Antibacterial activity of super-paramagnetic iron oxide nanoparticles against Edwardsiella tarda from water

doi:10.21203/rs.3.rs-1764636/v1

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Antibacterial activity of super-paramagnetic iron oxide nanoparticles against Edwardsiella tarda from water

https://doi.org/10.21203/rs.3.rs-1764636/v1

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The current study was conducted to evaluate the antibacterial activity of super-paramagnetic iron oxide nanoparticles (SPIONs) against Edwardsiella tarda from water. The antibacterial activity of different concentrations of SPIONs viz. 0, 6.25, 12.5, 25, 50, 100, 200, 500 and 1000 µM were assessed in sterilized distilled water with different initial bacterial loads of E. tarda viz. 1×10³, 1×10⁴, 1×10⁵, 1×10⁶ and 1×10⁷ CFU ml^− 1 at various exposure time (15, 30, 45 and 60 min). At lowest bacterial load 1×10³ CFU ml^− 1, > 98% bacteria was removed by 500 µM of SPIONs concentration group after 15 min exposure, which was increased up to 100% by increasing exposure time 45 min. However, at highest bacterial load 1×10⁷ CFU ml^− 1, > 78% bacterial load was removed by highest SPIONs concentration (1000 µM) by 15 min exposure, which was further increased > 85.32% by increasing the exposure time 60 min. The antibacterial activity was increased with increasing the concentration of SPIONs as well as exposure time while increasing the bacterial load the activity was decreases. At an initial bacterial load of E. tarda (1×10³ to 1×10⁷ CFU ml^− 1), the effective concentration (EC₅₀) ranged between 61.36 to 372.80 µM respectively after 15 to 60 min exposure. Thus, it can be concluded that the antibacterial activity of SPIONs depends on concentration and exposure time. To remove high bacterial load require high amount of SPIONs and exposure time as well. Hence, SPIONs can be used as a biocidal agent to treat Edwardsiellosis in fish.

SPIONs

Edwardsiella tarda

Antibacterial activity

Effective concentration

Aquaculture

Aquaculture is one of the fastest emerging foods-producing sector contributes to the development of world economy. It not only source for animal protein, also provide the essential micronutrients for human health (Devi et al. 2019). Intensification of aquaculture operations, currently a global trend to maximize the production per unit area to meet food demands for a growing global population. Intensification caused the change in culture condition leads to stress, impairing physiological functions of the fish, and increasing the susceptibility to several bacterial infections by immune suppression (Baldissera et al. 2019). Disease outbreaks caused the billions of dollars revenue loss worldwide in current aquaculture scenario (Lightner 2003). One of the major challenge in an intensified aquaculture operation is to maintain the optimum quality water parameters for prevention of disease outbreak in running crop. Bacterial infections are considered as a major cause of fish mortality in running crop due to alteration of cultured parameters. Around 10–15% aquaculture production loss per year due to occurrence of bacterial diseases (Ravikumar et al. 2010).

The Edwardsiella tarda is the most important bacterial fish pathogen associated with global economic losses. It is intracellular Gram-negative bacilli belonging to the Enterobacteriaceae family. This bacterium is widely distributed in the freshwater and marine environment, possessing a wide geographical distribution. It generally affects the fishes maintained in adverse aquatic environmental conditions such as high temperatures and organic load, transportation, low DO and handling stress. The symptoms of edwardsiellosis varies with the age of fish and species cultured. The affected fish shows the external symptoms such as loss of skin colour, abdominal distension, cutaneous haemorrhagic lesions and rectal prolapse. Common internal lesions in fishes include ascites, peritonitis, abscesses, hepatic, splenic and renal congestion (Miniero Davies et al. 2018). Besides representing a great cause of concern to aquaculture, E. tarda occasionally causes infections in humans also. The course of infection is dependent on the immunological status of the individual and linked to the environmental exposure, contact with exotic animals such as fishes, amphibians or reptiles, or ingestion of raw fish meat (Novotny et al. 2004).

