Influential eradication of resistant Salmonella Typhimurium using bioactive nanocomposites from chitosan and radish seed-synthesized nanoselenium

Haddad A. El Rabey; Rehab F. Almassabi; Ghena M. Mohammed; Nasser H. Abbas; Nadia Bakry; Abdullah S. Althiyabi; Ibrahim H. Alshubayli; Ahmed A. Tayel

doi:10.1515/gps-2024-0090

Article Open Access

Influential eradication of resistant Salmonella Typhimurium using bioactive nanocomposites from chitosan and radish seed-synthesized nanoselenium

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Published/Copyright: September 12, 2024

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From the journal Green Processing and Synthesis Volume 13 Issue 1

Abstract

Biosynthesized nanomaterials and nanocomposites (NCs) could have promising potentialities to overcome the multi-drug-resistant (MDR) pathogenic bacteria, particularly Salmonella Typhimurium. Radish seed (Raphanus sativus) mucilage (RSM) was employed for synthesizing/capping selenium nanoparticles (SeNPs) and their nanoconjugates with chitosan (Ct) were assessed for inhibiting MDR S. typhimurium. The SeNPs were effectually biosynthesized using RSM and have 4.21 nm mean size and −25.6 mV surface charge. Different NC formulations of Ct/RSM/SeNPs were generated and validated using infrared spectroscopy and electron microscopy. The entire formulations could suppress S. Typhimurium growth, including MDR strains. F3 NCs (with 53.64 nm diameter and +21.1 mV surface charge) had the strongest anti-S. Typhimurium activity that exceeded the action of cephalosporin, and the subsequent antibacterial formulation was F2 (with 41.77 nm diameter and −17.3 mV charge). The NCs of Ct/RSM/SeNPs could severely destruct, deform, and lyse S. Typhimurium cells’ structures throughout 10 h of exposure. The innovative fabricated NCs of Ct/RSM/SeNPs are auspiciously suggested as effectual biocides to eradicate MDR S. Typhimurium in various food-processing facilities.

Keywords: antibacterial; bacterial pathogens; biopolymers; biosynthesis; nanomaterials

1 Introduction

Illnesses from bacterial infections lead to ∼35% of human mortalities worldwide; prevention of such infection outbreaks is with great prominence, as these microorganism types are plentiful and the infection dosages are low [1]. From the several identified Salmonellae serovar types (>2,610 serovar), human infections with Salmonella Typhimurium serotype were the most frequent [2]. The multi-drug-resistant (MDR) emergence in S. Typhimurium became significantly a serious health concern. The leading contributing factors in widespread MDR S. Typhimurium emergence are the misuse and indiscriminate therapeutic/prophylactic uses of accustomed antimicrobials within humans, animals, and foodstuffs [3].

The investigation of MDR microbes advocated the exploration of nature-derived sources to generate more effectual and combined antimicrobial that can hinder these pathogens, such as plant derivatives, biopolymers, bionanocomposites, and phytocompounds [4,5,6]. Even the MDR pathogen will not resist a consortium of antimicrobial agents with diverse compositions/actions [4], although these composites are much safer for human usages.

The medicinal bioactivities of plants and their derived compounds are mainly depending on their functional metabolites/constituents, e.g., tannins, phenolics, terpenoides, flavonoids, and alkaloids [7]. The Brassicaceae family of plants comprises most of these constituents; the radish “Raphanus sativus Linn.” is the consumable annual herb that belongs to this family and possesses many folkloric medical and nutraceutical benefits [8]; almost all radish parts (e.g., leaves roots and seeds) are exploited in phytomedicine. The seeds of radish possess laxative, expectorant, carminative, diuretic, stomach tonic, and antitussive actions, which enable their employment in numerous biomedical disciplines, including anticancer, antidiabetic, antioxidant, diuretic, hypertensive, antifertility, hepatoprotective, nephroprotective, gastroprotective, and antimicrobial applications [8,9,10,11,12]. The radish seed extract and its polysaccharides contained many antimicrobial active compounds including isothiocyanates, sulforaphene, and sulfur compounds [13,14,15].

The composite materials, especially those based on biopolymers, have elevated potentialities for applications as antimicrobial agents and for removal of hazardous materials from water and environmental wastes [16,17,18,19,20].

