A comparative account of biogenic synthesis of silver nanoparticles using in-house potential probiotics and their antimicrobial activity against challenging antibiotic resistant pathogens

doi:10.21203/rs.3.rs-806048/v1

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A comparative account of biogenic synthesis of silver nanoparticles using in-house potential probiotics and their antimicrobial activity against challenging antibiotic resistant pathogens

https://doi.org/10.21203/rs.3.rs-806048/v1

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The present work focusses on development of a safe, inexpensive, and more accessible source for biosynthesis of silver nanoparticles. Four different in-house probiotic isolates i.e., Lactobacillus pentosus S6, Lactobacillus plantarum F22, Lactobacillus crustorum F11 and Lactobacillus paraplantarum KM1 isolated from different food sources, were used in the current study to check their ability to synthesize silver nanoparticles. All the probiotics synthesized silver nanoparticles shows maximum Surface Plasmon Resonance (SPR) at a peak of 450 nm, which confirms the formation of silver nanoparticles. Scanning Electron Microscopy (SEM) analysis identified the shape and distribution of silver nanoparticles. Transmission Electron Microscopy (TEM) revealed the average size of synthesized nanoparticles in the range of 10-50 nm, with smallest size of 5 nm for silver nanoparticles synthesized by L. crustorum F11. Further, Fourier-transform infrared spectroscopy (FTIR) detected the presence of different functional groups responsible for reduction of silver ion to form silver nanoparticles. The antimicrobial activity of these AgNP was also found to be effective against different bacterial and fungal pathogens viz. antibiotic resistant Staphylococcus aureus, Bacillus cereus, Listeria monocytogenes , Pythium aphanidermatum , Fusarium oxysporum and Phytopthora parasitica . However, L.crustorum F11 synthesized AgNP showed maximum inhibition against all the bacterial and fungal pathogens, with highest against S. aureus (20 0.61mm) and F. oxysporum (23 ). Findings from this study provide a durable and ecofriendly method for the biosynthesis of silver nanoparticles, having strong antimicrobial activity against different multidrug resistant microorganisms.

General Microbiology

silver nanoparticles

AgNP

probiotics

Lactobacillus

antibacterial

TEM

FTIR

Nanotechnology is a rapidly evolving field of science, that has been flourishing since the beginning of last century. It involves the synthesis of particles at nanoscale level having size less than 100 nm (Arshad, 2017). There is an increase concern worldwide about the rise in antibiotic resistant cases, as harmful pathogenic microorganisms have developed resistance against already used different antibiotics (Khatoon et al. 2019). These multidrug- resistant organisms (MDROs) are multiplying at faster rate, making various health related infections almost untreatable (Lee et al. 2019; Boucher et al. 2009; Peleg and Hooper, 2010). Therefore, nanotechnology is coming forward with a solution to treat these infections as studies revealed that the utilization of nanoparticles provides a potential to manage infection caused by these pathogenic microorganisms (Baptista et al., 2018; Muzammil et al. 2018). Among metallic nanoparticles, silver and gold nanoparticles are most promising nanoparticles because of their large surface area to volume ratio, which has garnered interest in the researchers due to the growing microbial resistance against metal ions, antibiotics and the development of resistant strains (Mosallam et al. 2014). Silver nanoparticles (AgNPs) are gaining attention as one of the most promising nanoparticles due to its unique properties (Yusof et al. 2020). AgNPs have strong toxic effect against wide range of microorganisms and can be used as a potential antimicrobial agent (Naseer et al. 2020). There are different physical and chemical methods already being used for the synthesis of nanoparticles, since these are associated with hazardous chemicals exhibiting toxicity (Hemlata et al. 2020), biologically synthesized metallic nanoparticles are preferred for their ecofriendly nature, cost effectiveness and less hazardous effect.

