Synthesis and investigation of antimicrobial activity of SrWO4 nanoparticles against a panel of Gram-positive and Gram-negative bacteria

doi:10.21203/rs.3.rs-3958154/v1

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Synthesis and investigation of antimicrobial activity of SrWO₄ nanoparticles against a panel of Gram-positive and Gram-negative bacteria

https://doi.org/10.21203/rs.3.rs-3958154/v1

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Introduction: Elevated resistance of bacteria to common antibiotics and the lack of efficient alternatives to treat bacterial infections are the main concerns of health services. Therefore, the need to figure out new therapeutic options is inevitable. Strontium Tungsten Oxide nanoparticles (SrWO₄ NPs) as an antimicrobial agent have recently received attention. However, few reports have been published on its antimicrobial properties.

Material and methods: In the present study, SrWO₄ NPs were synthesized by hydrothermal method. To confirm the NPs synthesis procedure, spherical morphology, and particle size, XRD, SEM, TEM, FT-IR, and EDS analysis were performed. The antimicrobial properties of SrWO₄ NPs were assessed via the micro broth dilution method.

Results: The NPs size was nearly distributed 21 to 27 nm. The antibacterial effects of SrWO₄ NPs against both Gram-positive (Staphylococcus aureus (ATCC 25923) and Enterococcus faecalis (ATCC 29212) and Gram-negative bacteria (Pseudomonas aeruginosa (PAO1), Escherichia coli (ATCC 25922), and Enterobacter aerogenes (ATCC 13048) were evaluated using the micro broth dilution assay. The lowest and highest minimum inhibitory concentrations (MIC) were observed against Enterococcus faecalis (16 µg/mL) and Pseudomonas aeruginosa (256 µg/mL), respectively.

Conclusions: The chemical method can be used with high efficiency to synthesize NPs. Additionally; SrWO₄ NPs could serve as a valuable antibacterial candidate, particularly against Gram-positive bacteria.

SrWO4 NPs

antibacterial

Gram-positive

Gram-negative

Health-care-associated infections (HAIs) represent a significant challenge to health systems, affecting over 100 million patients worldwide annually [1]. Reports indicate that HAIs rank as one of the ten causes of death in the USA [2]. Both Gram-positive and negative bacteria are involved in HAIs. A reason for the remarkable importance of nosocomial pathogens like Staphylococcus aureus (S. aureus) is the ability to adapt to different environmental conditions [3–5]. Enterococcus faecalis (E. faecalis) is recognized as a lethal nosocomial pathogen. In the United States and Europe, enterococci are the second most common pathogen associated with HAIs [6, 7]. Escherichia coli (E. coli) leads to HAIs such as catheter-associated urinary tract infection (UTI) and ventilator-associated pneumonia [8, 9]. Enterobacter species implicate in the myriad range of the hospital and community-acquired infections. Enterobacter aerogenes (E. aerogenes) is the third most common species isolated from the respiratory tract in ICU patients [10]. Pseudomonas aeruginosa (P. aeruginosa) is frequently found in HAIs (up to 7%). This bacterium plays a decisive role in Hospital-acquired pneumonia and ventilator-associated pneumonia occurrence. It is second only to S. aureus, accounting for up to 20% [11].

Another driving force behind the HAIs is the spread of antibiotic-resistant isolates. Shortly after the introduction of antibiotics, drug-resistant bacteria appeared. Therefore, more advanced and newer drugs were developed to deal with resistant bacteria. This vicious cycle was the beginning of the emergence of multidrug-resistant bacteria. It is estimated that number of people died due to bacterial infections will surpass 10 million in 2050, which will be higher than all cancer-related deaths. To battle resistant bacteria, it is imperative to expand new antibacterial agents faster than the bacteria can evolve [12].

In recent decades, nano-based materials have been successfully applied in medicine. The unique characteristics, including high surface-to-volume ratio, biocompatibility, and small size, have encouraged scientists to use this technology for improving antibacterial therapy. Antibacterial behavior of NPs may attribute to mechanisms including cellular function disruption after the deposition of NPs on the surface of bacteria and increased generation of reactive oxygen species (ROS). This results in interference in cell activities (cell signaling and the electron transport system) and intracellular organelles disfunction [13]. The positive surface charge of NPs facilitates the attraction of NPs to the negatively charged bacteria, rupturing the bacterial cell wall [14]. The notable adverse side effects of the inorganic NPs, such as Ag and Cu, have restricted their usage. Therefore, searching for safer NPs continues [15].