Chitosan (Ct)-based nanocomposites (NCs) and nanoparticles (NPs) attracted much interest from researchers and industry overseers, attributed to the amazing bioactivities and biosafety of these biopolymers that derived from natural chitin [21,22,23,24]. The foremost characteristics of Ct and its based NCs are their capabilities to serve as potent antibacterial, antiviral, and antifungal molecules; these potentialities were much augmented with Ct nanocompositing with other biopolymers, phytocompounds, antibiotics, and nanometals, where Ct can promisingly their potential biotoxicities toward human [25,26,27,28,29,30,31]. The Ct-based NCs were furthermore counseled for the powerful control of MDR microbial pathogens, with exceeding activities than standard antibiotics [32,33].

Selenium is a vital element for human development (with a daily requirement of 30–300 µg), and the selenium nanoparticles (SeNPs) have prominent attributes than bulk metals as anticancer, antioxidant, antimicrobial, and growth-stimulant agents [34,35]. The synthesis of SeNPs is achievable through various protocols, but the biosynthesis (green synthesis) is much desirable for diminishing the NP biotoxicity, reducing the process cost, residual hazards, and energy saving [36,37,38,39]. The NC of biosynthesized SeNPs with further phytocompounds and biopolymers (e.g., Ct) can greatly increase the NCs’ biosafety, while this enhanced and enforced their antimicrobial potentialities, even against MDR microbes [1,30,39,40,41].

The application of radish mucilage for SeNP biosynthesis was not fully covered previously, and the nanoconjugation of these materials with nanopolymers was insufficiently investigated, for usage as antimicrobial composites.

Therefore, we targeted the extraction of radish seed mucilage (RSM), to inventively apply it for SeNP biosynthesis, to fabricate innovative bioactive NCs from Ct and RSM/SeNPs, and to assess their potentialities for suppressing MDR S. Typhimurium development.

2 Materials and methods

2.1 Materials

Dried seeds of organically farmed radish “R. sativus L. var. caudatus” were acquired from the ARC “Agricultural Research Center, at Giza, Egypt.” The used plants are edible and food-grade, which guarantees their biosafety for application. The entire certified employed chemicals, buffer, reagents, and microbiological media, in experiments, were procured, unless the further source is stated, from “Sigma-Aldrich Co.; St. Louis, MO.” According to the reported SDS “Safety Data Sheet” of employed compounds/reagents, most of the used materials are “Not a hazardous substance or mixture according to Regulation (EC) No 1272/2008.” Other potentially hazardous materials (e.g., sodium selenite) were handled as instructed by the manufacturer.

2.2 Extraction of RSM

The extraction of RSM from R. sativus seeds was slightly adapted [38,42]. First, the seeds were mildly crushed in a mortar, and then the hydration process was applied. Crushed seeds were soaked in double distilled water (DW) at 1:50 (w/v) ratio and stirred mechanically with a magnetic stirrer (Caframo Ltd, Ontario, Canada) at room temperature (RT; 25 ± 2°C) for ≥2 h. The formed mucilaginous solution was separated from seeds’ residues by centrifuging at 8,700 × g for 33 min “2‑16KL; Sigma Laborzentrifugen GmbH, Osterode am Harz, Germany”. Thereafter, the solution was vacuum filtered to eliminate any residual seed parts attached to mucilaginous gel. The resulting RSM mucilaginous gel was freeze-dried and stored at RT.

2.3 Biosynthesis of RSM/SeNPs

The protocol for SeNP bioreduction/mediation using RSM was adapted from a recent procedure [43]. First, aqueous Na₂SeO₃ (sodium selenite, 10 mM) and RSM (0.1%, w/v) solutions were individually prepared in DW at RT, through stirring at 245 × g for 70 min. Solutions were filtered via passing over a syringe (0.45 µm) filter, and 15 mL of RSM solution was dropped over equal amounts of selenite solution (while Na₂SeO₃ solution was stirred at 610 × g) for 95 min. A few drops (up to 20) of ascorbic acid solution (1.0%, w/v) were added gradually to the mixture solution to speed the synthesis process. The mix solution color was switched into brownish orange that could be seen visually, as an indication of RSM/SeNP formation. The fabricated NCs were gathered through 32 min of centrifugation at 10,200 × g, washed with DW, re-centrifuged, and freeze-dried. To achieve purified SeNP particles, the RSM/SeNP pellets were washed by DW and re-centrifuged five successive times, to mostly exclude the attached RSM.

