Abstract

The present research studied the anti-bacterial effect of silver-coated red soil nanoparticles on Gram-negative bacteria Escherichia coli (E. coli) from water. The effects of disinfectant concentration (0.02, 0.05 and 0.1 g/mL), contact time (10, 20 and 30 minutes) and bacteria no. (102, 104 and 106 CFU/mL) have been also investigated. To obtain important factors, the interactions between factors and optimal experimental design in surface response method were used based on Box-Behnken Design. According to the research findings, the system is efficient in eliminating E. coli. The results showed that E. coli elimination efficiency intensified through increasing the amount of disinfectant from 0.02 to 0.1 g/mL. Expanding contact time from 10 minutes to 30 minutes also heightened the E. coli elimination rate. R2 for E. coli elimination is 0.9956 indicating a good agreement between model experimental data and forecasting data.

INTRODUCTION

Concern for the supply of drinking water requirements due to population growth and depletion of drinking water sources is now evident in many countries throughout the world. Water scarcity resulting from increasing environmental pollution has turned water supply and sanitary requirements into one of the main issues of the present world (Leonard et al. 2003). Diseases caused by water contamination have led to the death of tens of thousands people. However, the possibility of refining water provides access to resources for several purposes, and may, in some cases, compensate for water resources scarcity (Vörösmarty et al. 2000). Through the increasing production and consumption in various industries, natural and artificial pollutants have challenged access to traditional water-treatment practices to achieve the required standard as pollutants approach surface and groundwater resources. Sewage discharge to water resources means the source of such water pollution needs to be identified, controlled, and deterred.

The first step is to monitor water pollution. Focus on particular organisms, including the coliform family, must be applied rather than monitoring all parameters to assess pathogenic microbial contamination. The coliform family is not pathogenic and remains in the environment for a relatively long time in large numbers; further, as they are exclusively intestinal, their presence in the environment is an indication of fecal contamination (Ashbolt 2004). Coinciding with the start of drinking water disinfection with chlorine in 1904, outbreaks of epidemics associated with contaminated water consumption was severely reduced (Bryant et al. 1992; Frederick 1998). Then, different methods of drinking water disinfection like ozone and UV light for infection prevention were applied. However, because of the numerous advantages of chlorine and its derivatives, drinking water disinfection using these compounds is globally the most common method of disinfection (Alicia & Alvarez 2000; El-Shafy & Grünwald 2000).

Using new methods is inevitable on account of population growth, the need for water supply, and sanitary requirements due to widespread pollution of water sources. Today, nanotechnology is proposed to solve the issues of water quality and quantity (Bottero et al. 2006). The effect of metal ions on water disinfection has been studied by many scientists (Jain & Pradeep 2005; Deng et al. 2017; Fan et al. 2018; Mnatsakanyan & Trchounian 2018; Motshekga et al. 2018; Park et al. 2018). Silver, copper and zinc ions have been long known for their antimicrobial properties. Some studies have shown that the metal ions react with proteins through binding to sulfhydryl groups (–SH) in enzymes and finally disable proteins (Yoon et al. 2007). If the metals are tiny, they would show better antimicrobial properties as a result of increased surface to volume ratio (Zhang et al. 2008). The metal nanoparticles can be used for coating some parts for anti-microbial properties and filters in medical equipment. Use of these materials offers some challenges, including microbial resistance against chemical antimicrobial agents, but also produces disinfection using conventional disinfectants. Innovation in new technologies on the development of disinfection and water treatment is a new achievement in the field of nanotechnology.

