Abstract

The study is concerned with the designing of a pressure-free filtration system that contains a polyvinyl alcohol (PVA)/chitosan (CS) polymeric membrane integrated with silver nanoparticles (AgNPs) for the purification of microbe-contaminated water. The AgNPs were greenly synthesized using culture filtrate of Bacillus endophyticus. PVA/CS membrane was prepared, integrated with washed and unwashed silver nanoparticles, and their proper integration was characterized using Fourier transform infrared (FTIR) spectroscopy, thermogravimetric analysis (TGA), scanning electron microscopy (SEM), transmission electron microscopy (TEM), particle size analyzer (PSA) and mechanical properties. The membrane was tested against six pathogenic microbes and showed potent antimicrobial activity especially against Klebsiella pneumoniae. A tap water sample was passed through the filtration system and tested for its microbial content before and after filtration. The obtained results showed that the optical densities of the tap water before the treatment and after the passage through the PVA/CS membrane were 1.397 and 1.214, respectively, with almost 88% of the original microbial content. The optical density of the tap water after passage through PVA/CS–washed AgNPs membrane was close to zero. The repeated observations resulting from the obtained optical densities of treated and untreated water refer to the future applicability of the prepared materials and the designed system for the safe purification of microbe-contaminated water for drinking, industrial or pharmaceutical purposes.

INTRODUCTION

Silver nanoparticles (AgNPs) are gaining much interest due to their superior physiochemical properties (Zhang et al. 2016), which recommend them to be used in various applications, including water treatment (Kolya et al. 2015). On the other hand, silver nanoparticles (AgNPs) are considered as one of the most vital and fascinating nanomaterials that are involved in various bio-applications, including antimicrobial (Kolya et al. 2015) and biomedical applications (Burduşel et al. 2018). To meet the increasing demands for commercial nanoparticles, new eco-friendly (green) methods of synthesis are being discovered, where (AgNPs) are precipitated from their salt solutions using microorganisms (Magdi et al. 2014), or biomaterials, such as plant extracts (Kolya et al. 2015; Khan et al. 2018). Polyvinyl alcohol/chitosan (PVA/CS) composite is attractive to researchers because of noticeable features related to CS and PVA individually. The combination of these two membranes may be appropriately designed to yield unique processes in the fields of energy, sensors, engineering, and chemical sciences (Chauhan et al. 2014; Habiba et al. 2017). CS is derived from chitin and has recently attracted increasing interest both in research and developmental aspects. Because of its excellent properties, CS has several applications including filtration, removal of heavy metal ions, tissue and biomedical engineering, food preservation, environmental applications, and adsorption processes (Vakili et al. 2014; Kyzas et al. 2015). PVA is a typically non-toxic and soluble-in-water synthetic polymer. It is a biocompatible and biodegradable material. Because of the properties compatible with those of PVA, it is believed that a membrane of CS and PVA, especially in the form of structures, can lead to novel functional biodegradable materials for particular applications (Karimi et al. 2014). The aim of this work was to design and fabricate a pressure-free system including a polymeric integrated silver nano-particle membrane for the safe purification of water that might be invaded with pathogenic microbes. The purified water could be safely used for various industrial applications, drinking water or irrigation purposes.

MATERIALS AND METHODS

Microbial pathogens

The pathogenic microbes Pseudomonas aeruginosa ATCC9027, Escherichia coli NCTC10418, Bacillus cereus ATCC6633, Candida albicans ATCC 700, Vibrio cholerae ATCC700 and Klebsiella pneumoniae ATCC13883 were kindly provided by the National Institute of Oceanography and Fisheries (NIOF), Alexandria, Egypt.

Chemicals

Chitosan (purity >90%, purchased from Biobasic, Canada), PVA (with an average MW of 72,000 g/mol, purchased from Merck, Germany), acetic acid (assay ≥99%, obtained from Sigma-Aldrich Chemicals, Ltd, Germany).