2.4 NCs of Ct/RSM/SeNPs

The construction of targeted NCs from Ct/RSM/SeNPs employs the following steps [43]:

RSM/SeNP solution (0.1%, w/v) was made in DW.
Ct (≥85% deacetylation; ∼350 kDa; CAS 9012-76-4) solution (0.1%, w/v) was made in acetic acid (1.5%, v/v) aqueous solution.
Individually, solutions are sonicated for 17 min.
1.0% (w/v) of TPP (Na-tripolyphosphate) is appended into 20 mL of RSM/SeNP solution and dissolved via sonication.
Gently dropping the RSM/SeNP-TPP solution (∼20 mL·h⁻¹) into speedy stirred (740 × g) Ct solution to form the NCs, with the following formulations:

F1 (2 RSM/SeNPs: 1 Ct),
F2 (1 RSM/SeNPs: 1 Ct),
F3 (1 RSM/SeNPs: 2 Ct).

After dropping, stirring is continued for an additional 45 min.
The formulated NCs were gathered via centrifuging (10,520 × g), washed by DW, recentrifuged, and freeze-dried.

2.5 Nanomaterial/NC characterization

2.5.1 Fourier transform infrared (FTIR) spectroscopic analysis

Infrared (IR) spectroscopy was operated to analyze the potential involving biochemical bonds/groups in investigated materials/NCs and their probable interaction, comprising Ct, RSM, RSM/SeNPs, and Ct/RSM/SeNPs. After a combination of KBr with material/NC powders, the FTIR “FT-IR-360, JASCO, Japan” spectra are reviewed; their transmitting IR spectra were plotted within a wavenumber between 450 and 4,000 cm⁻¹ range.

2.5.2 Nanomaterial particles’ sizes (Ps) and zeta (ζ) charges assessment

The assembled nanomaterials/NCs (dissolved in DW and sonicated at 45 W for 18 min) were screened for distribution physiognomies (Ps and ζ potential), employing zetasizer “Malvern™, Worcestershire, UK” at RT, associated with DLS “dynamic light scattering” principles.

2.5.3 Transmission electron microscopic (TEM) and scanning electron microscopic (SEM) imaging

The TEM “Leica; Leo-0430; Cambridge, UK” and SEM “JEOL IT100, Tokyo, Japan” imaging explicated the NP/NC structure, distributions, and Ps. Aqueous suspensions (0.1%, w/v) of NPs/NCs (RSM/SeNPs, F1, F2, and F3) in DW were made and sonicated before inspection. The inspection of RSM-mediated SeNPs employed TEM; NP solution was dropped onto grids (copper), vacuum-dehydrated for ∼34 min, and then subjected to operated TEM at 20 kV. The screening of NC solutions employed SEM; NC solutions are mounted onto SEM discs (self-adhesive carbon), coated with palladium/gold “the coater: E5100 II, Polaron Inc., PA,” and inspected with acceleration of 10–15 kV.

2.6 Anti-Salmonella activity

2.6.1 Bacterial strains

Diverse strains of S. Typhimurium “Salmonella enterica ssp. enterica serovar Typhimurium” were employed for challenging, including the ATCC-700408 (MDR standard strain) and the isolates R and S (isolated from chef’s hands and kitchen surfaces, respectively). The isolates of S. Typhimurium were primarily identified using Gram stain, microscopic morphology, endospore formation, and catalase-oxidase reactions. Standardized procedures (ISO 6579-1:2017 and ISO/TR 6579-3:2014) were ensued for validating the S. Typhimurium identity [44,45]. Confirmation of strain identity was further done using (API) automated system “BioMérieux Vitek-II System, France” for profile index analysis, then using 16S rRNA assessment [46]. The R isolate displayed an MDR pattern toward tetracycline, ampicillin, sulfonamide, and streptomycin, whereas the S isolate was sensitive to most of these antibiotics. Culture was activated, propagated, and challenged, aerobically at 37 ± 1°C in nutrient agar and broth “NA and NB; Difco Lab., Detroit, MI.” Cephalosporin© was employed for comparing the efficacy of examined antimicrobial nanomaterials.