Probiotics are the live microbes that exert health beneficiary effects to the host cell, when administrated in an adequate amount (Pandey et al. 2010). The utilization of probiotic bacteria to synthesize nanoparticles has been reported in different studies and is a focus of ongoing research nowadays (Akhtar and Pathak, 2017). Probiotics are now being employed in synthesizing or more precisely biosynthesizing various nanoparticles, such as metallic as well as non-metallic nanoparticles. Probiotics synthesized nanoparticles has its application in health industry, food industry, cosmetics and biotechnology. The bacterial genera Lactobacillus and Bifidobacterium are the most widely used probiotics, that are being used in biosynthesis of silver nanoparticles. These probiotic synthesized silver nanoparticles have been found to possess effective antimicrobial efficacy against a wide range of pathogenic microbes and have enhanced surface area to volume ratio, high catalytic capabilities and tendency to generate reactive oxygen species (Berton et al. 2014). Thus these Probiotics synthesized nanoparticles can be employed as an alternative of antibiotic as they have the ability to inhibit harmful microorganisms present in human body (Hong et al. 2019; Gillor et al. 2008).

As the use of probiotics in synthesizing nanoparticles is a novel and current trending research due to multiple benefits of probiotics, in the present paper an attempt has been made to synthesize silver nanoparticles from four in-house potential probiotic cultures i.e. Lactobacillus pentosus S6, Lactobacillus plantarum F22, Lactobacillus crustorum F11 and Lactobacillus paraplantarum KM1 that have already been isolated from different food sources and their characterization by using UV-Visible spectroscopy, Scanning Electron Microscopy (SEM), Transmission Electron Microscopy (TEM) and Fourier Transform Infrared Spectroscopy (FTIR). Further their antagonistic spectrum was examined against different challenging pathogens (Bacteria and Fungi).

Materials

The four in-house potential probiotic cultures isolated from different food sources were collected from Microbiology laboratory, Department of Basic Sciences, UHF Nauni, Solan, H.P, India, for the biosynthesis of silver nanoparticles and analysis of their antimicrobial potential. Table 1 shows the different in-house cultures collected for the study. All the probiotic isolates were cultivated in de Man, Rogosa and Sharpe (MRS) broth separately for 24h (37°C). The bacterial strains used in the study were obtained from MTCC (IMTECH, Chandigarh), CRI (Kasauli) and IGMC (Shimla). All the chemicals used in this study were of analytical grade.

Table 1

list of in-house potential probiotic cultures collected for synthesis of silver nanoparticles
Name	Accession number	Food Source
Lactobacillus pentosus S6	KU92122	Siddu
Lactobacillus plantarum F22,	KT865223	Chhang
Lactobacillus crustorum F11	KT865221	Human milk
Lactobacillus paraplantarum KM1	KX671558	Milk
Source: Microbiology research laboratory, Deptt. Of Basic Sciences, UHF Nauni, Solan, H.P, India

Biosynthesis of silver nanoparticles using probiotic isolates

The collected probiotic strains were inoculated in 100 ml of MRS media and was incubated overnight at 37°C for 24 h. After incubation, the culture was centrifuged at 10,000 rpm for 15 min.10 ml of culture supernatant from each isolate was separately mixed with 90 silver nitrate (AgNO₃) solution (0.1 mM) and another reaction mixture without silver nitrate was used as control. The prepared solutions were incubated at 30°C (24 h) and kept in dark to avoid any photochemical reactions during the investigation. The change in color in synthesized silver nanoparticles was observed after 24 h. The biosynthesized silver nanoparticles were then characterized by using UV-vis, SEM, TEM and FTIR spectroscopy.

Characterization of silver nanoparticles

UV-Visible Spectroscopy Analysis

Silver nanoparticles were analyzed by UV-Vis spectrophotometer (Shimadzu 1600, Japan). The bio reduction of silver ion in aqueous solution was monitored by periodic diluted sampling of aliquots and subsequently measuring the spectra of the solution on UV-Vis spectrophotometer (Sarvamangla et al. 2013). The absorbance of all the four synthesized silver nanoparticle was read at different wavelengths i.e., 350, 450, 550 and 650 nm.

Scanning electron microscopy (SEM)

The thin film of the different probiotic synthesized nanoparticles was prepared separately on aluminum plate by just dropping a very small amount of the sample on the plate, extra solution was removed using blotting paper and then the film on the plate was allowed to dry overnight. The SEM analysis was performed on a JEOL; model JSM – 6610LV instrument operated at an accelerating voltage of 20 KeV (Sarvamangla et al. 2013).