E. coli bacteria is a Streptococcus genus, Gram-positive organism, catalase-negative, oval and non-sporulation, facultative (lactic acid production from lactose) with complex nutritional requirements and exists in most vegetables, herbs and foods, especially foods of animal origin, such as dairy products. Also, it is part of normal intestinal flora of some mammals and humans (Rezaei-Zarchi et al. 2010). Berendjchi et al. (2011) performed a study to evaluate the activity of copper nanoparticles prepared in the form of a coating on cotton layer through sol-gel method. The results revealed that nanoparticles are effective both in Escherichia coli (Gram -ve) and on Staphylococcus aureus (Gram +ve) (Berendjchi et al. 2011). Dong et al. (2011) analyzed antibacterial activity of magnetic nanoparticles (Fe3O4). According to the research results, the modified nanoparticle is more effective against E. coli bacteria. Nanoparticles in a magnetic field can be recovered from the sample (Dong et al. 2011). Cortés et al. (2012) conducted a study to investigate magnetic properties and antibacterial activity of a quad-core copper complex. The results displayed that the 4-phenylamide azole complex is effective for cereus bacteria and other Gram-positive bacteria; whereas, pyridine N-oxide complex and 2-methylamide azole are only effective against Gram-negative bacteria (Cortés et al. 2006). Sanpo et al. (2013) examined spinel ferrite nanoparticle antibacterial activity using citric acid as a chelating agent through the sol-gel method. According to the research findings, zinc and copper substitution in nano-cobalt ferrite particles significantly increases Escherichia coli and Staphylococcus aureus antibacterial activity (Sanpo et al. 2013). Tian et al. (2014) explored nanocomposite antibacterial activity consisting of iron oxide, silver oxide, and graphene oxide nanoparticles as the core, and only compared silver nanoparticles antibacterial activity. According to the research findings, obtained nanocomposites (GO-IONP-Ag) showed more powerful antimicrobial activity than silver nanoparticles; moreover, antibacterial effect was also observed on both Gram-negative bacteria (E. coli) and Gram-positive bacteria (Staphylococcus aureus) (Tian et al. 2014). We thus hypothesize that red soil is a viable filtration–sorption media to consider for practical application of bacteria removal. This media is usually rich with Fe and Al oxides and clay and is widespread in the world, which may lower costs and human dependence on chlorine. The present study aimed to evaluate the effect of silver-coated red soil on E. coli removal in disinfecting water.

MATERIALS AND METHODS

General

This is an applied research carried out at a laboratory experimenting a lyophilized strain of E. coli: ATCC 25922 prepared by a center of fungi collection and industrial bacteria in Iran. All chemical reagents such as silver nitrate (AgNO3; Merck, Germany), NaOH, sodium borohydride and culture medium were of analytical grade (Merck) and were used without further treatment. The red soil used in the present study was collected from Hormoz Island, Hormozgan Province, Iran. Selected basic properties of the red soil used in this study are shown in Table 1.

Table 1

Selected basic properties of the red soil used in this study

pH 5.12 
Specific surface areaa (m2/g) 34.92 
Organic matterb (g/kg) (Nelson & Sommers 19824.11 
Free Fe2O3c (mg/kg) (Van Raij & Peech 197233152.91 
Free Al2O3c (mg/kg) (Van Raij & Peech 19727403.55 
Cation exchange capacityd (mmol/kg) (Thomas 1982110.43 
pH 5.12 
Specific surface areaa (m2/g) 34.92 
Organic matterb (g/kg) (Nelson & Sommers 19824.11 
Free Fe2O3c (mg/kg) (Van Raij & Peech 197233152.91 
Free Al2O3c (mg/kg) (Van Raij & Peech 19727403.55 
Cation exchange capacityd (mmol/kg) (Thomas 1982110.43 

aDetermined by a Micrometrics apparatus (Gemini 2375) by adsorption of nitrogen at 77 K according to the traditional method of Brunauer, Emmet and Teller or BET.

bDichromate method.

cDithionite-citrate-bicarbonate method.

dAmmonium acetate method.

The experiments were carried out according to the standard methods contained in the Standard Methods for Water and Sewage Testing (APHA AWWA WEF 2012).

Silver coating red soil

First, the red soil was ground and, after sifting, 3 g of powdered red soil was extracted and added to 250 ml of distilled water in a 500 ml beaker, which was dissolved in the solution for an hour by vigorous stirring. Then, 0.2361 g of the silver nitrate weighed previously was added to the solution. The solution was mixed for a maximum of 24 hours with a magnetic stirrer. While mixing, 140 ml of freshly prepared solution of sodium borohydride (NaBH4) of 0.04 M (prepared by dissolving 1.5 g of the NaBH4 and 0.5 g of NaOH per liter of distilled water) was added. The resulting mixture was stirred for another hour. The solid and liquid portions were then separated through filter paper. The residue was washed three times with distilled water, dried at 60 °C overnight, and milled to achieve smooth powder. Finally, it was stored in a dark container. Inductively coupled plasma atomic emission spectroscopy (ICP-AES) was applied for determining the amount of the Ag nanoparticle loading on red soil. After coating silver nanoparticles on red soil, its effect on disinfection and removal of Gram-negative bacterium of E. coli from water was investigated (Kooti et al. 2014).