2.6.2 ZOI “inhibition zone” qualitative antibacterial assay

The S. Typhimurium strains were propagated in NB for 24–36 h at 37°C, and then 120 µL of grown bacterial cultures were spread onto plates of NA and individually confronted assay paper discs (with 6 mm diameter), which were impregnated with nanomaterial/NC solutions (25 µL of 10 mg·mL⁻¹ concentration). Individual discs were amended with Ct, RSM/SeNPs, and NCs (F1–F2–F3), and the challenge treatment was subjected to incubation for 30–35 h until the development of ZOIs around discs. These diameters of ZOIs as means were assessed and computed.

2.6.3 Quantitative minimum inhibitory concentration (MIC) measurement

The MICs of Ct, RSM/SeNPs, and NCs (F1–F2–F3) against screened S. Typhimurium strains were determined via “Micro-dilution” protocol [47]. Grown cultures of Salmonella in NB (∼2.8 × 10⁷ cells·mL⁻¹) were subjected to successively adjusted concentrations from individual agents/NCs (from 1.0 to 100 µg·mL⁻¹ concentration range) in 96-well microplates. The p-iodonitrotetrazolium violet (chromogenic indicator; 4% w/v) was employed for validating the MIC results. The MIC values express the least concentration from each agent/NC that inhibited particular strain development.

2.6.4 SEM remarks of NC-exposed S. Typhimurium bacteria

After contact of S. Typhimurium strain S and R to Ct/RSM/SeNPs (F3 formulation) in NB, at their corresponding MIC values, cells were incubated for 5 and 10 h, and the superficial morphological disparities after challenging were captured by SEM photographs. The exposed S. Typhimurium cells were collected through centrifuging (4,970 × g), washed using 0.9% NaCl saline buffer, dehydrated using gradual EtOH concentrations onto SEM stubs, coated (by gold/palladium), and inspected for instinctive distortion/deformation emergence.

2.7 Statistical analysis

The SPSS software “v17.0 package SPSS Inc., Chicago, IL, USA” computed the analysis of statistical data. SD “standard deviations” and means after triplicates’ assessments were calculated. The significances using t-tests and analysis of variance (one-way) were computed with p ≤ 0.05.

3 Results and discussion

3.1 Optical observation of RSM-synthesized SeNPs

The visual expression of SeNP synthesis with RSM and their UV-spectral analysis after 2 h of reaction is depicted in Figure 1. The transformation of interaction solution color (Figure 1a) from bale yellow (RSM) and colorless (Na-selenite) to deep brownish orange (RSM/SeNPs) directly indicated the NP formation [29,36,38]. The UV-spectral analysis of synthesized nanometals could give direct evidence about the synthesis process and effectiveness [29,38].

Figure 1

Biosynthesis of SeNPs using RSM, evidenced by visual observation (a) and UV analysis of synthesized NPs (b).

Furthermore, the maximum absorbance (λ-max) at 261 nm of the reaction solution color additionally validated SeNP biosynthesis, by the detected SPR “Surface Plasmon Resonance” that is distinctive to biogenic SeNPs, around 260–275 nm [37,48,49].

3.2 IR (FTIR) analysis

The FTIR spectral investigations were performed to pinpoint the key functional group/bonds that are involved in SeNP synthesis/capping with RSM and their nanoconjugates with Ct (Figure 2). The FTIR spectrum of Ct appointed the occurrence of main distinctive groups/bonds of standard Ct (Figure 2, Ct). The key Ct indicative peaks appeared around 3,390 cm⁻¹ (vibrated O−H and N−H stretching), 2,922 cm⁻¹ (vibrated C−H stretching), 1,700 cm⁻¹ (amide I stretched C═O), 1,664 cm⁻¹ (amide II vibrated N−H), 1,420 cm⁻¹ (vibrated –CH₂), 1,121 cm⁻¹ (vibrated −OH stretch of C3), 1,038 cm⁻¹ (vibrated −OH stretch of C6), 1,028 cm⁻¹ (stretched C═O), and 672 cm⁻¹ (vibrated −OH) [27,30,32,47].