Transmission electron microscopy (TEM)

Transmission Electron Microscopy was performed by using model FP 5022/22-Tecnai G2 20 S-TWIN. TEM shows the size, shape, appearance and crystal structure of the particles. The grid for TEM analysis was prepared by placing a drop of the synthesized nanoparticles suspension on a carbon-coated copper grid and allowing the water to evaporate inside a vacuum dryer for 1 h.

Fourier transform infrared spectroscopy (FTIR)

The synthesized silver nanoparticles were further characterized by their FTIR analysis. The small amount of synthesized silver nanoparticles was dried in freeze‐drier separately (Lyophilizer) for 24 h, then freeze dried sample was appointed with KBr pellets and analyzed using a Thermo Nicolet model: nexus 870 in range of 450‐4000 cm^‐¹at a resolution of 4 cm^‐¹(Omidi et al. 2014)

Antibacterial efficacy of silver nanoparticles

Antibacterial assay of synthesized silver nanoparticles was performed against three standard test indicators i.e., antibiotic resistant Staphylococcus aureus IGMC, Listeria monocytogenes MTCC839 and Bacillus cereus CRI using well plate assay (Kimura et al. The inoculum of each pathogen was grown in nutrient broth overnight (37⁰ C). Each pathogen was streaked on a separate nutrient agar plate using sterilized swabs. Wells were punched on nutrient agar plate with the help of a sterile borer.100µl of biosynthesized silver nanoparticles (concentration: 200µg/ml) from all the four different probiotic isolates was added to each well cut on the agar plate separately. The experiment was performed in triplicates.

Antifungal activity of silver nanoparticles

Antifungal activity was checked against three fungal pathogens viz. Pythium aphanidermatum, Fusarium oxysporum and Phytopthora parasitica by well plate assay using dual culture technique (Mew and Rosales, 1984). On the one side of prepoured sterilized potato dextrose agar (PDA) plates, 7 days old culture bit of indicator fungi was placed with the help of sterile well borer and inoculating loop. On the other side of PDA plate, well was cut with the help of sterile borer followed by addition of 100µl of 0.1 mM probiotics synthesized AgNP were added to the well. Plates were incubated at 28±2ºC for 7 days and observed for inhibition of mycelial growth produced around the well. The experiment was performed in triplicates.

The utilization of microorganisms for the biosynthesis of nanoparticles, has gained considerable attention in the recent times as compared to the previously used standard methods. This work reports the biosynthesis of AgNPs using four different in-house potential probiotic strain i.e., Lactobacillus pentosus S6 and Lactobacillus plantarum F22, Lactobacillus crustorum F11 and Lactobacillus paraplantarum KM1, to check their ability to synthesize them and determination of their antimicrobial activity.

Biosynthesis of silver nanoparticles

Silver nitrate was used as a precursor for the biosynthesis of silver nanoparticles. The first distinctive feature of the formation of silver nanoparticles is the color change in the solution after 24 hours of incubation. Silver nitrate was colorless and after reduction by probiotic isolates, the supernatant changed into brown color. All the four probiotic isolates were capable of synthesizing silver nanoparticles as all of them showed color change after incubation as compared to control (AgNO₃) (Fig. 1 a). The severity of color is due to actuated surface Plasmon vibration in the metal nanoparticles (Prasad et al. 2011). Different microorganisms have different mechanisms of synthesizing nanoparticles. However, nanoparticles are usually formed when microbial cells trapped metal ions on the surface or inside, and then trapped metal ions are reduced to nanoparticles in the presence of enzymes (Xiangqian et al. 2011). Several studies have reported the synthesis of silver nanoparticles using different microorganisms, but much work is needed to be done to improve their efficacy, maintaining their particle size and future safety concerns. Thus, in the present study an attempt has been made to check the ability of different in-house probiotic microorganisms that are isolated from different food sources to synthesize silver nanoparticles. Over the last few decades, there has been growing interest in the use of probiotics as potential alternatives for synthetic antibiotics and anti-inflammatory drugs, not only due to the side effects of synthetic drugs but also to the improper use of antibiotics promotes the development of antibiotic-resistant bacteria. Mikiciuk et al. (2016) depicted the influence of silver nanoparticles on probiotic bacteria. Probiotic bacteria like Bifidobacterium animalis subspecies lactis BB-12, Lactobacillus acidophilus LA-5, and Streptococcus thermophilus ST-Y31 have been taken from fermented milk products to synthesize silver nanoparticles. Ysouf et al. (2020) reported the utilization of biomass of Lactobacillus plantarum TA4 for the biosynthesis of silver nanoparticles.