Nowadays, several methods are used in the World to control/minimize the disease occurrence in the aquatic system, such as drugs and chemicals, antibiotics, and regular exchange of water. The treatment of edwardsiellosis is troublesome in culture condition due to the emergence of multi-resistant strains of E. tarda (Singh and Ebibeni 2016). The major drawback of using continuous, excessive and uncontrolled chemicals and antibiotics to treat the bacterial disease in fish and shrimp causes the change in physiology of cultured organism, change in environmental parameters, bioaccumulation and development of antibiotic resistance of pathogenic and environmental bacteria (Bilen and Elbeshti 2019). Hence, it is very essential to generate/develop as an alternate of antibiotics such as a novel technique/biocide to kill even multi-resistance strain of pathogenic microorganism.

Super-paramagnetic iron oxide nanoparticles (SPIONs) are a special class of metal oxide nanomaterials which exhibit different valuable properties such as large surface area to volume ratio, high adsorbing and magnetic properties, and high antibacterial and antifungal activity (Margabandhu et al. 2015; Parveen, et al. 2018; Nivethitha and Rachel, 2020). In addition, SPIONs can be reused either as such or after washing with water and alcohol (Dong et al. 2011). The mass scale production synthesized by a cost-effective, high yield co-precipitation method. It exert their antibacterial effect with different mechanisms such as by contacting with bacterial cell membrane (physical damage) (Polyak et al. 1997; Inoue et al. 2002), internalisation induces apoptosis and alteration of the bacterial cell membrane structure thus leading to the production of reactive oxygen species (ROS) (Pramanik et al. 2012; Arakha et al. 2015; Li et al. 2018), accumulation of nanoparticles in the cell direct damage of DNA and protein and subsequent leads to cell death (Arakha et al. 2015; Li et al. 2018). Recently, several studies were conducted to evaluate the antimicrobial activity of SPIONs (Arakha et al. 2015; Dinali et al. 2017; Li et al. 2018; Saqib et al. 2019), nanoparticulate zero-valent iron (nZVI), ferrous ion (Fe(II)), and magnetite nanoparticles (Taylor and Webster 2009).

The present study was conducted to develop the antibacterial or biocidal agent to remove the disease causing bacterial load from water which can be used as an alternative of antibiotics. The synthesized SPIONs were already characterized in our previous study for their structural and magnetic properties using UV-Vis spectrophotometer, DLS, FEG-TEM, FT-IR, XRD, and VSM analysis. Further, the characterized SPIONs were used to evaluate their antibacterial activity/bacterial removal efficiency against fish disease causing microorganism E. tarda.

Chemicals

Ferric chloride hexahydrate (FeCl₃ .6H2O), ferrous chloride tetrahydrate (FeCl₂ .4H₂O) and glucose were procured from Sigma Aldrich. Sodium hydroxide (NaOH) was procured from HiMedia Laboratories, Mumbai, India. The glassware and plasticware were procured from the Borosil and Parsons, respectively.

Synthesis of superparamagnetic iron oxide nanoparticles (SPIONs)

The SPIONs was synthesized via the co-precipitation method given by Singh et al. (2018) with slight modifications. The nanoparticles synthesis was done by sodium hydroxide (NaOH) mediated precipitation from a mixure of ferric and ferrous chloride solution in 2:1 M ratio. The 0.270 g FeCl₃ hexahydrate (10 mmol) and 0.097 g FeCl₂ (5 mmol) were dissolved in 100 mL of degassed autoclaved distilled water. Then, the mixture was kept under nitrogen gas flashing to maintain an anaerobic or reducing condition on a magnetic stirrer at 800 rpm. The reaction mixture was adjusted to pH 11 by adding 2 M NaOH drop by drop. The mixture was allowed to proceed for 4–5 hr at 65–70 °С with constant stirring (800 rpm). Then, the resulting black slurry of SPIONs was prepared and then heated at 70–80°C in a water bath for 30–40 min. The particles thus obtained exhibited a strong magnetic response. The removal of ion impurities such as chlorides was done by washing the nanoparticles 4–5 times with distilled water. The synthesized nanoparticles were dispersed in 20 mL autoclaved distilled water. The prepared SPIONs were stored at room temperature.