The bactericidal effects of photocatalytic NPs opened up a new perspective within nanotechnology. UV and visible light serve as an activator of photocatalyst NPs. Electrons will be excited following the photon strike. The combination of the stimulated electron and O₂ accelerates O₂⁻ formation. HO₂ radicals are formed when O₂⁻ radicals react with H⁺ released from H₂O separation. The reaction between HO₂ and H⁺ ions leads to H₂O₂ formation. H₂O₂ radicals effectively enter the cytoplasmic space and kill bacteria [14]. Tungstates-based nanomaterials are an excellent photocatalyst with a potential application in air purification, cancer therapy, and antimicrobial therapy [16]. The low-cost production and high solubility are the reasons for the broad adoption of these NPs. Clinically applications of strontium (Sr) oxide NPs in medicine include biomedical imaging, cancer therapy, drug delivery, osteoporosis treatment, dental treatments, and chemical sensing. However, research into nanosized tungsten and Sr-based NPs is scarce [17]. In the present project, SrWO₄ NPs were prepared by hydrothermal method. NPs synthesis was confirmed via XRD, SEM, TEM, FT-IR, and EDS analysis. Finally, the antibacterial activity of SrWO₄ NPs was determined by the minimum inhibitory concentration (MIC) assay.

Bacterial Strains

The bacterial species applied in the current study were as follow: S. aureus ATCC 25923, E. faecalis ATCC 29212, E. coli ATCC 25922, P. aeruginosa PAO1, and E. aerogenes ATCC 13048. All bacterial isolates were kindly procured from Kashan University of Medical Sciences and Health Services. Stock cultures were freeze-dried and kept at − 20°C. Before use, bacteria were cultivated on a blood agar medium (Merck, Germany) overnightly.

Preparation of SrWO₄ NPs

First, 1 mmol of sodium tungstate (Sigma, USA) was resolved in 30 mL of double distilled water. Then, 1 mmol of strontium nitrate (Sigma, USA) was resolved in 30 mL of solvent with 3 mmol of masking agent at 70°C. Next, the two solutions obtained from previous step were added together under stirring and ultrasonic waves, followed by washing and drying the acquired sediment. Finally, the sediment was heated at 500°C for one hour. The white powder was SrWO₄ NPs used for further investigations [18].

Characterization of SrWO₄ NPs

The SrWO₄ NPs were characterized by X-Ray diffraction (XRD), transmission electron microscope (TEM) and scanning electron microscopy (SEM), infrared spectroscopy (FT-IR), and Energy-dispersive X-ray (EDS) analysis. XRD provides information about the crystallographic structure and physical properties of NPs. Investigation of the morphology and size of particles was performed by electron microscopic images. To study the chemical structure and type of bonds, FT-IR and EDS analysis were used.

Determining the antimicrobial properties of SrWO₄ NPs

Determining the minimum inhibitory concentration (MIC)

Bacteria were incubated in blood agar medium for 24 hours at 37°C. After that, a suspension with a concentration equal to 0.5 McFarland was prepared from bacteria by cultivating for 24 hours in muller-hinton-broth (MHB) medium (Merck, Germany). These bacterial suspension was diluted with MHB medium in a ratio of 1:20. Ten µl of above bacterial suspension (1.5 × 10⁶) were added to each well of the 96-well plates containing 100 µl NPs suspension with various concentration (1024, 512, 256, 128, 64, 32, 16, 8, 4, 2 µg/mL) and 100 µl of MHB medium. The microplate was incubated for 18 to 20 hours at 37°C. At the end of incubation period, the optical absorbance of the wells was measured at a wavelength of 630 nm using an ELISA reader to estimate MIC value. The MIC is defined as the lowest concentration of antibacterial agents with visible inhibition effects against bacterial growth. In each run, the wells containing MHB alone and MHB plus were placed as negative and positive controls, respectively [19]. Three replicates were performed for each strain in each series of tests. The data were represented as mean ± standard division. Vancomycin and imipenem were used as control antibiotics.