UV-Visible spectroscopy

The UV-Vis spectroscopy analysis was the second characterization method used for the confirmation of the synthesis of silver nanoparticles. The process of reaction between the metal ions and biosynthesized silver nanoparticles was monitored using UV spectra through the aqueous solution. The presence of nanoparticles synthesized by Lactobacillus pentosus S6, Lactobacillus plantarum F22, Lactobacillus crustorum F11 and Lactobacillus paraplantarum KM1 was confirmed by obtaining a spectrum in different wavelength range i.e., 350, 450, 550 and 650nm respectively (Fig 1 b). The highest absorbance peak for all of the four isolates was found at the wavelength of 450 nm, which was specific for silver nanoparticles synthesis. Dhoondia and Chakraborty (2012) observed the maximum absorption peak at 430 nm for silver nanoparticles synthesized using Lactobacillus mindensis. Malathi et al. (2015) monitored the synthesis of silver nanoparticles from Lactobacillus by UV-spectroscopic analysis. The peak was observed between 400-450 nm indicating the presence of silver nanoparticles.

Scanning Electron Microscopy (SEM)

The synthesized silver nanoparticles were further characterized by Scanning Electron Microscopy (SEM). SEM reveals the external morphology and texture of silver nanoparticles. Fig 2 (a, b, c and d) depicts the SEM analysis of silver nanoparticles synthesized from different probiotics. From the SEM analysis, it can be observed that silver nanoparticles from all the four probiotic isolates were spherical in shape and were found as an individual particle and also present in aggregates. Tayo and Papoola (2017) reported that SEM is an important tool for AgNP characterization. Production of silver nanoparticles from Lactobacillus sp. with varying shape i.e., rectangular to spherical was observed (Prabhu et al. 2014). Arshad A (2017) examined SEM analysis of silver nanoparticles synthesized from Bacillus sp, are spherical and pseudo-spherical in shape.

Transmission Electron Microscopy (TEM)

Transmission Electron Microscopy (TEM) is a valuable tool used to visualize size of synthesized silver nanoparticles. Fig 3 (a, b, c and d) and Table 2 depicts the TEM images of silver nanoparticles synthesized from L. pentosus S6, L. plantarum F22, L. crustorum F11 and L. paraplantarum KM1 respectively. Silver nanoparticles of different size were synthesized by all the four isolates. L. pentosus S6 synthesized silver nanoparticle has a mean size of 50nm, whereas, for silver nanoparticle synthesized from L. plantarum F22 it is 20 nm. AgNP from L. plantarum F22 has a size of 10 nm and for L. paraplantarum KM1 it is 50 nm. The silver nanoparticles synthesized in this work were in the same approximate range as reported by other authors for silver nanoparticles synthesized from lactic acid bacteria and other microorganisms (Sintubin et al. 2009; Kalimathu et al. 2008). However, out of all the four probiotics synthesized silver nanoparticles, one synthesized using L. crustorum F11 was found to be smaller (10 nm) of all. Size plays an essential role in nanoparticles applications; smaller particles have a relatively large surface area as compared to larger ones; this increases their interaction with harmful pathogens and consequently trigger more toxic and adverse effect. Many researchers also observed the almost same range of silver nanoparticles synthesized using probiotics just like our findings. Garmasheva et al. (2016) reported the TEM analysis of silver nanoparticles synthesized from lactic acid bacteria and found that the size of nanoparticles was between 10 and 40 nm. Prabhu et al. (2014) also observed the size of silver nanoparticles synthesized by Lactobacillus sp. and found the average size of about 20-40 nm. Ranganath et al. (2012) observed the TEM picture of the silver nanoparticles formed by Lactobacillus sp. VRS-2. The TEM Technique used to visualize size and shapes of biosynthesized silver nanoparticles have predominantly shown spherical shape structures with size ranging between 2nm - 20 nm and have shown the presence of individual as well as number of aggregates of silver nanoparticles.