Bacteria suspension preparation of E. tarda

The pure culture of gram-negative bacteria E. tarda, one of the most dangerous pathogenic strain of freshwater aquatic system collected from the Division of Aquatic Animal Health Management, Central Institute of Fisheries Education, Mumbai, India was selected to evaluate the antibacterial activity of SPIONs. The E. tarda was grown in 100 mL of brain heart infusion (BHI) broth medium at 37^oC for 16–24 hr in a thermostatic incubator with continuous agitation. The cultured cells of E. tarda was separated from the growth medium by centrifugation at 5,000 rpm for 5 min at 15^oC. The collected pellet were washed three times by re-suspending in sterilised deionised water to obtain bacterial stock solutions. The concentration of the bacteria suspension was established using the optical density at 600 nm (OD 600) measured with a UV spectrophotometer (Shimadzu, Japan). The dilutions were plated on a solid medium, and the colonies were then counted. Bacterial concentrations were expressed as colony-forming units (CFU). The desired bacterial concentration was checked by the standard plate count technique. Only plates with 30–300 colonies were counted. Finally, the different bacterial load such as 1×10³, 1× 10⁴, 1×10⁵, 1×10⁶ and 1× 10⁷ CFU ml^− 1 were prepared by serial dilution.

Antibacterial activity of G-SPIONs against E. tarda

To study the antibacterial activity of different concentrations of G-SPIONs such as 0, 6.25, 12.5, 25, 50, 100, 200, 500 and 1000µM were selected and dispersed in 100 mL bacterial suspension with a varying bacterial cell density viz. 1×10³, 1×10⁴, 1×10⁵, 1×10⁶ and 1×10⁷ CFU ml^− 1. The four different exposure time were selected to evaluate the bacterial reduction at different time interval such as 15, 30, 45 and 60 min. The experiment was conducted at room temperature. At every time interval, the SPIONs were separated from the suspension by using the magnet and 0.5 mL supernatant was collected at every time interval. The collected supernatant was spread on an agar plate to count bacterial colonies by the TPC method. A control treatment was performed without exposing SPIONs. For each nanoparticle concentration, the experiment was conducted in triplicate and average mean value was used to calculate the antibacterial activity of exposed SPIONs at different time interval against various bacterial cell count.

$$\text{B}\text{a}\text{c}\text{t}\text{e}\text{r}\text{i}\text{a}\text{l} \text{r}\text{e}\text{m}\text{o}\text{v}\text{a}\text{l} \text{p}\text{e}\text{r}\text{c}\text{e}\text{n}\text{t}\text{a}\text{g}\text{e} =\frac{\text{C}\text{F}\text{U}0 – \text{C}\text{F}\text{U}\text{t} }{\text{C}\text{F}\text{U}0}\text{X} 100$$

Where CFU₀ is the initial bacterial number, and CFU_t is the number of colonies in the G-SPIONs treated supernatant (El-boubbou et al. 2007).

Statistical analysis

Results of the present study were expressed as the mean ± standard error. Different parameters were analysed by one-way analysis of variance (ANOVA), and the significance of differences among the experimental groups was assessed by Duncan multiple range test. The significance level was accepted at a 5% level (P < 0.05). EC₅₀ values and confidence intervals were calculated using EPA Probit Analysis Program V. All statistical analysis was performed using SPSS, version 22.0 (SPSS Inc., USA).

In the present study, the co-precipitation method was used to synthesize SPIONs. It is most widely cost-effective, simple and high yield production method (Saqib et al. 2019). In our previous study, the SPIONs were characterized by UV–Vis spectrophotometer, DLS, FT-IR, FEG-TEM, XRD, and VSM analysis published by Kumar et al. (2021). The E. tarda is a major threats in aquaculture Worldwide by causing edwardsiellosis in the fresh and brackish water fishes such as tilapia, rohu, catla, catfish, silver carp, Pangasius is turbot, pangas Japanese flounder, European eel etc. (Xu and Zhang 2014; Kerie et al. 2019). This disease is not only found in cultivated fish, but also in wild species such as European eels in natural wetlands (Alcaide et al. 2006). It has been found to cause serious infections such as hemorrhagic septicaemia, skin lesions, and internal organ damage, resulting in increased mass mortality in many fish species (Dubey et al. 2018). Hence, in the present study, the antibacterial effect of different concentration of SPIONs viz. 0, 6.25, 12.5, 25, 50, 100, 200, 500 and 1000 µM were checked against E. tarda with various initial bacterial load 1 × 10³, 1 × 10⁴, 1 × 10⁵, 1 × 10⁶ and 1 × 10⁷ CFU ml^− 1 along with four exposure time 15, 30, 45 and 60 min. Several pieces of research have been conducted for the removal of bacteria from water using SPIONs for removal of aquatic bacteria with minimum permissible and nil bacterial load for aquaculture system without wasting the billions of water in daily routine or using the banned antibiotics for treatment of bacterial disease of fishes.