Culture medium

Escherichia coli species were cultured according to the manufacturer guidelines. Briefly, a single colony of E. coli was taken from a refrigerated stock and pre-cultured in 20 mL tryptic soy broth (TSB) by incubation at 37 °C for 24 hours. Then it was transferred into tryptic soy agar (TSA) and incubated for 24 hours at 37 °C. The top of each colony was touched with a sterile loop and the growth was transferred into a tube containing 4 to 5 mL of distilled water (IROST 2016). A McFarland standard 0.5 was used to determine the cell concentrations. The cell density was compared to the standard using a UV/VIS spectrophotometer; an equivalent optical density of 0.1 at 625 nm with regard to the calibrated standard cell suspensions in distilled water (Dhara & Tripathi 2013). A barium sulfate turbidity standard was used to standardize the inoculums density for a susceptibility test, its turbidity was equivalent to that of a 0.5 McFarland standard the latter made according to Garcia (Garcia 2010). To obtain the required cell suspensions, the stock was serially diluted in distilled water. This resulted in a suspension containing approximately 102, 104 and 106 CFU/mL. The standard plating method was applied to confirm the bacterial concentrations. This test was done in triplicates on tryptic soy agar. Samples were plated in triplicates. The colonies were visually identified and counted after incubation at 37 °C overnight.

Response level method

The response level method is a collection of useful statistical and mathematical methods for modeling and analyzing problems, in which the desired response level is affected by multiple variables (Ahmadi et al. 2005). In recent years, the method has been well considered in the field of water treatment, as it is very easy with a quick and accurate design. The method provides a second-order polynomial model to fit the test responses as follows (Myers et al. 2004): 
formula
(1)
where Y is the response, (X1, X2, X3) are the encoded variable factors, b0, bi and bij (i, j = 1, 2, 3) are the model estimated coefficients.

In the response level method, the Box-Behnken Design (BBD) has been used to optimize the responses. The parameters significance level was 95%. To eliminate Escherichia coli, from contaminated water, the effect of nanoparticle factors, pH, and contact time on removing Escherichia coli has been investigated. The levels of the factors are presented in Table 2. Regarding the number and levels of selected factors using response level and BBD method, through Design-Expert software 8.0.1, 15 tests have been introduced in the proposed range. The results were analyzed using ANOVA table and 3D charts.

Table 2

Selected factors and levels for the removal of E. coli

Factors Actual and code values of factors
 
+ 1 − 1 
Silver-coated red soil (g) 0.1 0.05 0.02 
Contact time (min) 30 20 10 
Bacterial count (CFU/ml) 106 104 102 
Factors Actual and code values of factors
 
+ 1 − 1 
Silver-coated red soil (g) 0.1 0.05 0.02 
Contact time (min) 30 20 10 
Bacterial count (CFU/ml) 106 104 102 
To calculate the removed amount of E. coli by nanoparticle, the following equation is used: 
formula
(2)
where R represents the percentage of bacterial elimination, C0 is the number of primary bacteria, and Ct is the number of bacteria remaining after disinfection time t.

RESULTS AND DISCUSSION

Properties of the silver nanoparticle-coated red soil

The soil was characterized by low pH and organic matter content, high contents of clay and Fe and Al oxides, and high specific surface area (Table 1). These features are reported to be favorable for virus and bacteria removal (Gerbo et al. 1981; Moore et al. 1982; Zhang et al. 2010). The morphology and structure of the prepared nanocomposite were investigated with TEM analysis. TEM image of red soil/Ag nanocomposites is shown in Figure 1. Clear spherical and non-homogenous structures can be seen in Figure 1. The average size of the nanocomposites evaluated from the TEM image is about 40 nm. The inductively coupled plasma atomic emission spectroscopy (ICP-AES) was applied for determining the amount of the Ag nanoparticle loading on red soil. It showed 0.071 mmole of silver nanoparticle per gram of the prepared disinfectant.

Figure 1

TEM image of red soil/Ag nanocomposite.

Figure 1

TEM image of red soil/Ag nanocomposite.

In order shows the presence of Ag nanoparticles on the red soil, X-ray diffraction (XRD) analyses have been used. The XRD patterns (Figure 2(a)) indicate red soil structure according to Worden & Morad 2003. As seen in Figure 2(b), the principal peaks at 2θ = 38.1 is related to Ag (Zazouli et al. 2017), verifying the presence of Ag nanoparticle on the red soil samples.

Figure 2

XRD patterns of (a) red soil and (b) red soil/Ag.

Figure 2

XRD patterns of (a) red soil and (b) red soil/Ag.

Development and evolution of prediction model

Table 3 shows experimental results of eliminating Escherichia coli according to the design table with the response level and BBD with red soil/Ag NPs.