Table 2: Transmission Electron Microscopy (TEM) analysis of synthesized nanoparticles by different probiotics

Probiotic culture	Size of synthesized nanoparticles (nm)
Lactobacillus pentosus S6	50
Lactobacillus plantarum F22	20
Lactobacillus crustorum F11	10
Lactobacillus paraplantarum KM1	50

Fourier transform infrared spectroscopy (FTIR)

Formation of silver nanoparticles was further confirmed, by analyzing the characteristic functional groups present in silver nanoparticles. FTIR spectrum is used to identify different functional groups, responsible for the reduction and stabilization of silver ions to silver nanoparticles. The FTIR spectrum of synthesized silver nanoparticles was presented in Fig 5 (a, b, c and d) respectively. L pentosus S6 synthesized silver nanoparticles (Fig 4a) shows absorbance peak at 1710cm^-1 which correspond to C=O stretching vibration of ketone. The absorbance peak at 2273 cm^-1 corresponds to N=C=O stretching and presence of isocyanate functional group, whereas absorbance peak at 1367 cm^-1 indicated C-O stretching vibration of an ester (Beekes et al. 2007). L. crustorum F11 synthesized silver nanoparticles (Fig 4b) shows absorbance peak at 3222 cm^-1 referred to O-H stretching and presence of carboxylic acid, whereas absorbance peak at 1628 cm^-1 revealed C=C stretch and the presence of alkene. The peak at 1146 cm^-1 represents O-H bond of the aliphatic ether, 1062 cm^-1 corresponds to O-H stretch of primary alcohol, 1925 cm^-1 peak indicated C=C=C stretch of allene. For silver nanoparticles synthesized from L. plantarum F22 (Fig 4c) the absorbance peak at 1695 cm^-1 corresponds to C=N stretching of imine group. The absorbance peak at 1324 cm^-1 could be attributed to C-N bond of aromatic amide, and absorbance peak at 1635 cm^-1 represented C=C stretching of alkenes. Silver nanoparticles synthesized by L. paraplantarum KM1 (Fig 4d) shows peak at 1695 cm^-1 had C=O stretch of conjugated aldehyde and peak at 1941 cm^-1 was identified as C-H stretch of aromatic compound. The peak at 2161 cm^-1 represented S-C=N stretch of thiocyanate and 1647 cm^-1 peak pointed out the C=N stretch of sulfone (Fig. 5d). All the four probiotic isolates used in the study contain important functional groups (hydroxyl, protein, and carboxyl) in the cell membrane, which plays an important role in the reduction of silver nitrate and thus capable of biosynthesizing silver nanoparticles. Viorica et al., (2017) studied the FTIR spectrum of silver nanoparticles synthesized from Lactococcus lactis and observed absorption bands at 1650 cm^-1 revealed the presence of amide, whereas amide II region (N–H bending and C–N stretching) occurred at 1550 cm^-1. Milanowiski et al., (2017) observed peak at 1530-1630 cm^-1which could be attributed to amide II vibrations, for silver nanoparticles synthesized by L.casei.

Antibacterial efficacy of silver nanoparticles

The antimicrobial efficacy of synthesized AgNPs was assessed against challenging pathogens i.e., Staphylococcus aureus, Bacillus cereus and Listeria monocytogenes (Fig). All the four-probiotic synthesized AgNPs was found to exhibit strong antibacterial activity against the bacterial pathogens. However, out of all L. crustorum F11 synthesized AgNPs showed maximum zone of inhibition against all the microbial strains with maximum zone of inhibition of 20 0.61mm against S. aureus, 14 1.01 mm for L. monocytogenes and 12 7.07 for B. cereus respectively (Fig. 5). However, Several Studies reported the antibacterial activity of lactic acid bacteria synthesized AgNP against different pathogens, while our study concluded the effectiveness of major probiotics against harmful challenging pathogens. Moodley et al. (2018) reported the antibacterial activity of silver nanoparticles against K. pneumoniae and S. aureus. Kumar et al. (2016) observed the antimicrobial efficacy of silver nanoparticles synthesized from Lactococcus amylophilus GV6 against P. aeruginosa MTCC 424, B. subtilis MTCC 121, S. aureus MTCC 96, E. coli MTCC 43 and Klebsiella pneumoniae MTCC 109 by using agar well plate assay and reported the zone of inhibition of 1.5 cm against S. aureus MTCC 96. Yusof et al. (2020) observed the antibacterial activity of biosynthesized silver nanoparticles from Lactobacillus plantarum TA4 against S. aureus, S. epidermidis, E. coli and Salmonella by agar well diffusion method.

