanomaterials, also the
465 use of combinations of magnetic compounds displays attractive characteristics for
466 current applications, these nanocomposites besides maintain magnetic behavior
467 complementary add functional proprieties to the final product, [136]
468 As presented above numerous studies focus its determinations on Salmonella
469 Typhimurium mainly because it is the most common pathogen related to food poisoning
470 in western countries causing gastro ententeritis [173]. If well it is the model or the target
471 of the experimentations, the modifications in for example primers design or binding
472 proteins may allow to replicate the studies carried with this strain to any other food
473 pathogen [138,139,174].
474 4. Challenges and limitations to detect pathogens by DNA using nanobiosensors

475 The importance of exceptionally responsive devices is essential in advancing
476 biosensors. Insufficient sensitivity and affinity towards biomarkers can significantly
477 impact the performance of the device, in fact some of the biomarkers are at ultra-low
37
478 concentration in the samples (pM) and in consequence it is necessary that the device
479 could detect these concentrations. [175]. For the application of biosensor-base detection
480 protocols a range of detectable concentration are dependent of biomarker selected, also
481 of the analyte source, in fact some limit of detection has a range of pM to mM of
482 concentrations, for pathogen detection [176] However, using a genetic and whole cell-
483 based biomarker targets, some of the bionsensor has limit of detection of 3 genetic copies
484 per sample [177], 1CFUmL-1 [178] or even reaching a detection limit of 3x10 6 gene copies
485 per sample [8] or 5x104 CFUmL-1 biomarker concentration in the sample [179]
486
487 As is mentioned above, the choice of signal recognition technology can determine
488 the sensitivity level required to identify biochemical, genetic or whole cell biomarker
489 concentration in the sample [180,181] affect the performance of the device, in fact the
490 detection ultra-low concentration of pathogen-diseases biomarkers concentration in
491 samples is a mandatory request to early detection in clinical diagnoses [182]
492
493 Some of the disadvantages of biosensor-based pathogens detection are firstly: the
494 factors to be determined is the target molecule to be sensed, in fact the sensitivity and
495 specificity are compromised by the biomarker choice [96]. The use of genetic markers
496 makes the device more sensitive, however it necessitates intricate systems and laborious
497 sample/re-agent handling procedures [183].
498
499 On the other hand, signal emission technology is another important factor in
500 pathogen detection, colorimetric-based biosensor has several factors that may alter its
501 detection capability, such has colorimetric substrate, incubation time and even the
502 temperature in the signal is measured [184], particularly in DNA-based biosensor other
503 factors can be, Lack of the ability to form complex, complication in large-scale patterns,
504 reaction induction by mistake and are sensitive to enzymatic degradation and oxidation
505 [96].
506
507 However, there are several applied technologies in the biorecognition section of the
508 biosensor device, for microbial pathogens detection, are the use of gene sequence
509 biomarkers such as, CRISPR/Cas9-based technology, where the low limit of detection
510 was 3x100 genetic copies per sample, reaching to 3x10 6 gene copies per sample [8] in this
511 study the detection signal was dose-response intensity. CRISPR/Cas12 based lateral
512 flow, where the low limit of detection was 4x10 0 gene copies in the sample [177]. Other
513 of the limitations to consider in the application of these device is the ability of the
514 biosensor to discriminate between Live/death cells (LOD 1 CFUmL -1), the use
515 functionalized NPs with bacteriophages as a biorecognition agent is a solution applied
516 for successfully discrimination between live/death [178].
517
39
518 Conclusions
519 Over the years, significant advancements have been made in the field of biosensors,
520 particularly in areas related to food safety and the monitoring of pathogenic
521 microorganisms associated with food and waterborne illnesses. Despite these
522 achievements, progress in technologies for the development of biosensors applied to
523 pathogen detection remains a highly promising area of study. This is due to the presence
524 of various nanomaterials (MNPs, QD, carbon nanotubes, among others) with specific
525 properties that enable the identification of specific pathogens.
526 The nanomaterials used in biosensors offer unique advantages for pathogen detection.
527 Thanks to their small size and large specific surface area, they facilitate more effective