Figure 2

Infrared (FTIR) analysis of chitosan (Ct), RSM, RSM-synthesized SeNPs (RSM/SeNPs), and the combined NC (Ct/RSM/SeNPs).

Regarding RSM analysis (Figure 2, RSM), the spectrum depicts an intense appeared band within 3,300–3,450 cm⁻¹, which corresponds to the functional hydroxyl group of alcoholic/phenolic compounds existing in RSM [50]. The peaks of 2,926 and 1,639 cm⁻¹ are attributed to the stretched C–H vibration of saturated hydrocarbons and amide I or vibrated C═O of proteins’ aromatic ring, respectively [50]. The peaks at 1,518, 1,435, 1,259, 1,051, and 805 cm⁻¹ mainly correspond to both C–N stretching and N–H bending of amide II [51]; bending C–H, stretched C–N vibration of primary amine [27]; aliphatic amine groups; and alkylated halides, respectively [9].

However, the reduction of Na-selenite via RSM led to the SeNP formation and exhibited many shifts in RSM spectral peaks as revealed in Figure 2, RSM/SeNPs. Numerous peaks disappeared/shifted in the RSM/SeNP spectrum, after the reduction of SeNPs with RSM. These peaks were mainly positioned within 2,980–35,500 cm⁻¹, within 1,700–1,750 cm⁻¹, within 1,220–1,350 cm⁻¹, and within 520–980 cm⁻¹, which indicated the occupation of disappeared bonds with the newly synthesized SeNPs [40,47,48]. Additionally, several bands emerged or had more intensity after conjugation of SeNPs with RSM, e.g., within 3,630–3,810 cm⁻¹, within 2,770–2,940 cm⁻¹, within 1,420–1,610, and within 1,100–1,190 cm⁻¹, which appointed the formation/development of additional bonds between SeNPs and RSM biomolecules [30,36,39]. The SeNPs’ conjugation with RSM resulted in more stretching of the hydroxyl group –OH or the amino groups –NH bands located around 3,400 cm⁻¹ [52]. The blue zones appoint the disappeared peaks, whereas the red zones are the emerged peaks after SeNP synthesis by RSM (RSM/SeNPs), compared to the RSM spectrum.

The nanoconjugation between Ct and RSM/SeNPs generated biochemically bonded NCs, as evidenced by their FTIR spectrum (Figure 2, Ct/RSM/SeNPs). The spectrum has most of the RSM/SeNP distinctive beaks in addition to numerous bands that were allocated from Ct bonds (appointed with yellow zones in the figure). The nanoconjugation and positioning of diverse molecules from Ct and interacting nanomaterials/biopolymers were stated formerly during the synthesis of Ct-based NCs, as an indication of successful NC formation [27,40].

3.3 Nanomaterial physiognomies

The produced nanomaterials (RSM/SeNP and Ct/RSM/SeNP NCs; F1, F2, and F3) were characterized using electron microscopy (Figure 3) and DLS analysis (Table 1), which appraised the morphology and structural characteristics of employed materials and fabricated NCs. The evaluation of the DLS pattern could give a direct relation to NPs size, charge, and distribution, whereas the electron microscopy imaging illustrates the exact figures of synthesized nanomaterials.

Figure 3

TEM Electron microscopy imaging of synthesized SeNPs by RSM (a), and imaging of chitosan/RSM/SeNPs NCs using scanning (b) and transmission (c) microscopy.

Table 1

Size and charges of synthesized materials/NCs including chitosan, RSM, RSM-synthesized SeNPs, and their composites

Material/composite	Size range (nm)	Mean size (nm)	Charge (mV)
Ct	>1,000	>1,000	+28.7
RSM	>1,000	>1,000	−18.9
SeNPs	0.81–18.36	4.21	−25.6
Ct/RSM/SeNPs (F1)	26.22–151.62	65.58	−23.5
Ct/RSM/SeNPs (F2)	16.95–83.47	41.77	−17.3
Ct/RSM/SeNPs (F3)	22.61–162.12	53.64	+21.1