Determining the Minimum Bactericidal Concentration (MBC)

Broth dilution method was used to calculate MBC of NPs. Broth dilution method was used to calculate MBC of NPs. MBC is referred to the minimum concentration of an antimicrobial agent which able to kill 99.9% of the bacterial population. Following determining the MIC of SrWO₄ NPs, 50 µl of all wells showing no visible bacterial growth were inoculated onto blood agar plates and incubated for 24 hours at 37°C. Afterward, plates were assessed for the presence or absence of bacterial colonies [19].

Characterization of SrWO₄ NPs

In this study, SrWO₄ NPs with a size of 21–27 nm were synthesized. SrWO₄ NPs were characterized with FTIR, XRD, EDS, SEM and TEM analyzes

XRD analysis

Determinating of crystal structure, size, and, purity of NPs was performed by XRD spectrometer. The XRD pattern depends on the wave properties of X-rays and the periodic arrangement of the crystal. For a crystal sample, there are many peaks at different angles and with different intensities. Each of these peaks corresponds to a specific page of the sample. The X-ray diffraction pattern of strontium oxide tungsten nanostructures is shown in the Fig. 1. According to this figure, the XRD pattern is in perfect agreement with the diffraction pattern related to SrWO₄ nanostructure with reference number of 01-085-0587.

Electron microscopy

SEM and TEM (Aria Optoelectronics Company) were used to determine the shape and size of SrWO₄ NPs. SEM images of hydrothermally prepared SrWO₄ NPs are shown in Fig. 2. It is clear that morphology and structural properties of NPs is strongly under the influence of reaction temperature and duration. As we can see in Fig. 3, SrWO₄ NPs spherical morphology and suitable particle size (21 to 27 nm) were obtained in high temperature

FTIR analysis

FTIR was applied to identify absorption bands and realize the successful construction of nanocomposites and also their possible interactions. Absorption bands were in the range of 400–410, 800–810, 910–930, 1380–1395, 1600–1650, 1710–1725 and 3350–3450 cm (Fig. 4).

EDS analysis

The chemical composition of SrWO₄ NPs was investigated by EDS analysis. The existence of of W, Sr, and O atoms in the EDS spectrum of strontium tungsten oxide indicates the high purity of the product (Fig. 5).

MIC and MBC concentrations

To determine the antibacterial properties of the SrWO₄ NPs, MIC was estimated. The lowest and highest MIC values of SrWO₄ NPs was determined for E. faecalis (16 µg/mL) and P. aeruginosa (256 µg/mL), respectively. More detail about the MIC values of tested bacteria is provided in Table 1.

Table 1

The rate of MIC in the investigated standard bacterial strains
Bacterial strain	MIC (µg/mL)	P value
S. aureus	64	0.0001 <
Enterococcus faecalis	16
Escherichia coli	128
Pseudomonas aeruginosa	256
Enterobacter aerogenes	128

The lowest MBC value of SrWO₄ NPs was determined for E. aerogenes and the highest MBC value was related to P. aeruginosa (Table 2). Comparison of MIC and MBC values of all tested bacteria was illustrated in Figs. 6 and 7.

Table 2

The rate of MBC in the investigated standard bacterial strains
Bacterial strain	MBC (µg/mL)	P value
S. aureus	512	0.0014 <
Enterococcus faecalis	512
Escherichia coli	512
Pseudomonas aeruginosa	1024
Enterobacter aerogenes	256

Despite the infection prevention and control (IPC) program implemented by WHO to reduce the incidence of HAIs, these infections remain a potential threat due to several factors like elevated antibiotic-resistant pathogens causing disastrous consequences, including high mortality rates and healthcare costs [20]. Therefore, we evaluated the antibacterial effects of SrWO₄ NPs against a range of Gram-negative and Gram-positive bacteria.

In this study, spherical SrWO₄ NPs with a size ranging from 20 to 27 nm were synthesized using a hydrothermal method. The distinct multiple properties of this method allow the synthesis of many different types of nanostructures. For instance, controlling the size, shape, and crystallization of the particles can be achieved through synthesis at high temperatures (100–250°C) and vapor pressures [21]. The hydrothermal method offers several advantages, including easy-to-use equipment, minimal material consumption, low production costs, environmental friendliness, and mild preparation requirements [22].

