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 Table of Contents  
Year : 2021  |  Volume : 8  |  Issue : 4  |  Page : 415-421

Antibiofilm activity of selenium nanorods against multidrug-resistant staphylococcus aureus

Department of Biotechnology, Progressive Education Society’s Modern College, Ganeshkhind, Pune, Maharashtra, India

Date of Submission15-Jul-2021
Date of Acceptance26-Nov-2021
Date of Web Publication22-Dec-2021

Correspondence Address:
Dr. Uttara Oak
Department of Biotechnology, Progressive Education Society’s Modern College, Ganeshkhind, Pune 411016, Maharashtra.
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/mgmj.mgmj_35_21

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Objective: This study aimed at the synthesis and application of selenium nanoparticles (SeNPs) against biofilm formation by multidrug-resistant (MDR) Staphylococcus aureus isolated from the domestic sewage treatment plant. Materials and Methods: Chemically synthesized SeNPs were characterized using Ultraviolet–visible spectroscopy, X-ray diffraction, and high resolution scanning electron microscopy (HR-SEM).. Bacteria were isolated from domestic sewage water samples and characterized and identified using standard techniques. The drug resistance pattern of the isolates was determined using a disk diffusion assay. Biofilms of this MDR isolate were established (microtiter plate method—colorimetric assay and a slide method). Minimum inhibitory concentrations (MIC) of selenium nanorods (SeNRs) and their effect on biofilm formation were established using a colorimetric method. Results: The HR-SEM analysis of nanomaterials revealed its shape (rod), size (between 85 nm and 275 nm), and purity of the material. The disk diffusion assay attributed MDR status to an isolate that was identified and found to be S. aureus, a pathogenic bacterium isolated from an environmental sample. The MICs of antibiotics against biofilm were found to be at least threefold higher than those against the planktonic state. In the presence of SeNRs, biofilm formation was inhibited. Conclusion: SeNRs synthesized using wet chemical method showed antibacterial activity against MDR S. aureus and inhibited biofilm formation by this organism. These SeNRs can be further developed as an alternate drug lead to combat the challenge posed by the MDR bacteria. The study has a future prospectus in investigating the mechanism of inhibition of biofilm formation and its action on preformed biofilm by this isolate.

Keywords: Biofilm formation and disruption, MDR Staphylococcus aureus, MIC, selenium nanorods

How to cite this article:
Hasani S, Khare T, Oak U. Antibiofilm activity of selenium nanorods against multidrug-resistant staphylococcus aureus. MGM J Med Sci 2021;8:415-21

How to cite this URL:
Hasani S, Khare T, Oak U. Antibiofilm activity of selenium nanorods against multidrug-resistant staphylococcus aureus. MGM J Med Sci [serial online] 2021 [cited 2022 Jan 18];8:415-21. Available from: http://www.mgmjms.com/text.asp?2021/8/4/415/333313

  Introduction Top

The bacterial biofilms are an accumulation of cells in a matrix of the extracellular polymeric substances (EPS).[1],[2] The biofilm formation by bacteria initiates adsorption of the planktonic cells to a substrate under the influence of physical forces or with the help of the bacterial appendages such as flagella, pili, or fimbriae. This is referred to as adhesion, whereas the cells attach and the process is termed cohesion.[2],[3] The cells bind irreversibly to the substratum, divide and the daughter cells develop in the upward and outward directions from the point of attachment. This leads to the formation of a mushroom-like structure..[3],[4] These microcolonies, under the influence of enzymes such as nucleases, proteases, and surfactant-like molecules such as Bacillus subtilis surfactin, Pseudomonas aeruginosa rhamnolipid, phenol-soluble modulin β-peptides in Staphylococcus,[5] release the cells embedded in the biofilm for the establishment of fresh biofilms on new substrates.[3],[6]