Table 3

The Box–Behnken design matrix with three independent variables (A, B, and C)

Experiment no. A
Bacteria No. (CFU/ml) (code) 
B
Amount of silver-coated red soil (g) (code) 
C
Contact time; min. (code) 
R
% E. coli removal 
104 (0) 0.02 (−1) 30 (1) 95.4 
102 (−1) 0.05 (0) 10 (−1) 97.1 
106 (1) 0.1 (1) 20 (0) 99.1 
104 (0) 0.05 (0) 20 (0) 98.9 
102 (−1) 0.05 (0) 30 (1) 99.5 
104 (0) 0.05 (0) 20 (0) 98.7 
102 (−1) 0.1 (1) 20 (0) 99.9 
106 (1) 0.05 (0) 30 (1) 98.8 
106 (1) 0.02 (−1) 20 (0) 94.0 
10 102 (−1) 0.02 (−1) 20 (0) 95.1 
11 104 (0) 0.05 (0) 20 (0) 98.8 
12 104 (0) 0.02 (−1) 10 (−1) 91.2 
13 106 (1) 0.05 (0) 10 (−1) 94.9 
14 104 (0) 0.1 (1) 10 (−1) 96.4 
15 104 (0) 0.1 (1) 30 (1) 99.8 
Experiment no. A
Bacteria No. (CFU/ml) (code) 
B
Amount of silver-coated red soil (g) (code) 
C
Contact time; min. (code) 
R
% E. coli removal 
104 (0) 0.02 (−1) 30 (1) 95.4 
102 (−1) 0.05 (0) 10 (−1) 97.1 
106 (1) 0.1 (1) 20 (0) 99.1 
104 (0) 0.05 (0) 20 (0) 98.9 
102 (−1) 0.05 (0) 30 (1) 99.5 
104 (0) 0.05 (0) 20 (0) 98.7 
102 (−1) 0.1 (1) 20 (0) 99.9 
106 (1) 0.05 (0) 30 (1) 98.8 
106 (1) 0.02 (−1) 20 (0) 94.0 
10 102 (−1) 0.02 (−1) 20 (0) 95.1 
11 104 (0) 0.05 (0) 20 (0) 98.8 
12 104 (0) 0.02 (−1) 10 (−1) 91.2 
13 106 (1) 0.05 (0) 10 (−1) 94.9 
14 104 (0) 0.1 (1) 10 (−1) 96.4 
15 104 (0) 0.1 (1) 30 (1) 99.8 

The results of analysis of variance (ANOVA) for the independent variables are presented in Table 4. The confidence level was considered 95%. For this reason, p ratio must be less than 0.05 so that the model or the factors effect is significant. This means that there is a 5% probability of error that a non-important factor is considered important. One of the most important factors in the statistical analysis of F ratio is the model statistical significance. If the F ratio of an agent is higher, it indicates that this factor is significant and its effect on the response rate is more important. The analysis of variance for the removal of E. coli is shown in Table 4.

Table 4

Analysis of variance for the response rate of Escherichia coli elimination

Source df Sum of squares Square mean F value p value Remark 
Model 96.24 10.69 125.06 <0.0001 Significant 
A (Bacteria No.) 3.51 3.51 41.07 0.0014 Significant 
B (Amount of silver-coated red soil) 48.51 48.51 567.38 <0.0001 Significant 
C (Contact time) 26.64 26.64 311.64 <0.0001 Significant 
A × B 0.023 0.023 0.26 0.6298  
A × C 0.25 0.25 2.92 0.1480  
B × C 0.090 0.090 1.05 0.3520  
A2 0.028 0.028 0.33 0.5902  
B2 12.81 12.81 149.80 <0.0001 Significant 
C2 5.21 5.21 60.90 0.0006 Significant 
Lack of fit 0.41 0.14 13.58 0.0693  
Pure error 0.020 1 × 10−0.02 – –  
Source df Sum of squares Square mean F value p value Remark 
Model 96.24 10.69 125.06 <0.0001 Significant 
A (Bacteria No.) 3.51 3.51 41.07 0.0014 Significant 
B (Amount of silver-coated red soil) 48.51 48.51 567.38 <0.0001 Significant 
C (Contact time) 26.64 26.64 311.64 <0.0001 Significant 
A × B 0.023 0.023 0.26 0.6298  
A × C 0.25 0.25 2.92 0.1480  
B × C 0.090 0.090 1.05 0.3520  
A2 0.028 0.028 0.33 0.5902  
B2 12.81 12.81 149.80 <0.0001 Significant 
C2 5.21 5.21 60.90 0.0006 Significant 
Lack of fit 0.41 0.14 13.58 0.0693  
Pure error 0.020 1 × 10−0.02 – –  

Considering p-value and F ratios of eliminating Escherichia coli, the effect of amount of silver-coated red soil (disinfectant concentration) factor, bacteria number and contact time on Escherichia coli elimination is significant. Disinfectant concentration factor has the greatest effect on E. coli removal. Other factors showed no significant relationships.

