Food spoilage is a major health problem in the world due to the presence of foodborne disease germs. Food contamination includes two approaches in the food industry, one of them is linked to environmental conditions such as irrigation water system, infected animals. Whereas, another approach is related to the industrial processes (Scallan et al., 2011; Xu and Sun, 2013). According to the US Centers for Disease Control and Prevention (CDC), Escherichia coli and Salmonella typhimurium are most common foodborne diseases, the statistics refer that millions of people in the United States are sicked each year and approximately 450 deaths annually (McNicholl et al., 2007). Antibiotic resistance is a significant problem in the medical section. It has an adverse effect on people’s health. Also, it causes a massive economic loss (Bush et al., 2011). Nowadays, scientists are focusing on developing a novel antibiotic by applying various approaches (Czaplewski et al., 2016; Naylor et al., 2018; Alkawareek et al., 2019). Some bacterial strains formed an adhesion biofilm on synthetic surface which led to form a slime. The biofilm prevented the antibiotic action due to the bacterial resistance (Inbaraj et al., 2012; Dwivedi et al., 2014). Nanomedicine has had a magnificent role in medical applications in the last decade (Brollo et al., 2014). Silver nanoparticles are classified as highly effective bactericides against a broad spectrum of bacteria (Sotiriou and Pratsinis, 2010; Badrelden et al., 2018; Yin et al., 2020). Silver nanoparticles enhance the release of silver ions, which cause the antibacterial activity (Mahdavi et al., 2013). Metal oxide nanoparticles such as titanium dioxide nanoparticles, zinc oxide nanoparticles, and magnetic oxide nanoparticles have antibacterial properties (Hassan et al., 2021). Magnetic nanoparticles (MNPs) also have distinct properties such as biocompatibility, chemical stability, and magnetic properties (Arakha et al., 2015a). By using an external magnetic field, MNPs are applied in molecular target therapy (MTT). Also, MNPs have antibacterial properties due to their ability to produce reactive oxygen species (ROS; Seil and Webster, 2012). Silver magnetic core shell nanoparticles have unique properties such as biocompatibility with chemical stability and higher toxicity against bacteria than Ag-Fe₂O₃ heterdimers or plain Ag (Arakha et al., 2015b). Nanosize is characterized by its small size with a high surface area to volume ratio. Hence, the nanoparticle’s high Photoactivity leads to an increase in the production of ROS (Mikhaylova et al., 2004; Garza-Navarro et al., 2010). Recently, scientists have recently become interested in core/shell nanoparticles because of their unique properties and potential applications in a variety of fields, including semiconductor electronic and biomedical applications (Cho et al., 2005), Magnetic resonance imaging for diagnostic and thermal therapies (Cho et al., 2005), drug target therapy (Asmatulu et al., 2005), chemical sensors (Cho et al., 2005), and high-density magnetic recording (Yamaura et al., 2002) are a few examples. Metal-oxide/metal nanoparticles with regulated dimensions are difficult to produce.

Preparation of water-soluble magnetite/silver nanoparticles improves biocompatibility and chemical stability by preventing further oxidation of the magnetic core. In the work, we synthesize silver nanoparticles, magnetite nanoparticles, and silver magnetite core-shell nanoparticles and characterize them all. Then, investigated their antibacterial activity, and the kinetics of inhibitory mechanism against S. typhimurium (ATCC14028) and E. coli (ATCC35218).

Recently, foodborne pathogens are considered a major problem, causing food spoilage all around the world. Food contamination can occur during the food processing steps in the food industry, either by direct or cross contamination (Scallan et al., 2011; Xu and Sun, 2013). There are two sources of contamination: during the industrial process by washing water or soiled worker hands or irrigation water, animals, or pathogens exiting the soil. Escherichia coli and Salmonella are the most common foodborne pathogens that cause diseases. According to the US Centers for Disease Control and Prevention (CDC) data, there are millions of people suffering from diseases in the United States due to foodborne pathogens (McNicholl et al., 2007). Antibiotic activity is limited due to the formation of biofilm on the surface. The formation of bio-film on the surface is due to the adherence of bacteria on the surface by van der Waals, hydrogen bonds, and electrostatic forces. Noble nanometal is a major common anti-bacterial drug due to its unique features such as small size, wide surface area, and toxicity against many bacteria strains (Bush et al., 2011).

The interaction of metal-based nanoparticles with bacterial envelopes results in good bactericide performance and penetrates bacterial cell walls and membranes, resulting in bacteriostatic and bactericidal effects (Ma et al., 2022). The application of metal-based nanoparticles as antibacterial agents is a new approach to minimize microbial resistance and toxicity to human cells (Alabresm et al., 2021).