Antifungal activity of probiotics synthesized silver nanoparticles

The antifungal activity of synthesized silver nanoparticles was assessed against three fungal pathogens viz. Pythium aphanidermatum, Fusarium oxysporum and Phytopthora parasitica. Here also, L. crustorum F11 synthesized AgNP showed maximum inhibition against all the three fungal pathogens i.e., 23±0.37 for F. oxysporum, 20±1.01against P. parasitica and 32.6±0.48 against P. aphanidermatum F11(Fig. 6). Matei et al. (2020) investigated the antifungal activity of silver nanoparticles synthesized by lactic acid bacteria against Aspergillus ochraceus, Penicillium expansum and Aspergillus flavus and observed maximum antifungal activity for Penicillium expansum (15.87±1.01).

Although all the probiotic synthesized silver nanoparticles exhibited strong antimicrobial activity, but the one synthesized from L. crustorum F11 stands apart, as it showed the maximum antagonistic spectrum against different bacterial and fungal pathogens. This strong inhibitory effect could be attributed to its smaller size (10 nm) as compared to the other probiotic synthesized silver nanoparticles. Similar work is reported by Lu et al. (2013) where they examined size dependent antimicrobial activity of AgNPs against oral pathogenic bacteria. They observed that AgNPs having a size of 5 nm has a stronger antagonistic activity as compared to the one with size of 15 and 55 nm respectively. Morones et al. (2005) suggested that antimicrobial activity of silver nanoparticles was size dependent with higher antagonistic effect from nanoparticles whose size ranges from 1~10 nm. The small particle size helps AgNPs to adhere to the cell wall and penetrate the cell easily, which in turn enhances their antimicrobial activity against harmful pathogenic bacteria.

This study was carried out with the sole purpose to biosynthesize silver nanoparticles using health beneficial probiotic isolates and their antagonistic potential against challenging microbial strains. All of the four different in-house probiotic isolates used in this study were found to be safe and effective for the synthesis of silver nanoparticles. SEM analysis depicted the morphology and TEM analysis evaluated the size of different probiotic synthesized silver nanoparticles (20, 10 and 50nm). FTIR analysis identified different organic compound responsible for reduction and formation of silver nanoparticles. Furthermore, these biosynthesized silver nanoparticles revealed pronounced antimicrobial activity against different challenging bacterial and fungal pathogens. The results in our study recommend using probiotics, as a novel and ecofriendly tool for biosynthesizing silver nanoparticles, having effective antimicrobial activity and thus can be used against different health deteriorating multi drug resistant microorganisms.

Conflict of interest

The authors declare that they have no conflict of interest

Acknowledgment

The authors thanks Mr. Arjun, Technician, Indian Institute of Technology, Mandi, Himachal Pradesh, India for technical support and help in obtaining TEM and FTIR results.

SEM

Scanning Electron Microscope

TEM

Transmission Electron Microscope

FTIR

Fourier Transform Infrared Spectroscopy

AgNP

Silver Nanoparticles

AgNO₃

Silver Nitrate

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A comparative account of biogenic synthesis of silver nanoparticles using in-house potential probiotics and their antimicrobial activity against challenging antibiotic resistant pathogens

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Abstract

Figures

Introduction

Materials And Methods

Materials

Biosynthesis of silver nanoparticles using probiotic isolates

Results And Discussion

Conclusions

Declarations

Abbreviations

References

Supplementary Files

Status:

Version 1