Bioprocess Biosyst Eng DOI 10.1007/s00449-014-1169-6


Green synthesis of silver and gold nanoparticles using Zingiber officinale root extract and antibacterial activity of silver nanoparticles against food pathogens Palanivel Velmurugan • Krishnan Anbalagan • Manoharan Manosathyadevan Kui-Jae Lee • Min Cho • Sang-Myeong Lee • Jung-Hee Park • Sae-Gang Oh • Keuk-Soo Bang • Byung-Taek Oh

Received: 26 October 2013 / Accepted: 6 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014

Abstract In the present study, we synthesized silver and gold nanoparticles with a particle size of 10–20 nm, using Zingiber officinale root extract as a reducing and capping agent. Chloroauric acid (HAuCl4) and silver nitrate (AgNO3) were mixed with Z. officinale root extract for the production of silver (AgNPs) and gold nanoparticles (AuNPs). The surface plasmon absorbance spectra of AgNPs and AuNPs were observed at 436–531 nm, respectively. Optimum nanoparticle production was achieved at pH 8 and 9, 1 mM metal ion, a reaction temperature 50 °C and reaction time of 150–180 min for AgNPs and AuNPs, respectively. An energy-dispersive X-ray spectroscopy (SEM–EDS) study provides proof for the purity of AgNPs and AuNPs. Transmission electron microscopy images show the diameter of well-dispersed AgNPs (10–20 nm) and AuNPs (5–20 nm). The nanocrystalline phase of Ag

P. Velmurugan  K.-J. Lee  M. Cho  S.-M. Lee  J.-H. Park  B.-T. Oh (&) Division of Biotechnology, Advanced Institute of Environment and Bioscience, College of Environmental and Bioresource Sciences, Chonbuk National University, Iksan, Jeonbuk 570-752, South Korea e-mail: [email protected] K. Anbalagan  M. Manosathyadevan Department of Environmental Science, Periyar University, Periyar PalkaliNagar, Salem, Tamil Nadu 636011, India S.-G. Oh Mine Reclamation Corp., Seoul 110-727, South Korea K.-S. Bang (&) Department of Oriental Medicine Resources, Advanced Institute of Environment and Bioscience, College of Environmental and Bioresource Sciences, Chonbuk National University, Iksan, Jeonbuk 570-752, South Korea e-mail: [email protected]

and Au with FCC crystal structures have been confirmed by X-ray diffraction analysis. Fourier transform infrared spectroscopy analysis shows the respective peaks for the potential biomolecules in the ginger rhizome extract, which are responsible for the reduction in metal ions and synthesized AgNPs and AuNPs. In addition, the synthesized AgNPs showed a moderate antibacterial activity against bacterial food pathogens. Keywords Antibacterial activity  Food pathogens  Silver and gold nanoparticles  Zingiber Officinale

Introduction Nanotechnology has emerged as a rapidly growing field for the manufacture of new materials on the nanoscale level, with frequent applications in science and technology [1]. On the nanoscale level, materials have different electrical, magnetic, optical, physical and chemical properties due to their surface area to volume ratio, which can be manipulated for human benefit [2]. Food plays a vital role in day-to-day life, providing nutritional support for the body. Food may be broadly classified into groups based on their nutritive values in categories such as carbohydrates, fats, proteins, vitamins and minerals. Foodborne diseases are a persistent problem that can be prevented by proper hygienic care of food products. Bacteria-related foodborne diseases are the most common, and several cause food poisoning or spoilage. To avoid such dilemmas, we have studied the ‘‘green’’ use of Zingiber officinale root extract-mediated synthesis of AgNPs as an antibacterial agent against food pathogens. For over 500 years in Siddha medicine, silver and gold have been used in different proportions with other ingredients, such