528 interaction with pathogenic agents, enhancing the sensitivity and selectivity of
529 biosensors. Furthermore, their capacity to be functionalized with specific molecules,
530 such as antibodies, nucleic acids, or aptamers, provides intrinsic advantages. In
531 particular, aptamers, due to their chain-like structure, offer greater flexibility and ease of
532 design, making them highly selective and sensitive agents for the precise detection of
533 pathogens.
534 In addition, pathogen detection through biosensors has a substantial impact on public
535 health. By enabling the precise and rapid identification of pathogenic agents in food and
536 water, this technology contributes to preventing disease outbreaks and taking
537 appropriate measures to ensure consumer safety.
538 In summary, the nanomaterials employed in biosensors present diverse advantages for
539 pathogen detection. Their reduced size, high specific surface area, functionalization
540 capacity, and signal amplification properties contribute to the sensitivity, selectivity, and
541 precision of biosensors. These qualities, combined with the potential to use techniques
542 such as fluorescence and others, make nanomaterial-based biosensors promising tools
543 for pathogen monitoring and detection, enhancing safety in the food industry and public
544 health overall.
545 Author Contributions:
546 Conceptualization. H.M.V.A., A.A.A. E.R.M.S; Writing— original draft preparation: H.M.V.A.,
547 A.A.A, E.R.M.S;; Data curation: H.M.V.A, A.A:A, E.R.M.S;; Writing—review and editing:
548 H.M.V.A., E.R.M-S; A.A.A, xxxxxxxxxx Funding acquisition: xxxxxxx; Supervision. J.E.S.H., R.P.S.
549 Supplementary Materials: The following supporting information can be downloaded at:
550 www.mdpi.com/xxx/s1, Figure S1: title; Table S1: title; Video S1: title.
551 Author Contributions: For research articles with several authors, a short paragraph specifying
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553 “Conceptualization, X.X. and Y.Y.; methodology, X.X.; software, X.X.; validation, X.X., Y.Y. and
554 Z.Z.; formal analysis, X.X.; investigation, X.X.; resources, X.X.; data curation, X.X.; writing—
41
555 original draft preparation, X.X.; writing—review and editing, X.X.; visualization, X.X.; supervision,
556 X.X.; project administration, X.X.; funding acquisition, Y.Y. All authors have read and agreed to
557 the published version of the manuscript.” Please turn to the CRediT taxonomy for the term
558 explanation. Authorship must be limited to those who have contributed substantially to the work
559 reported.
560 Funding: Please add: “This research received no external funding” or “This research was funded
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43
597 must be declared in this section. If there is no role, please state “The funders had no role in the
598 design of the study; in the collection, analyses, or interpretation of data; in the writing of the
599 manuscript; or in the decision to publish the results”.
600 Appendix A
601 The appendix is an optional section that can contain details and data supplemental
602 to the main text—for example, explanations of experimental details that would disrupt
603 the flow of the main text but nonetheless remain crucial to understanding and
604 reproducing the research shown; figures of replicates for experiments of which
605 representative data is shown in the main text can be added here if brief, or as
606 Supplementary data. Mathematical proofs of results not central to the paper can be
607 added as an appendix.
608 Appendix B
609 All appendix sections must be cited in the main text. In the appendices, Figures,
610 Tables, etc. should be labeled starting with “A”—e.g., Figure A1, Figure A2, etc.
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1 Type of the Paper (Review)

2 Emerging Applications of Nanobiosensors in Pathogen

3 Biosensors 2023, 13, x. https://doi.org/10.3390/xxxxx www.mdpi.com/journal/biosensors

38 Keywords: Nanobiosensors, Nanomaterials, Foodborne diseases, Waterborne diseases, Food

Figure 1. General structure of nanobiosensor with differents agents of biorecognition

152 Nanomaterials have been identified as ideal candidates to enhance biosensors in

172 2. Biofunctionalization of Nanostructured Surfaces for Interaction with

195 Figure 2. Different techniques of bioconjugation in nanomaterials

196 2.1 Biorecognition section of bionsensor device: Enzymes applications

212 To enhance the biosensor recognition capacities, the immobilization and

343 3. Nanomaterials for the detection of pathogens in water and food

Nanomateria Pathogen Matrix LOD Signal Bioconjugate Reference

Ag-NPs S. aureus Water 1,0 Electrochemical Aptamer [121]

SiNPs AFB1 from Peanut, 0.214 Fluorescence Aptamer [132]

474 4. Challenges and limitations to detect pathogens by DNA using nanobiosensors

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