Green synthesis of silver nanoparticles

The biosynthesis of silver nanoparticles was achieved using the bioproducts produced by Bacillus endophyticus strain KF011545. Luria Bertani broth (LB) without sodium chloride (yeast extract, 5 g/l; peptone, 10 g/l; and distilled water, 1,000 ml) was prepared and sterilized through autoclaving at 120 °C and 15 psi for 20 min. A single colony of the bacterial strain was transferred into 10 ml nutrient broth and was incubated at 30 °C and 150 rpm for 24 h as a pre-culture inoculum. One ml of the bacterial pre-culture was inoculated into 100 ml of the sterilized LB broth followed by incubation at 30 °C and 150 rpm for 48 h. After incubation, the whole culture was centrifuged at 10,000 rpm for 20 min, followed by filtration through 0.45 μm Millipore syringe filters to eliminate any residual microbial cells. The filtered solution (supernatant) including all the microbial metabolites was used as the raw material for the biosynthesis of silver nanoparticles through the addition of crystals of AgNO3 to obtain 1 mM as a final concentration. The mixture was incubated at 30 °C and 150 rpm for 3 days until the appearance of a dark brown color (Peiris et al. 2017).

Separation of silver nanoparticles (AgNPs)

The solution containing the AgNPs was divided into two equal parts. The first part was used immediately without modifications for the subsequent experiments and is referred to as unwashed AgNPs. The other part was subjected to centrifugation at 15,000 rpm for 30 min to spin down the formed AgNPs away from the medium components and is referred to as washed AgNPs. The collected nanoparticles were washed twice with absolute ethanol and once by distilled water and were then dried at 50 °C for 18 h and re-suspended in distilled water for characterization and further experimental work.

Preparation of PVA/CS–silver nanoparticle membrane

The polymer membrane was prepared by the casting method. Chitosan solution (2% w/v) was prepared by dissolving chitosan in 2% acetic acid solution at room temperature with stirring (400 rpm). The PVA solution (8% w/v) was prepared in distilled water. The solutions of PVA and chitosan were carefully mixed at the ratios 80:20 (%) with stirring (400 rpm) for 2 h. The control batch was not supplemented with any additives. AgNPs was added to the film-forming solution at a concentration of 25 mg/50 ml of unwashed AgNPs and washed AgNPs. All the membrane-forming mixtures were blended by stirring on a magnetic stirrer (400 rpm) at room temperature for 3 h. The membranes were prepared by casting an amount of 15 ml of each solution on Petri plates. After dryness, all formed membranes were characterized as follows.

Characterization of prepared materials

Fourier transform infrared (FTIR) spectroscopy (Shimadzu FTIR-8400 S, Japan) was used to identify the presence of functional groups in both the AgNPs and PVA/CS membranes and to confirm the chemical structure of PVA/CS-AgNPs membranes. Thermogravimetric analysis (TGA, Shimadzu TGA-50) was used to determine the weight loss and thermal degradation of both the AgNPs and prepared membranes. Surface and internal cross-section imaging of AgNPs, PVA/CS, and PVA/CS–AgNPs membranes were performed using scanning electron microscopy (SEM) (Ahmadi et al. 2013) (JEOL, JSM-6360LA, Japan). More characteristic analyses were performed for AgNPs using transmission electron microscopy (TEM, JEOL JEM-2100 plus, Japan) and particle size analyzer (PSA, Beckman Coulter, USA). The tensile strength of the polymer electrolyte membranes was measured using a universal testing machine (Shimadzu UTM, Japan), at room temperature. The measurements were carried out at constant speed of crosshead movement (3 mm/min).

Antimicrobial activity of PVA/CS–AgNPs membranes against pathogenic microbes

The antimicrobial activity of the prepared polymer integrated AgNPs was tested against six pathogenic bacteria and yeast using the disc diffusion method. A pure single colony of each pathogen was cultivated in 10 ml LB broth and incubated at 30 °C with shaking at 150 rpm for 24 h. After incubation, the turbid broth of each pathogen was aseptically diluted to 0.5 McFarland, followed by the spreading of 100 μl over LB agar plates using sterile cotton swabs. After complete dryness, discs with 0.7 mm diameter of blank polymer, or the two types of polymer integrated AgNPs (washed and unwashed AgNPs), were loaded over the surfaces of the inoculated LB plates. The plates were incubated at 30 °C for 24 h followed by checking and measuring the diameters of the formed inhibition zones.