Biofilm formation is one of the strategies used by pathogenic bacteria for its survival and transmission by the virtue of quorum sensing, increased adherence, horizontal gene transfer, dissemination of bacteria in sufficiently large numbers for causing successful infection, and thereby increased virulence.[7] Biofilms play an important role in certain diseases and a variety of device-related infections. It is estimated that biofilms contribute to more than 80% of human infections.[8] Biofilm-inducing bacteria such as gram-negative bacteria P. aeruginosa and Escherichia coli and gram-positive bacterium Staphylococcus aureus contribute to approximately 65%–80% of diseases as reported by the National Institute of Health (NIH) and Centre of Disease Control (CDC). They are implicated in a wide array of chronic infections, including sinusitis, otitis media, chronic obstructive pulmonary disease (COPD), endocarditis, decubitus, diabetic ulcers, prostatitis, conjunctivitis, superficial skin infections, airway infections in cystic fibrosis, vulvovaginitis, urinary tract infections, and periodontitis.[9],[10],[11] Biofilms grow on implanted medical devices such as catheters, prosthetic heart valves, artificial hip prosthesis, artificial voice prosthesis, and intrauterine devices,[12],[13] thereby increasing the chances of the aforementioned chronic infections.

The sensitivity of biofilm-associated microorganisms to antimicrobial agents is considerably decreased. This is due to multiple factors such as the inability of antibiotics to cross the EPS layer; overproduction of efflux pumps; enzymatic modification of the antimicrobial compound; alteration of the membrane lipids preventing entry of the drug into the cell; and the presence of persisters or dormant cells that slow down or shut down metabolism and no longer offer target site/molecules for the action of the antibiotics.[14],[15],[16],[17] These attributes render the multidrug-resistant (MDR) status to the biofilms, and the treatment of chronic infections with antibiotics turns ineffective. Therefore, it is becoming increasingly imperative to develop and test new antimicrobial compounds capable of bactericidal activity even in biofilm growth mode toward MDR bacterial species.

In recent years, the utilization of nanoparticles (NPs) has emerged as an alternative to the use of organic compounds as antimicrobial agents. A widespread antimicrobial activity is often a common trait of nanomaterials. The high surface-to-volume ratio of NPs enables its increased interactions with the target such as bacteria or biofilms as compared with their conventional micron particles.[18] As a result, NPs are likely to exert stronger antibacterial effects on bacteria or biofilms than their microcounterparts. The mechanisms involved in the bactericidal action of the NPs involve leakage of cellular contents by membrane disruption, inhibition of quorum sensing, and hindrance in bacterial adherence to the surfaces that are impregnated with nano-layers and downregulation of proteins.[19],[20]

These activities have enabled a wide range of applications of NPs in the medicinal field that includes antibiotic delivery systems, diagnostics for microbial detection, antibacterial vaccines, and coatings for medicinal materials in wound healing and implantable devices to prevent infections.[21],[22] The biofilm formation, decreased uptake of antibacterial compounds, and increased efflux of drug by the microbes can be vanquished by the NPs. As delivery agents, NPs also allow higher doses of the drug to the site of infection.[23],[24] Several NPs that include metal, metal oxide, nonmetal, and metalloid NPs along with composite NPs have shown promising activities w.r.t. reversal of antimicrobial resistance of bacteria and disruption of biofilms. However, the toxicity of these NPs has been a major concern.

Selenium is a trace element essential for the activity of many cellular proteins. It shows a strong antimicrobial and anticancer activity at low concentrations.[25],[26] In the present study, selenium NPs were synthesized using a soft chemical synthesis method, and its activity against the biofilm-forming MDR bacteria isolated from environmental samples is explored.

  Materials and methods Top

Chemicals and media

Dehydrated media, antibiotics, antibiotic disks, and microtiter plates were from HiMedia. The chemicals used in the study were procured from SRL and Sigma Aldrich and were of analytical grade.

Sample collection, isolation, and characterization of the isolates

The water sample was collected from a sewage treatment plant in Kasarwadi, Pune, India, in sterile containers and processed for isolation of bacteria. The sample was appropriately diluted (10−1 to 10−4) and spread on plate count agar and incubated at 37°C for 24 h. Individual colonies showing different morphologies were then selected, purified, and maintained on nutrient agar.

Drug resistance pattern and ability to form biofilm were determined, and the MDR bacteria forming biofilm were subjected to microscopic and biochemical tests,[1] for its identification.

Disk-diffusion assay for drug resistance

Cultures were isolated from the collected water samples, purified, and maintained on nutrient agar slants. Using the disk-diffusion method, 25 purified cultures (designated as A-Y) were screened to determine their resistance to antibiotics. Each of the cultures was grown overnight in Mueller Hinton Broth (MHB) at 37°C and diluted with sterile MHB to reach the 0.5 McFarland standard. 0.1 mL of the diluted culture was used to seed MHA plates. Antibiotic disks were placed on the MHA and the plates were incubated at 37°C for 24 h. The zone of growth inhibition was measured and reported based on CLSI guidelines (CLSI; M100S, 30th edition).