At lowest bacterial load of E. tarda 1 × 10³ CFU ml^− 1 in water, 100% antibacterial activity was observed by higher concentration of SPIONs 500 and 1000 µM at 45 and 15 min respectively (Fig. 1). While the lower concentration of SPIONs did not showed complete removal of bacterial load form water. At the bacterial load of 1 × 10⁴ CFU ml^− 1, the 11.15 and 26.22% bacterial load were removed after 15 min exposure at 6.25 and 12.5 µM of SPIONs which were increased up to 24.31 and 39.77% by increasing the exposure time (60 min) (Fig. 2). The 88.43 and 94.29% antibacterial activity was observed at 15 min by increasing the SPIONs concentration 500 and 1000 µM which will increase up to 93.19 and 98.96% by increasing the exposure time (60 min). The results indicated that low bacterial loads require less time of exposure and SPIONs concentration. In other words, with the increasing concentration of SPIONs and exposure time, the bacterial removal efficiency also increased. At an initial bacterial load of E. tarda 1 × 10⁵ CFU ml^− 1, the bacterial removal efficiency was increased from 17.31 to 96.27% by increasing the SPIONs concentration from 6.25 to 1000 µM after 60 min exposure (Fig. 3). Meanwhile, the antibacterial activity reached from 8.36 to 92.62% by increasing the SPIONs concentration 6.25 to 1000 µM after 60 min exposure at initial bacterial load of 1 × 10⁶ CFU ml^− 1 (Fig. 4). At lower SPIONs concentration, the significant antibacterial activity did not observed at both the bacterial load 1 × 10⁵ CFU ml^− 1 to 1 × 10⁶ CFU ml^− 1. Still, the 100% bacterial reduction did not occur in both initial bacterial load (1 × 10⁵ CFU ml^− 1 and 1 × 10⁶ CFU ml^− 1) even at highest SPIONs concentration. It was also found that the bacterial removal efficiency was decreased at high initial bacterial loads as compared to low initial bacterial load. In the present study, the highest initial bacterial load was 1 × 10⁷ CFU ml^− 1, at this bacterial load, a significant (p < 0.05) dose-dependent effect of SPIONs concentration was observed, and the bacterial removal efficiency increased significantly as the concentration of SPIONs as well as exposure time increased (Fig. 5). At higher initial bacterial load (1 × 10⁷ CFU ml^− 1), the bacterial removal efficiency of SPIONs was also not reached up to 100% even at highest SPIONs concentration (1000 µM) and even after 60 min exposure. The maximum bacterial removal efficiency 85.32% was found at the highest level of SPIONs (1000 µM) after 60 min exposure.

The effective concentration (EC₅₀) of SPIONs at which 50% of bacterial cell reduction occurred at an initial bacterial load of 1 × 10³ CFU ml^− 1 was estimated to be 61.36, 47.08, 36.56 and 30.88 µM of SPIONs concentration at different time interval 15, 30, 45 and 60 min (Table 1), however at initial bacterial load 1 × 10⁴ CFU ml^− 1, the estimated concentration was to be 132.49, 97.61, 75.88 and 55.05 µM at different time interval 15, 30, 45 and 60 min (Table 1). For removing the 50% bacterial population of E. tarda with cell density 1 × 10⁵ CFU ml^− 1, the effective concentration was estimated to be 206.96, 163.84, 133.12 and 105.58 µM of SPIONs and for initial cell density 1 × 10⁶ CFU ml^− 1 was detected to be 317.40, 252.57, 219 and 188.47 µM different exposure time 15, 30, 45 and 60 min respectively (Table 1). For 50% reduction of E. tarda bacterial population of E. tarda at highest cell density 1 × 10⁷ CFU ml^− 1, the effective concentration of SPIONs was decreased with increasing the exposure time, which was 548.23, 484.38, 334.81, 372.80 µM at different time interval 15, 30, 45 and 60 min respectively (Table 1).