The plain polysaccharides (Ct and RSM) had Ps of >1,000 nm, Ct was positively charged (+28.7 mV), whereas RSM and SeNPs were negatively charged (Table 1). Both electron microscopy imaging and DLS assessment provided matching outputs regarding nanomaterials Ps. The RSM-synthesized SeNPs appeared with spherical, well-distributed shapes, with mean Ps diameter of 4.21 nm, which highlights the superiority of RSM to reduce/cap/stabilize SeNPs. The formulated NCs (F1, F2, and F3) had disparate Ps distribution and zeta potentialities; F2 had the least Ps mean (41.77 nm). The F3 NCs were the only formulation that carried positive charges, whereas F1 and F2 were negatively charged (Table 1); this correlates with the ratio of Ct in the NCs. The increased ratio of Ct in F3 (2 Ct: 1 RSM/SeNPs) supports the positive charges to be the dominant on the NCs. The electron microscopy images of the F2 NCs illustrate the homogenous distribution of particles; the SEM image (Figure 3b) of Ct/RSM/SeNP NCs indicated the semi-spherical morphology of fabricated NCs, with homogenous size and distribution. Additionally, the TEM image (Figure 3c) of the NCs clearly emphasizes the occurrence of SeNPs within the Ct/RSM matrix, with consistent spreading.

The RSM was verified here as an effectual precursor for SeNP reduction and capping, and the radish seed extract was formerly investigated and effectually employed for the synthesis of silver nanoparticles (AgNPs) [50,52]; they attributed this to the existence of diverse biomolecules (e.g., flavonoids, phenolic compounds, enzymes, and proteins), in RSM. These biomolecules and constituents are the assumed factors for SeNP biosynthesis/capping. Additionally, the antioxidant potentiality of RSM was evidenced [10,53], which could have a potential role in nanometals reduction and synthesis.

The interaction between positively charged Ct and negatively charged RSM/SeNPs molecules imposed the effectual synthesis of NCs, which is supported by former observations [6,27,47], which fabricated NCs from Ct conjugation with oppositely charged biopolymers (e.g., cress mucilage and Na-alginate). This validated the nanocompositing process depending on the direct interaction between biopolymers with contrary particles’ charges, where Ct is the standard positive biopolymer to be employed in such a protocol [47].

3.4 Anti-Salmonella Typhimurium activity assessments

The antibacterial assays of NPs/NCs against S. Typhimurium strains involved the qualitative methods (e.g., ZOI) that appoint the potentiality of nanomaterials to suppress bacterial development, the quantitative assay (e.g., MIC) that quantifies the needed concentrations to kill the bacteria, and the electron microscopy imaging that screens the destructions in bacterial cells after exposure to nanomaterials. The bacterial inhibitory actions of entire compounds/NCs were proved against all challenged S. Typhimurium strains; NCs (F1, F2, and F3) have significantly stronger biocidal actions than their parental components (Table 2). The strongest antibacterial formulated NC was F3, considering the MIC and ZOI values of NCs; the F3 antibacterial action significantly exceeded cephalosporin (standard antibiotic), especially toward S. Typhimurium-resistant strains (R and A). The subsequent powerful materials/NCs were the F1, F2, SeNPs, RSM, and Ct, respectively. S. Typhimurium S had the highest susceptibility to the entire agents/NCs, whereas S. Typhimurium R was more resistant to them (Table 2). Therefore, the synergistic action between RSM, Ct, and SeNPs could be claimed. The strongest antibacterial action of F3 from Ct/RSM/SeNPs could be attributed to the abundance of Ct in the formulation and its net positive charge, which facilitates its interactions with negative bacterial cells. The antibacterial potentiality of F1 formulation can be attributed to the forceful power of RSM/SeNP complex.

Table 2

Antibacterial activity of synthesized materials/NCs including chitosan, RSM, RSM-synthesized SeNPs, and their composites against Salmonella Typhimurium strains*