Silver nanoparticles are considered an active antimicrobial agent due to their ability to liberate silver ions that kill microbial cells. Also, magnetite nanoparticles are considered a good anti-bacterial agent due to their excellent properties, such as biocompatibility, chemical stability, and antimicrobial activity. Ag@Fe₃O₄ -NPs combine the benefits of both silver and magnetite nanoparticles and can be used in the medical field.

The combination of MNPs and silver nanoparticles improves the silver’s biocompatibility and eliminates its contact with the cells. Ag@Fe₃O₄ -NPs has a higher bactericidal efficiency than Ag-Fe₂O₃ heterodimers or simple Ag. Previous studies mentioned the activity of silver/iron oxide nanoparticle compacts and their antibacterial properties. Bi-functional Fe₃O₄@Ag nanoparticles were synthesized by utilizing the water-in-oil microemulsion approach to reduce AgNO₃ on the surface of Fe₃O₄ nanoparticles. The bi-functional Fe₃O₄@Ag nanoparticles were approximately 20 nm in size (Gabrielyan et al., 2020). Also, silver nanoparticles synthesized by an electrochemical method and citric acid-coated iron oxide against E. coli wild type and S. typhimurium MDC1759, comparing the antibacterial activity of Ag-NPs and Fe₃O₄ nanoparticle coating with citric acid (Alabresm et al., 2021). Also, citric acid has antibacterial efficiency (Padilla-Cruz et al., 2021).

Padilla et al. reported that Ag-Fe bimetallic nanoparticles were synthesized by using an aqueous extract from the leaves of Gardenia jasminoides. In this study, as Figure 9 displayed the schematic steps of this study. Firstly, Ag@Fe₃O₄ -NPs were prepared by using an efficient, economical, and environmentally friendly method. The method depends on co-precipitation of the Fe⁺²/Fe⁺³ with molar ratios of 2/3 by using ammonia solution instead of NaOH in the absence of nitrogen gas (Mascolo et al., 2013; Hassan et al., 2019). The function of an ammonia solution is to combine with H₂O and dissociate into ammonia gas and hydroxide ions, which then precipitate magnetite. Whenever ammonia gas gives nitrogen to the atmosphere; it prevents oxygen from oxidizing iron salts into hematite (Lara et al., 2010). Ag@Fe₃O₄ -NPs a magnetite core nanoparticle surrounded by a silver cloud with a controlled shape, and investigated its antibacterial activity against the most common foodborne pathogens. Silver magnetite core shell nanoparticles have a cubic core with a diameter of 3 nm surrounded by a silver shell with a diameter of 25 nm, which emphasizes the formation of silver magnetite core shell nanoparticles with regular morphologies and without any aggregates. Secondly, the bacterial activity was evaluated using the Resazurin dye (Michels et al., 2017). The results showed that Ag@Fe₃O₄ -NPs were more effective than magnetite and silver nanoparticles against E. coli and S. typhimurium. The results showed that E. coli was less vulnerable to all of the testing materials than S. typhimurium due to the lipopolysaccharide blockage (Michels et al., 2017). In addition, the kill time assay revealed that Ag@Fe₃O₄ -NPs nanoparticles are more effective than Ag-NPs and MNPs against Gram-negative bacteria strains.

The antibacterial mechanism of Ag@Fe₃O₄ -NPs is based on two methods. The first is based on the action of free silver ions. The cell membrane is a built-up of protein and lipids. Silver ions can interact with proteins to form complexes with molecules containing oxygen, phosphorus, sulfur, or nitrogen atoms, which inactivate the membrane-bound proteins and enzymes. Previous studies reported that silver particles can bind to unsaturated fatty acids on the cell membrane and alter their dynamic function, which alters membrane permeability and integrity (Piao et al., 2011). Michels et al. mentioned that nanomaterials such as silver and magnetite nanoparticles investigated against ammonia-oxidizing bacteria adsorb continuously on the outer surface of the microbial cell membrane until the morphology of the surface layer is entirely destroyed (Michels et al., 2017). The amorphous thin porous oxide shell of Ag@Fe₃O₄ -NPs makes it easier to liberate silver ions from the outer silver surface, particularly Ag-NPs (Dakal et al., 2016).

The antibacterial activity of silver nanoparticles depends on the shape and size of the nanoparticles. Smaller sizes of silver nanoparticles within the size range of 5–10 nm can cause cell membrane damage and degradation of the bacterial chromosome (Alavi and Rai, 2021). Additionally, ROS is considered a major mechanism of toxicity in vitro and vivo generated by metal-based NPs such as noble metals and metal oxide NPs (Alavi et al., 2022). For instance, CuO and Ag-CuO-NPs in a spherical shape with a diameter of 18 and 20 nm, inhibited S. aureus with inhibition zones of 19 and 15 mm, respectively. Moreover, cleavage of pBR 322 DNA was observed at high levels for CuO-NPs relative to Ag-CuO NPs (Jadhav et al., 2018).