Table 1

Effective concentration of SPIONs at different incubation time for various bacterial load.
Bacterial load	Effective concentration of SPIONs (µM) at different time intervals
	15 min	30 min	45 min	60 min
1× 10³ CFU ml^− 1	61.36	47.08	36.56	30.88
1× 10⁴ CFU ml^− 1	132.49	97.61	75.88	55.05
1× 10⁵ CFU ml^− 1	206.96	163.84	133.12	105.58
1× 10⁶ CFU ml^− 1	317.40	252.57	219.00	188.47
1× 10⁷ CFU ml^− 1	548.23	484.38	334.81	372.80

Independent of the surface charge of bacterial cells, the nanoparticles showed broad spectrum antibacterial activity. (Chatzimitakos and Stalikas, 2016; Gudkov et al. 2021), metal oxide nanoparticles exert the antibacterial activity by changing the internal homeostasis and metabolic activity of bacterial cells (Li et al. 2018; Saqib et al. 2019). SPION's antibacterial activity is thought to be mediated by one of three mechanisms: oxidative stress induction, metal ion release, or non-oxidative mechanism (Wang et al. 2017; Li et al. 2018; Huseen et al. 2021). The nanoparticle caused oxidative stress and produced reactive oxygen species (ROS), which caused damage to bacteria's primary cellular components i.e. DNA, protein, ribosomes, lysosomes, changes in the permeability of cell membrane, and changes in genes expression lead to cause the bacterial cell death (Xu et al. 2016). According to Gabrielyan et al. (2019), IONPs showed antibacterial action against Gram-negative E. coli and Gram-positive Enterococcus hirae bacteria by altering redox potential, boosting ATPase activity, and decreasing H+-fluxes through the bacterial membrane by increasing ROS generation. Similarly, De Toledo et al. (2018) reported the IONPs showed the ROS dependent antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa. The antimicrobial capabilities of IONPs have been exploited in several studies against diverse bacterial species (Arakha et al. 2015; Dinali et al. 2017; Wang et al. 2017; Ramos et al. 2018; Li et al. 2018; Saqib et al. 2019; Huseen et al. 2021; Kumar et al. 2022). In the present study, the antibacterial activity of SPIONs E. tarda was observed due to the small size (10 nm) of nanoparticles. Similarly in our previous study, the antibacterial activity of SPIONs was observed against A. hydrophila (Kumar et al. 2021). Lee et al. (2008) and Hsueh et al. (2017) suggested that the small size of nanoparticles (10–80 nm) easily penetrating into the bacterial cell membrane could be the reason for the antibacterial activity of nanoparticles.

In the present study, the antibacterial activity of SPIONs was observed at every bacterial load, though the activity was reduced with increasing the bacterial load from 1×10³ to 1×10⁷ CFU ml^− 1. When the bacterial load was low, the number of bacterial cells was less as compared with SPIONs particle counts while, opposite trend was observed in case of higher bacterial load which cannot remove cent percent bacterial load. In our previous study, the bacterial removal efficiency of SPIONs against A. hydrophila was decreases with increasing the bacterial load1×10³ to 1×10⁷ CFU ml^− 1 (Kumar et al. 2021). In a recent investigation, the bacterial removal efficiency against E. tarda and A. hydrophila decreased as the bacterial load of both species increased from 1×10³ to 1×10⁷ CFU ml^− 1 (Kumar et al. 2022). Similar to our present study, by increasing the bacterial cell number of E. coli, the antibacterial activity of magnetic barium phosphate nanoflakes with embedded iron oxide nanoparticles decreased (Song et al. 2018).