Synthesis and characterization of SeNPs

SeNPs were synthesized using a method described by Webster and Tran[27] with some modifications. 3 mL of 25-mM sodium selenite and 3 mL of 100-mM glutathione (reduced form) were added to 9 mL of double-distilled water inside a laminar airflow hood. All the solutions were prepared in sterile double-distilled water. Sodium selenite and glutathione were mixed to which 1 mL of 1N NaOH was added, to shift the pH of the solution to alkaline range. The solution was left undisturbed for 2–3 h, to allow the precipitation of the particles. After which, the particles were separated from the liquid and were dried inside a hot air oven at 60°C. Dried powder and colloidal suspension of the synthesized NPs were used for characterization. Dried powder of SeNPs was suspended in deionized water and used for Ultraviolet–visible (UV–vis) spectroscopic analysis. Full-wavelength scanning was recorded from 200 to 800 nm using Shimadzu UV–vis spectrophotometer and checked for the maximum absorption peaks. Deionized water was used as blank.

The dried SeNP powder was analyzed using Bruker Advance-08 X-ray diffraction (XRD). The diffracted intensities were recorded from 10° to 70° 2θ angles. The spectra obtained were then compared with the International Centre for Diffraction Data database which is a standard data used as a fingerprint for all the powder diffraction samples which help in matching the peak patterns specific to individual samples. Sample for scanning electron microscope (SEM) analysis was prepared by drying the colloidal suspension on a silicon wafer under an infrared lamp. This sample was then used to check the morphology by using a Quanta 200 SEM at a magnification of 20,000×.

Biofilm formation

Cultures showing MDR were used to establish biofilms using the slide method (on glass coverslips) and microtiter plate method (on the bottom of the wells of a microtiter plate) as described by Merritt et al.[28] Cultures were grown overnight in tryptic soy broth (TSB) at 37°C and diluted with sterile TSB to reach the 0.5 McFarland standard and used to establish biofilms.

Slide method

The diluted suspension of each bacterial isolate was added to Petri plates containing sterile glass coverslips and incubated at 37°C for 0, 6, 18, 24, 30, and 48 h. The coverslips were carefully rinsed with peptone water (0.85% NaCl in 0.1% peptone) twice and stained with 0.1% (w/v) safranin solution for 10 min. The stained coverslips were rinsed with sterile distilled water, air dried, placed on glass slides, and observed under a microscope using a 40× objective.

Microtiter plate method

The bacterial suspensions were diluted in TSB supplemented with 2% glucose (w/v) and 2% sodium chloride (w/v), (TSBGS); in 1:100 and 1:200 ratio. A total of 200 μL of the inoculum (undiluted and diluted to 1:100 and 1:200) was added to the microtiter plate and incubated at 37°C for 24 h. The microtiter plate was read using an ELISA reader (Bio-Rad, USA) at 562 nm as a measure of total growth. The culture supernatant was removed and the plates were carefully rinsed with peptone water twice and stained with 0.1% safranin solution for 10 min. After which, safranin solution was removed and the plates were air-dried. Hundred microliters of sterile saline were added to the air-dried wells in the microtiter plate, which was read at 450 nm and A450 values were recorded.

MIC of antibiotics and SeNPs against biofilms of the MDR

MIC of five different antibiotics (final concentration in the range 0.98–1000 μg/mL) and the synthesized SeNPs (final concentration in the range 0.20–100 μg/mL) was determined using microdilution method described by Elkhatib et al.[29] Inoculum preparation and staining of the microtiter plate for biofilm were performed as described above in biofilm establishment experiments. 10 μL of the inocula (undiluted and diluted to 1:100 and 1:200) were added to 100 μL of the SeNPs and each of different concentrations of filter sterilized antibiotics in a microtiter plate and incubated at 37°C for 24 h. The microtiter plates were then stained and observed for biofilm formation. Inoculum without antibiotics (undiluted and diluted), antibiotics dissolved in appropriate solvents, uninoculated broth, 0.1% safranin in saline, and saline were used as controls. The control wells in the microtiter plates and those to which SeNPs were added at half the MIC and MIC values were also observed microscopically.

