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Magnetic Separation and Centri-Chronoamperometric Detection of Foodborne Bacteria Using Antibiotic-Coated Metallic Nanoparticles

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Magnetic Separation and Centri-Chronoamperometric Detection of Foodborne Bacteria Using Antibiotic-Coated Metallic Nanoparticles biosensors Article Magnetic Separation and Centri-Chronoamperometric Detection of Foodborne Bacteria Using Antibiotic-Coated Metallic Nanoparticles Mohamed Fethi Diouani 1,2,*,†, Maher Sayhi 1,2,3,4,*,† , Zehaira Romeissa Djafar 5,6, Samir Ben Jomaa 1,7, Kamel Belgacem 1, Hayet Gharbi 1, Mihai Ghita 8, Laura-Madalina Popescu 8 , Roxana Piticescu 8 and Dhafer Laouini 3,4 1 Laboratory of Epidemiology and Veterinary Microbiology (LEMV), Institut Pasteur de Tunis, LR11IPT03, Tunis-Belvédère 1002, Tunisia; [email protected] (S.B.J.); [email protected] (K.B.); [email protected] (H.G.) 2 Campus Universitaire Farhat Hached B.P. n◦ 94-ROMMANA, Université Tunis El Manar, Tunis 1068, Tunisia 3 Faculté des Sciences de Tunis, Campus Universitaire, El Manar, Tunis 2092, Tunisia; [email protected] 4 Laboratory of Transmission, Control and Immunobiology of Infections (LTCII), Institut Pasteur de Tunis, LR11IPT02, Tunis-Belvédère 1002, Tunisia 5 Laboratory of Improvement and Development of Plant and Animal Production (ADPVA), Sétif 19000, Algeria; [email protected] 6 Faculty of Sciences, University of Sétif, Sétif 19000, Algeria 7 Faculté des Sciences de Bizerte, Université de Carthage, Bizerte 1054, Tunisia 8 National R&D Institute for Non-Ferrous and Rare Metals, INCDMNR-IMNR, 102 Biruintei Blvd, Pantelimon, 077145 Ilfov, Romania; [email protected] (M.G.); [email protected] (L.-M.P.); [email protected] (R.P.) * Correspondence: [email protected] (M.F.D.); [email protected] (M.S.) † Co-first author: These authors contributed equally to this work. Citation: Diouani, M.F.; Sayhi, M.; Djafar, Z.R.; Ben Jomaa, S.; Belgacem, Abstract: Quality and food safety represent a major stake and growing societal challenge in the K.; Gharbi, H.; Ghita, M.; Popescu, world. Bacterial contamination of food and water resources is an element that pushes scientists L.-M.; Piticescu, R.; Laouini, D. to develop new means for the rapid and efficient detection and identification of these pathogens. Magnetic Separation and Conventional detection tools are often bulky, laborious, expensive to buy, and, above all, require Centri-Chronoamperometric an analysis time of a few hours to several days. The interest in developing new, simple, rapid, and Detection of Foodborne Bacteria nonlaborious bacteriological diagnostic methods is therefore increasingly important for scientists, Using Antibiotic-Coated Metallic Nanoparticles. Biosensors 2021, 11, industry, and regulatory bodies. In this study, antibiotic-functionalized metallic nanoparticles were 205. https://doi.org/10.3390/ used to isolate and identify the foodborne bacterial strains Bacillus cereus and Shigella flexneri. With bios11070205 this aim, a new diagnostic tool for the rapid detection of foodborne pathogenic bacteria, gold nanoparticle-based centri-chronoamperometry, has been developed. Vancomycin was first stabilized Received: 13 May 2021 at the surface of gold nanoparticles and then incubated with the bacteria B. cereus or S. flexneri to Accepted: 15 June 2021 form the AuNP@vancomycin/bacteria complex. This complex was separated by centrifugation, Published: 23 June 2021 then treated with hydrochloric acid and placed at the surface of a carbon microelectrode. The gold nanoparticles of the formed complex catalyzed the hydrogen reduction reaction, and the generated Publisher’s Note: MDPI stays neutral current was used as an analytical signal. Our results show the possibility of the simple and rapid with regard to jurisdictional claims in detection of the S. flexneri and B. cereus strains at very low numbers of 3 cells/mL and 12 cells/mL, published maps and institutional affil- respectively. On the other hand, vancomycin-capped magnetic beads were easily synthesized and iations. then used to separate the bacteria from the culture medium. The results show that vancomycin at the surface of these metallic nanoparticles is able to interact with the bacteria membrane and then used to separate the bacteria and to purify an inoculated medium. Copyright: © 2021 by the authors. Keywords: centri-chronoamperometry; biosensor; nanoparticles; foodborne bacteria; antibiotic Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 1. Introduction Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ Foodborne infectious diseases represent some of the most common public health 4.0/). problems that generate an enormous social and economic burden worldwide [1,2]. These Biosensors 2021, 11, 205. https://doi.org/10.3390/bios11070205 https://www.mdpi.com/journal/biosensors Biosensors 2021, 11, 205 2 of 