Filtration of tap water sample using PVA/CS–AgNPs membranes

The ability of the prepared membranes to allow the through-pass of a tap water sample and remove the microbes existing in the water was investigated. At the beginning, 100 ml of the real water sample was added to the filtration system, where the water was allowed to pass without external pressure but depending on the force of gravity. The filtration system was used to control the prepared polymeric-AgNPs membrane (5 cm diameter and 2.35 mm thickness) in the middle between two separated chambers (Figure 1). The upper chamber was specified to receive the untreated water (microbe-containing water), while the lower chamber was specified to receive the filtered water sample (presumptively: microbe-free water).

Figure 1

Design of filtration system for the elimination of microbes from probable contaminated water.

Figure 1

Design of filtration system for the elimination of microbes from probable contaminated water.

Detection of filtration system efficacy in water purification

The designed filtration system was used to investigate the microbial content of the tested water sample, before and after filtration. Three water samples, one before the filtration, which was the raw tap water, and two after the filtration (one passing through the PVA/CS membrane and the other passing through the membrane of PVA/CS–washed AgNPs) were tested for their microbial content. A volume of 50 μl of each sample (one raw tap water and two filtered water samples) was inoculated into 10 ml of sterile LB broth followed by incubation at 30 °C, 150 rpm for 24 h. After incubation, the optical density (OD600 nm) of each sample was measured and recorded using uninoculated LB broth as a blank.

RESULTS AND DISCUSSION

Characterization of prepared materials

Fourier transform infrared spectroscopy

FTIR spectroscopy was utilized for the identification of the functional groups involved in the formation of washed AgNPs, PVA/CS membrane, and PVA/CS–AgNPs (both of washed and unwashed AgNPs) membrane. Figure 2 shows the FTIR spectra of AgNPs, PVA/CS, and PVA/CS-AgNPs membranes. PVA and CS exhibited a characteristic broad-band OH group signal at 3,568–3,037 cm−1. The bands at 2,949 cm−1 are ascribed to symmetric stretching of CH2 while the bands at 1,118.75 cm−1 are due to CH wagging vibrations. For the CS component of the membranes, the characteristic broad band of NH2 absorption from O-C-NH2 groups is observed at 1,653.05 cm−1. The bands at 1,697.41 cm−1 are characteristic of carboxylic acid, from the acetic acid which was used for CS dissolution (Abu-Saied et al. 2017).

Figure 2

FTIR spectra of samples (a) AgNPs, (b) PVA/CS membrane, (c) PVA/CS–unwashed AgNPs and (d) PVA/CS–washed AgNPs.

Figure 2

FTIR spectra of samples (a) AgNPs, (b) PVA/CS membrane, (c) PVA/CS–unwashed AgNPs and (d) PVA/CS–washed AgNPs.

Thermogravimetric analysis

TGA is widely used to investigate the thermal decomposition of polymers and nanoparticles. The TGA thermograms of PVA/CS membrane and PVA/CS–AgNPs washed and unwashed, at a heating rate of 20 °C/min under a nitrogen atmosphere, are shown in Figure 3(a). The PVA/CS weight change between 26 and 240 °C is associated with the loss of adsorbed and bound water. PVA/CS membrane degradation started at 180 °C and continued up to 400 °C, with 69.651% polymer weight loss, while, up to 800 °C, 94.596% is lost. PVA/CS–unwashed silver nanoparticles reached polymer degradation up to 482.36 °C with 81.651% polymer weight loss, while up to 800 °C it was with 97.741% weight loss. PVA/CS–washed AgNPs reached polymer degradation up to 490.34 °C with 79.608% polymer weight loss, while up to 800 °C it was with 95.184% weight loss.

Figure 3

Thermogravimetric analysis of (a) PVA/CS membrane, PVA/CS–unwashed AgNPs and PVA/CS–washed AgNPs; (b) AgNPs.

Figure 3

Thermogravimetric analysis of (a) PVA/CS membrane, PVA/CS–unwashed AgNPs and PVA/CS–washed AgNPs; (b) AgNPs.