Mathematical model

The value of R2 for Escherichia coli elimination is 0.9956 indicating a good agreement between experimental data and the model predicted data. The comparison of the experimental model and predicted results of E. coli removal rate is presented in Figure 3.

Figure 3

The experimental model (squares) and predicted results (dash) for Escherichia coli removal.

Figure 3

The experimental model (squares) and predicted results (dash) for Escherichia coli removal.

Also, insignificance of the term not fitted in Table 4 implies that the proposed statistical model provided is well fitted to the experimental data. The second-order statistical model, offering the design of Escherichia coli removal rate in terms of agents' actual values (not coded values) is presented as follows: 
formula
(3)
where A is bacteria number in CFU/ml, B is disinfectant concentration in g/mL, C is contact time in minute and elimination of Escherichia coli (R1) is in percentage.

The effect of parameters

The effect of silver-coated red soil concentration

The silver-coated red soil concentration is one of the most important factors, as shown in Figure 4 for E. coli. Figure 4(a) illustrates the removal of E. coli with changes in disinfection concentration and contact time. Based on the results, an increase in disinfection concentration, as well as contact time, results in increasing the percentage of E. coli removal. Figure 4(b) shows the removal of E. coli, along with changes in disinfection concentration and the number of bacteria is observable. An increase in disinfectant concentration results in increasing the removal percentage. Inversely, increasing the number of bacteria leads to a reduction in removal percentage. These results can be attributed to an escalation in the contact surface of the disinfectant with bacteria; as well as an increase in hydrogen peroxide concentration produced from disinfectant intensifying bacteria elimination percentage (Sawai et al. 1996). The results of the present study are consistent with Zhang et al. (2007). It should be noted that in these experiments, the control test was performed at the following conditions: contact time = 20 min; disinfectant concentration (uncoated red soil) = 0.05 g/mL; E. coli no. = 104 CFU/mL. After culture on the medium (R2A agar), the bacteria grew and formed a colony. The bacterial inactivation percent was zero.

Figure 4

3D diagram of changes in Escherichia coli removal rate in terms of code and actual values: (a) red soil/Ag concentration and contact time; (b) red soil/Ag concentration and bacteria number.

Figure 4

3D diagram of changes in Escherichia coli removal rate in terms of code and actual values: (a) red soil/Ag concentration and contact time; (b) red soil/Ag concentration and bacteria number.

The effect of contact time

Contact time is the second most important factor. As shown in Figure 5 for Escherichia coli, increasing contact time leads to an increase in the removal percentage. However, an increase in the number of bacteria results in reducing the percentage of removal.

Figure 5

Removal percentage of E. coli with changes in contact time and the number of bacteria.

Figure 5

Removal percentage of E. coli with changes in contact time and the number of bacteria.

The control test was performed at the conditions described above.

The effect of number of bacteria

Based on Figure 4, bacterial removal rate decreases by augmenting the number of bacteria. As disinfectant contact surface with bacteria is declined by increased number of bacteria, and the turbidity is intensified, thus diminishing the disinfection properties of the disinfectant.

According to our results, the mechanism of bacterial inactivation by red soil-coated Ag is ionic. The mechanism operates based on the transformation of microorganisms by converting –SH bonds to –SAg bonds. Silver nanoparticles disable the enzyme by releasing Ag+ ions and absorbing the –SH bonds which are the basis of the protein enzymes at the bacteria surface. Therefore due to the lack of absorption of phosphate by the cell, the bacteria are inactivated. This mechanism does not terminate with the destruction of the bacteria and is a permanent process (Davies & Etris 1997).

CONCLUSION

The results of the present study demonstrated that Gram-negative E. coli bacterium is sensitive to red soil-coated silver. Intensifying disinfectant concentration increases bacterial removal percentage; furthermore, raising the number of bacteria reduces nanoparticle disinfection properties. Extended contact time of the bacteria with red soil/Ag may increase bacterial elimination percentage. R2 value for Escherichia coli elimination is 0.9956, implying a good agreement between the experimental model and predicted data. Through scientific nano-advances, it is possible to use red soil/Ag in the water and wastewater industry. Respecting silver nanoparticles, one of the limitations considered as a disadvantage of using disinfectant is the high price. However, silver reusing and recycling may, to some extent, moderate the constraint of this strong disinfectant.

ACKNOWLEDGEMENTS

The authors acknowledge the Islamic Azad University-Bandar Abbas Branch for financial support of this study.

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