15 diseases are mostly linked to the existence of microorganisms and toxins in food and water [3]. Over 250 different foodborne illnesses that can lead to severe diarrhea, debil- itating infections, severe poisoning, long-term illness, lasting disability, or even death have been identified [4]. Thus, pathogens causing such diseases represent a real source of human suffering. In 2017, bacterial agents were found to be responsible for the most reported food- borne (including waterborne) outbreaks in the European Union, with 50.4% of the total outbreaks. Specifically, 34.3% of the outbreaks were due to bacteria, 16.1% were caused by bacterial toxins, while 7.8%, 3.6%, and 0.6% implicated viruses, other causative agents, and parasites, respectively [5]. In addition, it has been reported that 1.6 million people died from diarrheal dis- eases in 2016 globally, and around half a million of them are children aged 5 years and younger. A large proportion of these cases is attributed to the contamination of food and drinking water [6]. B. cereus and Shigella are tremendous etiological agents of human diarrheal syndrome worldwide [7,8]. B. cereus are spore-forming Gram-positive bacteria that are capable of forming endospores and producing enterotoxins, responsible for the diarrheal syndrome, and emetic toxins, the causative agents of the emetic syndrome [9]. However, Shigella are non-spore-forming Gram-negative bacteria that cause a disease called Shigellosis or bacil- lary dysentery, which is responsible for 165 million diarrheal episodes and 600,000 deaths each year worldwide [10,11]. The latter are highly transmissible pathogens, and some of their strains can cause active infections in humans with exposure to only 10 cells [8,12]. Hence, there is a need to find ways to detect these bacteria at very low doses. Certain conventional and modern diagnostic tools are described as inexpensive and provide both qualitative and quantitative information on the tested microorganisms. How- ever, these tools are above all limited by the duration or the time suitable for the identifica- tion of pathogens, as well as by the sensitivity and the high detection limit [13–15]. Advances in technology and technical revolutions have enabled the development of new tools that largely meet current medical requirements. Biosensors are devices that detect a biological or physiological event and convert it into a measurable, quantifiable, and easy-to-use physical signal [16,17]. In the health field, these biosensors have multiple applications, in particular for the rapid detection and identification of pathogens at early stages of infection. To this end, many biosensors have been reported for the rapid and sensitive detection of foodborne bacteria and other pathogens [18,19]. Recently, nanotechnology has played a very important role in the improvement of these miniature biosensing systems. The introduction of nanomaterials into biosensors has remarkably improved the sensitivity, specificity, and selectivity of these devices [20,21]. In addition, these nanomaterials have reduced the required time to detect pathogens and have eliminated cumbersome steps in the diagnostic process [22–24]. Metallic nanoparticles have been proposed for these biomedical purposes [25]. During recent years, both gold and magnetic nanoparticles have been coupled with various biological molecules, including different types of antibiotics [26–30]. Equally, with their good biocompatibility, the unique physical, chemical, optical, and electrical properties of these materials have increased their range of applications [25,31–34]. The superparamagnetic propriety of iron oxide nanoparti- cles makes them a good candidate in many applications such as drug targeting, pathogen and toxin separation, and media purification [35–37]. Likewise, gold nanoparticles were widely used in cell targeting and labeling and pathogen detection based on their optical properties and electrochemical catalytic activity [38–40]. In the present study, antibiotic-coated iron oxide magnetic nanoparticles were em- ployed in order to easily extract and separate foodborne bacteria, to concentrate them in small volumes, and, by consequence, to assess the purification process of bacteria- inoculated liquid media. Separately, vancomycin-coated gold nanoparticles were employed to develop a centri-chronoamperometric assay for the rapid and easy detection of two foodborne bacterial strains, B. cereus and S. flexneri. This system is of great interest in the Biosensors 2021, 11, 205 3 of 15 bacterial sensing field, taking advantage of the ability of vancomycin at the surface of the nanoparticles to interact with a broad range of Gram-positive and Gram-negative bacteria. The use of gold nanoparticles allowed the easy and rapid labeling of bacteria in suspension with electrochemical detectable materials.
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