Figure 3(b) shows the TGA of the biosynthesized AgNPs when heated from room temperature to 500 °C. The initial weight loss (∼98.5%) observed below 100 °C was attributed to the water molecules present in the AgNPs. Another slight weight loss (<1%) behavior observed below 350 °C is most likely a consequence of the surface desorption of bioorganic compounds present in the nanoparticle powder. The final weight loss (<0.5%) observed above 350 °C is due to a phase transformation of the silver nanoparticles. This behavior is similar to that recorded by Khan and his colleagues (Khan et al. 2018).

Tensile strength

Tensile properties of the maximum force and elongation were measured, and the results are listed in Table 1. Two mechanical strength parameters (tensile strength and elongation) were increased with polymer including silver nanoparticles from 22.67 to 25.70 (using washed silver nanoparticles), while the maximum increase of PVA/CS–unwashed AgNPs was 45.91 MPa. On the other hand, the elongation increased from 33.4 mm to 34.30 mm (PVA/CS–unwashed AgNPs), which was oppositely observed in the case of PVA/CS–washed AgNPs.

Table 1

Tensile strength and elongation of PVA/CS, PVA/CS–washed AgNPs, and PVA/CS–unwashed AgNPs membranes

Elongation at break (mm)TS (MPa)Sample
33.40 22.67 PVA/CS 
34.30 45.91 PVA/CS–unwashed AgNPs 
29.03 25.70 PVA/CS–washed AgNPs 
Elongation at break (mm)TS (MPa)Sample
33.40 22.67 PVA/CS 
34.30 45.91 PVA/CS–unwashed AgNPs 
29.03 25.70 PVA/CS–washed AgNPs 

Particle size analyzer

As shown in Figure 4, PSA results reported that the particle size distribution of the obtained AgNPs is polydispersed in nature, with average diameter ∼66 nm. However, this result is in agreement with those prepared using PVA as stabilizer (Zielińska et al. 2009), which did not occur in our study.

Figure 4

PSA histogram of biosynthesized AgNPs.

Figure 4

PSA histogram of biosynthesized AgNPs.

Scanning electron microscopy

SEM micrographs of the surface of PVA/CS and PVA/CS of washed and unwashed AgNPs are shown in Figure 5. PVA/CS appears to have a smooth and homogeneous surface (Figure 5(b)). Likewise, the surface of PVA/CS of washed and unwashed AgNPs is also smooth with no pores and no evidence of significant phase separation. The formation of homogeneous blends of washed and unwashed AgNPs and PVA was probably caused by the presence of extensive hydrogen bonding between the functional groups of the two polymers (–OH and –NH2 groups in chitosan and –OH groups in PVA) (Abu-Saied et al. 2017).

Figure 5

SEM micrographs of (a) AgNPs, (b) PVA/CS, (c) PVA/CS–washed AgNPs and (d) PVA/CS–unwashed AgNPs membranes.

Figure 5

SEM micrographs of (a) AgNPs, (b) PVA/CS, (c) PVA/CS–washed AgNPs and (d) PVA/CS–unwashed AgNPs membranes.

On the other hand, the cross-sections of the prepared membranes showed that two of the three membranes were pored with the appearance of perforated cuts, which indicates the ability of these membranes to allow the water molecules to pass from one side to the other (Figure 6(a) and 6(b)). However, the micrograph of the third membrane (Figure 6(c)) exhibits solid and slimy shaped cuts, which appear as un-perforated cuts. These observations could indicate the inability of this membrane to allow water or any other solution to pass through.

Figure 6

SEM cross-section micrographs of (a) PVA/CS, (b) PVA/CS–washed AgNPs and (c) PVA/CS–unwashed AgNPs membranes.

Figure 6

SEM cross-section micrographs of (a) PVA/CS, (b) PVA/CS–washed AgNPs and (c) PVA/CS–unwashed AgNPs membranes.

Transmission electron microscopy

In the TEM micrographs the biosynthesized AgNPs were found to be spherical and monodispersed (Figure 7). The sizes of the obtained nanoparticles were in the 30–100 nm range, which is in agreement with the PSA recorded data. Both the shape and size of the obtained AgNPs strongly depend on the reducing and stabilizing agents of the microbial filtrate. Due to that, the synthesis of silver nanoparticles typically involves ‘bottom-up’ reduction of silver salts, most commonly silver nitrate (Hu & Hsieh 2016). Table 2 presents some examples of various AgNPs morphologies prepared through different preparation methods compared with our study (Abou-Okeil et al. 2012; Gopinath et al. 2012; Agnihotri et al. 2014; Gannimani et al. 2016). Study of AgNPs morphologies is important due their effect on efficiency as explained by Pal and his colleagues (Pal et al. 2007).