Material/composite	Salmonella Typhimurium R		Salmonella Typhimurium S		Salmonella Typhimurium A
Material/composite	ZOI	MIC	ZOI	MIC	ZOI	MIC
Ct	11.5 ± 0.7^a	85.0	12.9 ± 1.6^a	75.0	12.1 ± 2.1^a	77.5
RSM	14.9 ± 0.9^b	62.5	15.5 ± 2.1^b	57.5	16.1 ± 1.6^b	57.5
SeNPs	19.6 ± 1.7^c	55.0	23.2 ± 2.3^c	50.0	22.4 ± 2.4^c	52.5
Ct/RSM/SeNPs (F1)	29.2 ± 1.8^d	37.5	36.4 ± 3.1^d	30.0	32.8 ± 3.2^d	35.0
Ct/RSM/SeNPs (F2)	26.8 ± 2.3^d	42.5	33.7 ± 3.3^d	37.5	30.3 ± 2.2^d	37.5
Ct/RSM/SeNPs (F3)	33.2 ± 3.1^e	32.5	39.1 ± 2.9^d	22.5	38.4 ± 2.6^e	27.5
Cephalosporin	27.6 ± 1.3^d	45.0	34.3 ± 1.7^d	32.5	30.8 ± 1.8^d	42.5

*Dissimilar letters (superscript) inside one column indicate significant differences at p ≤ 0.05.

Many studies stated analogous antimicrobial synergism between Ct and other biopolymers and nanometals including garden cress mucilage, collagen, alginate, curcumin, SeNPs, and silver NPs [29,33,39,54]. However, the current study is leading to explore the antimicrobial synergism between Ct, RSM, and SeNPs.

Ct (the highly bioactive, biodegradable, biocompatible, and non-toxic natural biopolymer) has potently recorded bactericidal/bacteriostatic actions, which were proved in many reports [25,55,56]. The interactions (electrostatically) between highly Ct cationic structure and the negative constructions of microbial cells (e.g., cell walls, enzymes, DNA, proteins) could disrupt cells’ integrity, membranes’ permeability, DNA replication, and physiological bioactivities, leading to cells inactivation and death [56,57]. Ct can also act for binding/chelating trace essential elements that could distress microbial growth [25,28]. The Ct NPs and Ct-based NCs have stronger antimicrobial potentialities than bulk Ct; they can serve as bioactive carriers for further antimicrobial agents (e.g., antibiotics, phytochemicals, and nanometals), to facilitate their entrance and interactions with microbial membranes/interior components [31,36,58,59].

Regarding the RSM, it was reported that there are numerous types of isothiocyanate (ITC) (e.g., allyl-ITC, phenyl-ITC, benzyl-ITC, phenethyl-ITC, and 4-(methylthio)-3-butenyl-ITC), which possessed potent antibacterial activities against multiple pathogenic and resistant bacteria, including Escherichia coli, Staphylococcus epidermidis, Bacillus subtilis, Enterococcus faecalis, Staphylococcus aureus, Enterobacter aerogenes, Salmonella Typhimurium, and Enterobacter cloacae [13,60,61]. The sulforaphene bioactive molecule was an interesting extracted ITC from RSM and exhibited exceptional antibacterial actions against drug-resistant bacteria like Helicobacter pylori and S. aureus [11,15]. The crude extracted substances from RSM were addressed to have considerable antimicrobial effectiveness against all challenged pathogenic microbes [14].

The phenols and phenolic derivatives are also from the frequently detected bioactive defensive and antimicrobial compounds in extracts of cruciferous plants, including radish, which protect plants from microbial attack [8,62].

The nanometals that are biosynthesized using phytocompounds (e.g., SeNPs) possess influential bactericidal potentialities, chiefly depending on ROS “reactive oxygen species” generation and subsequent cytotoxicity toward cells via inactivation and interaction with microbial metabolic pathways [31,34]. The nanoconjugation of such nanoparticles (SeNPs) with enveloping biopolymer systems can impressively lessen their biotoxicity toward mammal cells, whereas it favorably sustains/reinforces their antimicrobial bioactivities toward pathogens [36,47].

For a feasible explanation of Ct/RSM/SeNP antibacterial actions (formulation F3), SEM imaginings were captured for subjected S. Typhimurium R and S cells to NCs after 0, 5, and 10 h (Figure 4). The cells in the treatment of zero-time existed with healthy, natural, smooth, and contacted structures, with no deformation/distortion signs (Figure 4, R0 and S0). After 5 h of exposure to NCs, remarkable cellular deformation and distortion indicators appeared on bacterial walls, the cells of the S isolate were swollen and shrunken in size (Figure 4-S5), whereas the R cells began to lyse and lost their integration (Figure 4, R5). The distortions, lysis, and deformations of both strain cells were very observable after Ct/RSM/SeNP exposure for 10 h (Figure 4, S10 and R10), the NCs appeared combining to distorted cells’ residues; the distortion signs were more observable in S strain, which mostly mislaid cells uniformed membranes (Figure 4, S10). The cells of the R strain were also mostly exploded and lost their distinctive structures (Figure 4, R10). Coordinated remarks were attested after various bacterial species’ exposure to Ct-based NCs, which contained diverse phytocompounds and nanometals [31,37,47].