  Results Top

Isolation and characterization of the isolate

Twenty-five isolates (designated A-Y) were obtained and purified from the water sample. Of the 25 isolates, the organism forming biofilms in the slide as well as microtiter plate assay (isolate W) was subjected to microscopic and biochemical analysis ([Supplementary Tables S1] and [S2]). This analysis suggested that isolate W was S. aureus.
Supplementary Table S1: Colony characteristics of isolate W

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Supplementary Table S2: Biochemical tests of the isolate W

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Disk diffusion test

The results of the disk diffusion test were analyzed as per the CLSI guidelines. On the basis of the diameters (in mm) of the growth inhibition zones ([Supplementary Table S3]), isolate W showed resistance to at least one antibiotic from at least three different classes of antibiotics each and thus was confirmed to be MDR. Isolate W showed MDR status in the disk diffusion assay and thus confirmed as MDR S. aureus and designated as MDRSA.
Supplementary Table S3: Growth inhibition zone diameters of the isolates against several antibiotic disks

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Synthesis and characterization of SeNPs

The addition of NaOH showed an immediate color change [Figure 1]A, from pale yellow to orange, indicating the formation of SeNPs via the reduction of sodium selenite by glutathione. The particles, after settling, showed a deep black color. The color shift from pale yellow to orange in the alkaline pH regime brought about the reduction of SeO32− to Se0. A strong absorption peak was observed with maxima at 215 nm [Figure 1]A when scanned from 200 to 800 nm in a UV–vis spectrophotometer. The peak observed is due to the surface plasmon resonance of the SeNPs. Synthesized nanoparticles were analyzed for their crystalline nature via XRD [Figure 1]B. Narrow diffraction peaks were visible, concluding that the particles synthesized were crystalline. The diffraction peaks were seen at 2θ = 23.9, 30.0, 41.7, 44.0, 45.7, 52.0, 56.4, 62.2, 65.5, and 68.4. The observed lattice constants a (Å) = 4.368 and c (Å) = 4.948 matches the expected value a (Å) = 4.3662 and c (Å) = 4.9536 (JCPDF File no. 06-0362), thereby confirming that the synthesized nanoparticles are of selenium. SEM images [Figure 1]C indicated the size of the particles and confirmed that the particles were in the nanoscale. The well-dispersed SeNPs were found to be in the range of 85–185 nm and were showing rod-like morphology. The SeNPs were then designated as selenium nanorods (SeNRs).
Figure 1: Characterization of SeNPs: (A) Ultraviolet–visible spectrum (inset: synthesis of SeNPs: pale yellow color before addition of NaOH; orange color on addition of NaOH); (B) X-ray diffraction pattern; (C) SEM images

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The ability of the MDRSA to form biofilm

Slide method

The development of biofilm of MDRSA was monitored at different time points under the light microscope [Supplementary Figure S1 (a–f)]. At 0 h, individual cells (planktonic cells) were seen and as time progressed, cells started to form communities and were seen in aggregates. Matrix was visible around some of the microbial communities after 18 h whereas, after 24 h, all the cells were seen in aggregates (microbial communities) and were surrounded by a well-defined matrix indicating the formation of biofilms.
Supplementary Figure S1: Biofilm development of MDRSA: a- 0 hours; b- 6 hours; c- 18 hours; d - 24 hours; e- 30 hours; f- 48 hours

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Microtiter plate method

The biofilm-forming capacity of MDRSA was determined based on A450 values. A450 < 0.20, 0.20 ≤ A450 ≤ 1.0, and A450 > 1.0 can be designated as negative, weak, and strong biofilm producers, respectively.[29] This organism shows A450 values between 0.20 and 1.0 ([Table 1]), indicating that the culture can produce biofilms.
Table 1: Biofilm measurement

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Antibiofilm activity of antibiotics and SeNPs against MDRSA

MIC of antibiotics against the planktonic state and biofilms of the MDRSA

MICs of five different ([Table 2]) antibiotics against the biofilms of MDRSA were multifold higher than the respective values at planktonic state. In both cases, MIC values were found to be at least threefold higher than the values suggested for resistance by the CLSI guidelines.
Table 2: MIC of antibiotics against MDRSA

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MIC of SeNRs against the biofilms of the MDRSA