Table 2

Previously published data on the shapes and sizes of AgNPs compared with the present results

Preparation methodCapping agentShapeSize (nm)ApplicationReference
Biosynthesized  Spherical 30–100  Current results 
Chemical Capped with cyclodextrin Spherical 20–30 Antibacterial Gannimani et al. (2016)  
Biosynthesis  Cubic 16–28 Antimicrobial Gopinath et al. (2012)  
Chemical Using aminated-cyclodextrin Spherical 40–80  Abou-Okeil et al. (2012)  
Co-reduction approach  Spherical 5–100 Antimicrobial Agnihotri et al. (2014
Preparation methodCapping agentShapeSize (nm)ApplicationReference
Biosynthesized  Spherical 30–100  Current results 
Chemical Capped with cyclodextrin Spherical 20–30 Antibacterial Gannimani et al. (2016)  
Biosynthesis  Cubic 16–28 Antimicrobial Gopinath et al. (2012)  
Chemical Using aminated-cyclodextrin Spherical 40–80  Abou-Okeil et al. (2012)  
Co-reduction approach  Spherical 5–100 Antimicrobial Agnihotri et al. (2014
Figure 7

TEM micrograph of the biosynthesized AgNPs.

Figure 7

TEM micrograph of the biosynthesized AgNPs.

Antimicrobial activity of PVA/CS–AgNPs

The effect of PVA/CS–AgNPs against six microbial pathogens was investigated. Most of these selected pathogenic microbes are known for their human pathogenicity; however, contaminated water is the probable source of infection transmission. For instance, Vibrio cholerae has caused millions of deaths in developed and developing countries through contaminated water as reported by Pandey et al. (2014). Similarly, Pseudomonas aeruginosa and Escherichia coli have also been reported to be transmitted by contaminated water resources.

The ability of the three tested membranes (PVA/CS membrane, membrane of PVA/CS–unwashed AgNPs, and membrane of PVA/CS–washed AgNPs) to halt microbial growth was varied (Table 3). In some cases, the antimicrobial activity was limited to the AgNPs alone, while, in other cases, both synergistic and antagonistic effects of the polymers and AgNPs were detected.

Table 3

Antimicrobial activities of PVA/CS membrane integrated with washed and unwashed AgNPs against microbial pathogens

SampleMicrobial strains/clear zone (mm)
S1S2S3S4S5S6
PVA/CS membrane 15 13 16 
Membrane of PVA/CS–unwashed AgNPs 
Membrane of PVA/CS–washed AgNPs 16 14 15 
SampleMicrobial strains/clear zone (mm)
S1S2S3S4S5S6
PVA/CS membrane 15 13 16 
Membrane of PVA/CS–unwashed AgNPs 
Membrane of PVA/CS–washed AgNPs 16 14 15 

S1: Vibrio cholerae; S2: Candida albicans; S3: Pseudomonas aeruginosa; S4: Escherichia coli; S5: Klebsiella pneumoniae; S6: Bacillus cereus.

The pathogenic strains Pseudomonas aeruginosa, Escherichia coli, and Bacillus cereus were only affected by the membrane of PVA/CS–washed AgNPs with clear zone diameters of 9, 14 and 15 mm, respectively (Table 3), while the PVA/CS membrane failed to show any antimicrobial activity against the same pathogens. These results indicate that the AgNPs are the main antimicrobial effector, while the effect of polymeric materials is negligible. The antimicrobial effect of AgNPs against Pseudomonas aeruginosa (Yuan et al. 2017), Escherichia coli (Mahmoud et al. 2016), and Bacillus cereus as has been previously reported (Ahmadi et al. 2013).