Our results revealed that SrWO₄ NPs reduced the number of viable bacterial cells. There are controversial hypotheses regarding the antibacterial properties of WO₂ NPs. As an example, Muzaffar and colleagues reported that WO₃ alone could not strongly inhibit bacterial growth but could effectively kill bacteria when combined with other materials. This result may reflect antibacterial activity determination exclusively against Gram-negative bacteria [23]. However, several studies have validated the ability of WO₂ NPs to suppress bacterial proliferation [24].

Strontium (Sr) is mainly recruited to enhance the antibacterial activity of other NPs. Compared to ZnO alone, Sr-decorated ZnO particles adorned with Sr were more toxic to bacterial cells, specifically S. aureus and E. coli. Electrostatic interactions between bacterial cells and NPs advance to membrane disassembly and cell death. The bactericidal activity is directly correlated with the Sr decoration ratio. A higher ratio of Sr reduces the particle size, penetrating more NPs into cells. Furthermore, under experimental conditions, Sr2 reduced sensitivity to other metal particles, like silver ions [14].

Several mechanisms have been proposed for the antibacterial action of NPs. Excessive intracellular production of ROS exceeding the capacity of neutralization enzymes during mitochondrial respiration damages various cellular components of bacterial cells. The charge difference between the bacterial membrane and metal oxide NPs leads to NPs aggregating on the cell surface and internalizing. This induces cellular toxicity, including DNA damage, protein synthesis inhibition, and metabolic pathways impairment [25]. The chemical groups on the bacterial membrane surface, which possess electronegative properties, serve as the primary binding sites for metal cations [26]. G Duan et al. discovered that treatment with WO₃-X nanodots induces stress in the bacterial membrane. The notable bacterial cell deformities, such as roughness and pores, were also clearly visible in the SEM and TEM images. Cellular collapse suggests loss of cytoplasmic effusion and membrane damage. Moreover, the process by which WO₃-x NPs were adsorbed on the membrane's surface through interaction with the lipid head groups and cause lipid peroxidation was well elucidated by molecular dynamics simulation analysis. Disruption of membrane structure causes leakage of the cellular components, osmotic death, and blockage of membrane-dependent functions such as ATP synthesis and proton motive force [27]. According to studies, visible light has a substantially lower band gap energy than tungsten oxide NPs. Photonic activation of NPs leads to the production of electron/hole pairs that react with water and oxygen to form superoxide anion and hydroxyl radicals, killing bacteria [28].

According to previous studies, the antibacterial effect of SrWO₄ was observed to increase in a dose-dependent manner. Neutral pH is favorable for a wide range of bacteria, especially pathogenic strains. Changes in pH can affect bacterial growth. For example, bacterial growth can be inhibited in an alkaline environment. High concentrations of certain NPs like SrWO₄ release dissolved ions, establishing alkaline states. Alkaline pH denatures bacterial enzymes, improving bactericidal effect [29]. Change in pH due to metal ions dissolution was also shown by Baheiraei et al. The incorporation of Sr to the scaffold prepared for bone regeneration improved bactericidal effectiveness against both Gram-positive and Gram-negative bacteria. It is worth noting that the scaffold had greater pronounced against Gram-positive bacteria [30]. In some studies, the acceptable inhibitory effects of Sr against methicillin-resistant S. aureus (MRSA) species were observed. Except for already discussed mechanisms, Sr ions liberation hinders cell wall synthesis, bacterial growth and reproduction, and chromosomal replication. More penetration within the bacterial cell is also influenced by the nature of the nanomaterials. The smaller the particles, the more effective they are against pathogens [31].