Figure 4

Scanning microscopy features of exposed Salmonella Typhimurium from antibiotic resistance (R) and sensitive (S) strains to chitosan/RSM/SeNPs NCs for 0, 5, and 10 h.

The Ct function in NC antibacterial bioactivity is principally involving the Ct competency for adherence onto microbial cells, its bactericidal activity, and enabling the encapsulated antimicrobials to penetrate inside microbes [26,48,63].

The bacteria (especially Gram^−ve types) comprise protective thin peptidoglycan layers, small condensed membranes, and lipopolysaccharides (with high negative charges) in the outer walls, which boost the development of porin channels and permit NP/NC penetration to interact with vital organelles of such microbes [58,61].

Such porines’ channels that selectively facilitate the penetration of NPs/NCs into cells, associating with ROS generation from SeNPs, can seriously cause the destruction and suppression of Gram^‒ve vital machineries (e.g., RNA, membranes, enzymes, DNA) [34,36]. Although the antibacterial actions of Ct/RSM/SeNPs were proved toward the entire S. Typhimurium strains, the destructive effect was more observable against S. Typhimurium S than against S. Typhimurium R, which gives potential insights for inhibiting the MDR strains with higher concentrations and exposure time from NCs.

The SEM images of Ct/RSM/SeNP-treated S. Typhimurium cells could provide potential mechanisms of NC antibacterial actions, instigated from reacted nanomolecule synergism, which includes the adherence onto bacterial cells’ membranes/walls, devastation of walls’ permeability and synthesis, NCs’ penetration inside cells, leaks of vital cellular components, and suppression of physiological metabolic pathways/bioactivities [34,36,61]. The electrostatic interactions between Ct and bacterial membranes could explicate/enforce these actions, which resulted in pores’ creation, disintegration, and destruction of cell structures [22,25,43,63].

4 Conclusion

The biosynthesis of SeNPs was innovatively achieved using RSM (as a reducing and capping agent); along with their nanoconjugation with Ct that generated bioactive NCs with diverse characteristics and bioactivities as antibacterial against S. Typhimurium, depending on blending ratios. The entire materials/NCs possessed powerful antibacterial powers against different S. Typhimurium, including MDR strains. The F2 (with 1:1 ratios of Ct:RSM/SeNPs) had the least (41.77 nm) particle average, whereas F3 (positively charged NCs) had the strongest anti-S. Typhimurium activity, which exceeded the antibacterial action of standard antibiotics. The NC action led to bacterial cells’ destruction/deformation within 10 h. The fabricated Ct/RSM/SeNP NCs are auspiciously suggested as innovative effectual biocides to eradicate MDR S. Typhimurium in various food-processing facilities.

Acknowledgments

The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia for funding this research work through the project number (0100-1443-S).

Funding information: The Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia funded this research work through the project number (0100-1443-S).
Author contributions: HAE contributed to the conception, design of the work, investigation, analysis, and funding acquisition; RFA contributed to the design of the work, investigation and analysis, and work drafting; GMM contributed to the interpretation of data, resources, administration and work drafting; NHA contributed to the conception, interpretation of data, work drafting, revising, and supervision; NB contributed to the interpretation of data, resources, administration, and work drafting; ASA contributed to investigation data curation and analysis and work drafting; IHA contributed to data curation, resources, and administration; AAT contributed to the conception, investigation, interpretation of data, supervision, work drafting, and submission. All authors read and approved the final article.
Conflict of interest: Authors state no conflict of interest.
Data availability statement: All data generated or analyzed during this study are included in this published article.

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Received: 2024-04-18

Accepted: 2024-07-17

Published Online: 2024-09-12

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

https://doi.org/10.1515/gps-2024-0090

Keywords for this article

antibacterial; bacterial pathogens; biopolymers; biosynthesis; nanomaterials

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