Moreover, a synergistic effect was detected against the Candida albicans strain, where the PVA/CS membrane showed a clear zone with 13 mm diameter, which was increased to 16 mm after the integration of AgNPs with the membrane (membrane of PVA/CS–washed AgNPs). It has formerly been shown that the chitosan membrane has antifungal activity against Candida albicans (Peña et al. 2013), while the capping of AgNPs with polymeric materials can enhance both the aggregation stability and antimicrobial activity of the nanoparticles (Panáček et al. 2016), which is almost matched with our results.

In addition, an antagonistic effect was detected against the strains Vibrio cholerae and Klebsiella pneumoniae. The PVA/CS membrane was able to stop the microbial growth and recorded 15 and 16 mm clear zones against the strains Vibrio cholerae and Klebsiella pneumoniae, respectively. The addition of washed AgNPs to the polymeric membrane showed a reduction of antimicrobial activity to close to zero. These results indicate that the AgNPs showed an antagonistic effect against these two bacteria. On the other hand, the membrane of PVA/CS–unwashed AgNPs failed to halt the growth of all tested pathogens indicating, from our point of view, that the residual broth components covered the surfaces of the polymeric materials and AgNPs and prevented them from releasing and exerting their antimicrobial activities.

We could attribute the different effects of the tested membranes against the tested pathogens to the physiological response of each microbial strain against the tested materials, which varied among the microbes. In addition, the observed differences may also be related to the ability of microbes to resist the antimicrobial effect of chitosan and hence, the exerted antimicrobial activity will either be exclusive to silver nanoparticles or to silver nanoparticles combined with chitosan. For more clarification, the chitosan/PVA showed antimicrobial activity against 50% of the tested microbes, while it did not show any antimicrobial activity against 100% of tested microbes when combined with unwashed silver nanoparticles (antagonistic effect). However, it showed higher antimicrobial activity when combined with washed silver nanoparticles (synergistic effect). This means that the effect is linked to both the microbial behavior against specific compounds and the type of applied materials.

Detection of filtration system efficacy in water purification

The three tap water samples including unfiltered tap water, tap water filtered through PVA/CS membrane, and tap water filtered through PVA/CS–AgNPs membrane with a flux rate of 45 ml/h were tested for their microbial content through inoculation into sterile LB broth. The obtained results revealed that the microbial content of the tap water filtered through PVA/CS membrane (OD600 1.397) was close to the microbial content of the unfiltered tap water (OD600 1.214) with 88% of the microbial content compared with the original unfiltered tap water content (Figure 8), which indicates that the PVA/CS membrane could neither prevent the passage of microbes nor kill them. However, the microbial content of the tap water filtered through PVA/CS–AgNPs membrane was approximately undetected (OD600 0.003) (Figure 8), which indicates that the integrated AgNPs were able to either prevent the passage of the water-existed microbes or kill them. Moreover, it is worth mentioning that no pressure was applied to push the water molecules to pass through the membranes from the upper chamber to the lower chamber. This property is a good sign for the future applicability of the designed system to be used for drinking water treatment machines. Khaydarov and his colleagues showed that AgNPs can attach to fibrous sorbents and prevent the growth and biofilm formation of pathogenic microbes during water treatment processes (Khaydarov et al. 2019).

Figure 8

Optical densities of LB growing microbes of filtered and unfiltered water samples.

Figure 8

Optical densities of LB growing microbes of filtered and unfiltered water samples.

On the other hand, no water flow was detected in the lower chamber of the filtration system after using the polymeric membranes integrated with unwashed AgNPs, indicating that the residual components of the broth medium might block the pores of the polymeric membrane and hence the water molecules have no way to pass to the other side, which matches the SEM cross-section micrographs (Figure 5(c)). It worth mentioning that the membrane can be reused several times under a condition of drying, disintegration using a phosphate buffer (pH 7.0), and recasting using similar original casting conditions.

CONCLUSION

It can be concluded that the PVA/CS–washed AgNPs membrane was able to prevent and/or kill the microbes existing in real water samples better than PVA/CS or PVA/CS-un-washed AgNPs membranes. These results represent the promising candidacy of this membrane in applied pressure-free filtration systems for drinking water purification.

ACKNOWLEDGEMENT

The authors extend their appreciation to the Deanship of Scientific Research, King Khalid University, for funding this work through the research groups program under grant number RGP 2/14/40.

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