In the current study, the antibacterial activity against E. tarda increased with increasing SPIONs concentrations 6.25 to 1000 µM as well as exposure time from 15 to 60 min. The dose-dependent antibacterial activity of polyvinyl-coated IONPs against S. aureus (5×10⁴ CFU ml^− 1) was observed with increasing the concentration of nanoparticles from 3 µg/mL to 30 mg/L in tryptic soy broth (Tran et al. 2010). The antibacterial activity of IONPs against E. coli at initial bacterial load 1×10⁷ CFU ml^− 1 was increased with increasing the concentration of nanoparticles 5 to 10 mM and the exposure time 4 to 6 hr (Li et al. 2018). Bhuiyan et al. (2020) also observed the dose-dependent antibacterial activity of IONPs against S. aureus by the agar plate method. The 7 ± 1 mm zone of inhibition was measured at lower nanoparticle concentration (5 mg/mL), which was increased almost doubled (12.5 ± 0.5 mm) by increasing nanoparticle concentration 30 mg/mL. Similarly, Arakha et al. (2015) also observed the dose-dependent antibacterial activity of IONPs against B. subtilis and E. coli. IONPs have been found to have dose-dependent antibacterial activity against a variety of bacteria, including E. coli, S. aureus, B.subtilis, Shigella, A.niger, and Candida albicans (Sandhya and Kalaiselvam 2020). The bacterial inhibitory activity of IONPs against E. coli increased with increasing the nanoparticle concentrations 1 to 100 mg/L and exposure time 30 min to 24 hr (Vihodceva et al. 2021). The antibacterial activity of SPIONs against A. hydrophila was increased with increasing SPIONs concentration 6.25 to 1000 µM and exposure time 15 to 60 min (Kumar et al. 2021). Similarly, the antibacterial activity of glucose conjugated SPIONs against A. hydrophila and E. tarda was also increased with increasing concentration of glucose conjugated SPIONs 1.5 mg/L to 240 mg/L and exposure time 15 to 60 min (Kumar et al. 2022)

The research will pave the path for new approaches to synthesis low-cost SPIONs as a novel antibacterial agent for removing the fish disease Edwardsiellosis from water and preventing disease outbreaks in culture systems. The SPIONs were synthesized in current study found to have an efficient antibacterial activity against E. tarda. The antibacterial activity was increased with increasing the SPIONs concentration 6.25 to 1000 µM and exposure time 15 to 60 min. By increasing the bacterial cell density from 1×10³ to 1×10⁷ CFU ml^− 1, the antibacterial activity was decreased. To remove higher bacterial cell number from water require higher concentration of SPIONs while lower nanoparticle concentration require to remove higher bacterial load. It is concluded that the SPIONs as a potential antibacterial/biocidal agent for removing E. tarda from water. Further, SPIONs from the treated water are easily removed using a magnet makes it highly user-friendly to treat the culture water.

Ethical approval: All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Consent to participate: All the authors agree to participate in this experiment.

Consent for publication: All the authors of this article agree to the publication.

Availability of data and material: All the date are included in the manuscript.

Conflict of interest: The authors declare no competing interests.

Funding details: No funding provided for this work.

Author’s contribution: Munish Kumar, conducted experiments, experimental sampling, sample processing, data analysis, results interpretation and manuscript writing. Gyandeep Gupta help in experimental sampling,data analysis and manuscript preparation. Tincy Varghese help in experimental results interpretation and manuscript writing and correction. Prem Prakash Srivastava help in designing of experiment, statistical analysis,data interpretation and manuscript correction. Subodh Gupta, as a major advisor help in conceptualization of experimental design, interpretation of experimental result, manuscript writing and correction.

Acknowledgements: The authors are thankful to the Director and Vice-chancellor, ICAR-Central Institute of Fisheries Education, Mumbai, for providing facilities. The first author acknowledges the Indian Council of Agricultural Research, New Delhi, for the PhD research fellowship at ICAR-CIFE, Mumbai. The authors acknowledge the Sophisticated Analytical Instrument Facility, Indian Institute of Technology, Mumbai, Roorkee, and the National Centre for Nanoscience and Nanotechnology, University of Mumbai.

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Antibacterial activity of super-paramagnetic iron oxide nanoparticles against Edwardsiella tarda from water

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