Interestingly, silver nanoparticles can penetrate the bacterial cell wall, where they contribute to the creation of free radicals and the generation of ROS, which leads to cell death. Similarly, silver ions released from nanoparticles into the cytoplasm might cause oxidative stress, causing dispersion in membrane morphology. As a result, silver can alter cellular architecture and intracellular biological processes, ultimately leading to death (Auffan et al., 2009). Iron may also interact with particular amino acids (–SH groups of cysteine) that are found in bacterial cell wall proteins (Auffan et al., 2009). Piao et al. reported that the breakdown of the mitochondrial membrane is the primary cause of apoptosis (Piao et al., 2011). Our data showed that after 12 h of exposure to Ag@Fe₃O₄ -NPs, apoptosis increased in a concentration-dependent manner. As shown in Equations 2, 3, ROS production is followed by the Fenton reaction, or the Haber-Weiss cycle, which accelerates the synthesis of H₂O₂ and causes DNA and protein damage. Also, as shown in Equations 1, 2, the presence of the magnetite species Fe⁺² and Fe⁺³ in the culture media activates the formation of ROS according to the Haber-Weiss cycle. According to our data, the formation of reactive oxygen species is concentration and time-dependent.

In the present study, Ag/Fe₃O₄ core shell NPs, Ag-NPs, and Fe₃O₄ NPs were synthesized by wet chemical reduction and co-precipitation methods and characterized by physiochemical techniques such as X-ray diffraction (XRD), Dynamic Light Scattering (DLS), Transmission electron microscopy (TEM), and Atomic Force Microscopy (AFM). The antibacterial efficacy of all the testing materials was evaluated by using the Kirby–Bauer Disk Diffusion test, MIC, MBC, CFU, and Killing Kinetics assays against S. typhimurium and E. coli, which were chosen as Gram-negative foodborne pathogens. Furthermore, the cytotoxicity mechanism of Ag/Fe₃O₄ core shell NPs was investigated using flow cytometer analysis and apoptosis and ROS assays. The results showed that Ag/Fe₃O₄ core shell NPs with a diameter of 3 nm were synthesized with a cubic core surrounded by a silver shell of 25 nm, confirming the production of silver magnetite core shells with regular morphologies and no aggregation. MIC values for Ag/Fe₃O₄ core shell NPs against S. typhimurium and E. coli were 3.1 and 5.4 μg/ml, respectively, whereas the MIC values for Ag-NPs and MNPs against S. typhimurium and E. coli were 4.1, 8.2 μg/ml for Ag-NPs and 6.9, 10.3 μg/ml for MNPs. CFU measurements revealed that Ag/Fe₃O₄ core shell NPs reduced S. typhimurium and E. coli viability by 19 and 35%, respectively. Also, the kill time test indicated that Ag/Fe3O4 core shell NPs reached a number of CFU/mL of 3 log units (99 percent) to zero value at 2xMIC (10.8 μg/ml) and 4xMIC (21.6 μg/ml) after 2 h of treatment with testing materials. Furthermore, the data revealed that the Ag@Fe₃O₄-NPs core shell nanoparticles’ ability to induce apoptosis and ROS in S. typhimurium and E. coli was concentration and time dependent. The antibacterial activity of silver nanoparticles depends on the shape and size of the nanoparticles. Smaller sizes of silver nanoparticles within the size range of 5–10 nm can cause cell membrane damage and degradation of the bacterial chromosome. In addition, ROS is considered a major mechanism of toxicity in vitro and vivo when generated by metal-based NPs such as noble metals and metal oxide NPs such as Fe₃O₄-NPs. The capacity of Ag@Fe₃O₄ -NPs core shell nanoparticles to release free silver ions and form reactive oxygen species via the Fenton reaction, or Haber-Weiss cycle, was shown to be a plausible mechanism for explaining the toxicity of silver/magnetite core shell nanoparticles. Finally, the compact Ag@Fe₃O₄-NPs core shell nanoparticles exhibit higher antibacterial activity than silver nanoparticles and magnetite nanoparticles against Gram-negative foodborne pathogens.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

ES: conceptualization and supervision. ES and AH: formal analysis, validation, visualization, and writing-original draft. FA-S, EF, and ES: funding acquisition. AH, FA-S, and ES: investigation. ES, FA-S, AH, and EF: methodology. ES and EF: project administration. FA, EF, and ES: resource. AH, DD, and FA: writing—review edition. All authors contributed to the article and approved the submitted version.

This work was fully supported by Taif University Researchers supporting project number (TURSP-2020/113), Taif University, Saudi Arabia.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.