On the other hand, Gram-negative bacteria were not as susceptible as Gram-positive bacteria. The highest and lowest antibacterial activities were observed against E. faecalis (16 µg/mL) and P. aeruginosa (256 µg/mLrespectively. This difference is typically ascribed to the structural differences in the cell wall. The presence of the outer membrane containing lipopolysaccharides restricts the accessibility of antibacterial agents to Gram-negative bacteria. Therefore, myriad hydroxyl radical assaults are required to completely incapacitate Gram-negative bacteria. In contrast, the reduced complexity of the cell wall of Gram-positive bacteria preferably absorbs many molecules [32]. In line with our findings, Matharu et al. demonstrated that the number of live S. aureus cells remarkably dropped compared to E. coli (83.7% versus 22.8%) after treatment with tungsten oxide NPs [33]. Our study had some limitations. For example, we didn’t evaluate the cellular toxicity of SrWO₄ NPs, as most metal NPs induce various toxicities in humans. On the other hand, to better understand the action mechanism of SrWO₄ NPs, further investigations are needed. Therefore, these findings cannot be directly generalized to clinical situations. Nevertheless, antibacterial properties and low risk of developing resistance make the NPs an ideal candidate for bacterial treatment.

Based on our findings, we concluded that: firstly, NPs were synthesized by hydrothermal method with minimal time and materials waste. Secondly, the characterization of NPs (morphology and size) indicated the antibacterial properties of particles. Thirdly, the inhibitory effects of NPs depend on bacterial species. In this regard, SrWO₄ NPs suppressed the growth of Gram-positive bacteria in a lower concentration than Gram-negative ones. It is relatively beacause of a lower absorption of molecules and compounds in the cell wall of Gram-negative bacteria. These results suggest that NPs could be considered a powerful alternative to overcome infections caused by drug-resistant bacteria in the future.

Research suggestions:

Use of SrWO₄ NPs in in vivo conditions

Investigation of the cytotoxicity of SrWO₄ NPs

Use of clinical strains

Conflicts of interest: The authors have no relevant financial or non-financial interests to disclose.

Funding: This study was funded by Kashan University of Medical Sciences, Kashan, Iran (Grant No 400176).

Ethics approval: This study was approved by the ethical board of Kashan University of Medical Sciences, Kashan, Iran (IR.KAUMS.MEDNT.REC.1401.190).

Data availability: The authors confirm that the data supporting the findings of this study are available within the article.

Authors’ contribution statements: All persons who meet authorship criteria are listed as authors, and all authors certify that they have participated sufficiently in the work to take public responsibility for the content. Furthermore, each author certifies that this material or similar material has not been and will not be submitted to or published in any other publication before its appearance in the “Polymer Bulletin”. Investigation, Methodology, Resources: [Meysam Ghaljehei], Nanoparticles synthesis: [Ali Sobhani Nasab], Conceptualization, Supervision and, Analysis: [Ali Nazari-Alam], Writing – review & editing: [Zeynab Marzhoseyni].

Acknowledgments

The authors would like acknowledge the Kashan University of Medical Sciences, Kashan, Iran to financial support.

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No competing interests reported.

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Version 1

posted

You are reading this latest preprint version

Synthesis and investigation of antimicrobial activity of SrWO₄ nanoparticles against a panel of Gram-positive and Gram-negative bacteria

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Bacterial Strains

Preparation of SrWO₄ NPs

Characterization of SrWO₄ NPs

Determining the antimicrobial properties of SrWO₄ NPs

Determining the minimum inhibitory concentration (MIC)

Determining the Minimum Bactericidal Concentration (MBC)

Results

Characterization of SrWO₄ NPs

XRD analysis

Electron microscopy

FTIR analysis

EDS analysis

MIC and MBC concentrations

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1

Synthesis and investigation of antimicrobial activity of SrWO4 nanoparticles against a panel of Gram-positive and Gram-negative bacteria

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Bacterial Strains

Preparation of SrWO4 NPs

Characterization of SrWO4 NPs

Determining the antimicrobial properties of SrWO4 NPs

Determining the minimum inhibitory concentration (MIC)

Determining the Minimum Bactericidal Concentration (MBC)

Results

Characterization of SrWO4 NPs

XRD analysis

Electron microscopy

FTIR analysis

EDS analysis

MIC and MBC concentrations

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1

Synthesis and investigation of antimicrobial activity of SrWO₄ nanoparticles against a panel of Gram-positive and Gram-negative bacteria

Preparation of SrWO₄ NPs

Characterization of SrWO₄ NPs

Determining the antimicrobial properties of SrWO₄ NPs

Characterization of SrWO₄ NPs