The assay was performed between the concentration 0.20 and 100 μg/mL. The MIC of SeNPs against the biofilm of the MDRSA was 50 μg/mL. Biofilms were not formed in the microtiter plate wells containing SeNRs at the MIC level ([Table 3]). This was further confirmed by observing the wells under the microscope (data not shown).
Table 3: Effect of nanoparticles on the biofilm formation of the MDRSA at 50 μg/mL

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  Discussion Top

The resistance developed to the conventional antibiotics has necessitated the exploration of alternate therapy methods to combat the MDR bacteria. The prevalence of MDR bacteria is common in hospital environments; however, its occurrence in the samples collected from the wastewater treatment plants can pose a serious threat with respect to spread of drug resistance. The present work, therefore, targets inhibition of biofilm formation by the MDR bacteria isolated from environmental samples with the help of SeNPs synthesized using a soft chemical method. In the present study, glutathione was used as a reducing agent for SeNRs synthesis. Vahdati et al.[30] have reported an alternate soft chemical method where ascorbic acid is used as a reducing agent for the synthesis of SeNPs. Both the methods can be easily used in a laboratory setup for the synthesis of SeNPs.

The synthesized SeNPs were characterized using UV–vis spectroscopy, XRD, and high resolution scanning electron microscopy (HR-SEM). The data obtained were compared with the reported characteristics of SeNPs in the literature. Prasad et al.[31] reported absorption maxima of 395 nm for SeNPs. However, other authors[32],[33] have reported SeNP peaks in the range of 200–300 nm. Also, the lattice constant values obtained in XRD analysis are consistent with those reported earlier.[26],[34] The HR-SEM analysis confirms the nanoscale range of the particles and reveals their morphology.

The ability of the MDRSA to form biofilm was confirmed using the slide as well as microtiter plate assays. When compared with the planktonic state A450 values, it is evident that the culture has established biofilms, on the bottom of the microtiter plate. Biofilm formation is one of the major mechanism by which methicillin-resistant S. aureus (MRSA) demonstrate drug resistance.[3],[35] Biofilm matrix impedes the diffusion of the antibacterial agent. In addition to diffusion, the alteration in the physiology of the bacteria in biofilm offers resistance to the drugs.[36] The SeNRs proved their ability to inhibit biofilm formation by the MDRSA. Cihalova et al.[37] and Zonaro et al.[38] have reported disruption of biofilms of drug-resistant S. aureus when SeNPs are used along with antibacterial compounds and have also shown a reduction in the MIC values of the antibiotics. Goswami et al.[39]and Mapara et al.[40] observed the release of intracellular contents from S. aureus and P. aeruginosa, respectively, posttreatment with silver nanoparticles and they further proposed that the nanomaterial deranged cell to cell adhesion resulting in disruption of biofilms. In another study, it was reported that inhibitory concentrations of silver nanoparticles showed a significant decrease in EPS production in Klebsiella pneumoniae thereby inhibiting biofilms.[41] Shakibaie et al.[42] demonstrated that SeNPs inhibited S. aureus, P. aeruginosa, and Proteus mirabilis biofilms. A similar activity of SeNPs was demonstrated on S. aureus and P. aeruginosa biofilms with a proposed mechanism of generation of reactive oxygen species (ROS) on the surface of NPs.[43] ROS production causes toxic effects on bacteria that disrupt the cell envelope. Disruption of a cell wall allows intracellular entry of the SeNPs and enables the SeNPs to interact and inactivate the intracellular proteins.[44] The production of ROS and disruption of the cell wall may also hinder biofilm formation. It may not allow the cell to cell adhesion thereby formation of biofilms. Similar mechanisms may be involved in the current study where biofilm formation is inhibited. However, a detailed further study will enable us to predict the exact mechanism of the SeNRs against the MDRSA.

  Conclusion Top

Selenium nanorods were synthesized using a chemical synthesis method and characterized to determine their size, morphology, crystal structure, and purity. Its antibacterial and antibiofilm activity was tested against biofilm-forming MDRSA. Synthesized SeNRs proved to be involved in the disruption of the biofilms formed by MDRSA. The scope of this study can be widened further for possible application of the SeNPs on implants, thereby treating the infections caused by such MDR bacteria. Also the mechanism underlying biofilm disruption can be unveiled.

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Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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