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as honey, ghee, milk and leaf juice, for treatment of certain diseases [3–5]. Due to its unique nature and novel developments in technology, silver nanoparticle synthesis, specifically, is a rising area of research and has diverse industrial applications related to biomedical technology, antimicrobials, electrons, optical receptors, catalysts in chemical reactions, sensing, and imaging [6–8]. Gold nanoparticles also have significant bio-applications in areas such as labeling, delivery, heating and sensing [9– 11]; however, due to its cost, it is not as often employed for further study. The main advantage of silver nanoparticles is that they have an inhibitory effect on microbes, which has led to extensive research attempting to understand the assorted mechanisms involved in these effects [12, 13]. Ginger, or zinger root, is the rhizome of the plant Z. officinale, which has been consumed as a delicacy, a medicine, and a spice for over 2,000 years [14]. It is widely used as a folk medicine, and 6-gingerol and its derivatives (1-[40 -hydroxy-30 -methoxyphenyl]-5-hydroxy3-decanone) comprise the major pungent properties of ginger [15]. Up to three percent of ginger contains a fragrant essential oil whose main constituents are sesquiterpenoids, with (-)-zingiberene as the main component. Smaller amounts of other sesquiterpenoids (bsesquiphellandrene, bisabolene and farnesene) and a small monoterpenoid fraction (b-phellandrene, cineol, and citral) have also been identified ( wiki/Ginger). In particular, gingerol-related components have been reported to possess antimicrobial and antifungal properties, as well as several pharmaceutical properties [16, 17]. Microbes can build a resistance against some antibiotics, but not silver ions because silver attacks a broad range of targets in the bacteria [18]. To defend themselves from silver, microbes would have to develop both a host mutation process and resistance simultaneously [19]. In this paper, we present a rapid, simple route of AgNP and AuNP synthesis by reducing aqueous salt solutions of metals silver and gold using Z. officinale root extract. Optimization of the production parameters, including pH, reaction temperature, metal ion concentration, and reaction time, were examined. The synthesized nanoparticles have been examined through various instrumental techniques followed by the analysis of antimicrobial activity against selective food pathogens.

Materials and methods Material used Fresh Z. officinale rhizome was purchased from the local market (Salem, Tamil Nadu, India) and was washed several


times in Milli-Q Ultrapure water (conductivity = 18lX/m, TOC \ 3 ppb, Barnstead, Waltham, MA, USA) to remove dirt. Twenty grams of the rhizome was cut into small pieces and pulverized with a mortar and pestle. The ground-down material was squeezed in a clean muslin cloth to isolate the extract. The extract was filtered using Whatman No. 1 filter paper and stored at 4 °C for further use. The AgNO3, acquired from DaeJung Chemicals, South Korea, and HAuCl4, acquired from Kojima Chemicals, South Korea, were used for the synthesis of AgNPs and AuNPs, respectively. Milli-Q Ultrapure water was used in subsequent experiments. To synthesize AgNPs and AuNPs, two 100-mL Erlenmeyer flasks were filled with 45 mL of Milli-Q Ultrapure water to which we added 5 mL of Z. officinale root extract and either 1 mM AgNO3 or HAuCl4. A control (without addition of AgNO3 and HAuCl4) was also run under the same conditions. Optimization of AgNP and AuNP production The optimization process was carried out with the aim of obtaining the final optimal reaction parameters. The reaction parameters involved in the optimization process were pH (pH 4, 5, 6, 7, 8, 9 and 10), reaction temperature (20, 30, 40, 50, 60, and 70 °C), reaction time(0, 10, 15, 30, 60, 90, 120, 150, 180 and 210 min), and metal ion concentration (0.25, 0.5, 1.0, 1.5, 2.0, 2.5, 3.0, 3.5 and 4.0 mM). The absorbance of samples was measured at 436–531 nm for AgNPs and AuNPs, respectively. The overall production was quantified using the obtained optimal parameters. Synthesis of AgNPs and AuNPs The Z. officinale root extract was used without any further modifications. The Z. officinale root extract and metal ion reaction mixture slowly turned a brown-yellow shade for AgNPs and purple for AuNPs. This was the preliminary means of detection for the formation of AgNPs and AuNPs. A 3.0-mL sample was withdrawn from each reaction mixture at different time intervals, and the maximum absorbance was measured using a UV-1800 UV–VIS spectrophotometer (Shimadzu, Japan). Later, the reaction mixture was filtered through 0.22-lm Steritop Millipore filters, which attach to a vacuum pump, and then filtrates were centrifuged at 9,0609g for 15 min to isolate AgNPs and AuNPs. The resulting pellets were resuspended in sterile, ultrapure water to eliminate any uncoordinated molecules. The process of centrifugation and resuspension in ultrapure water was repeated several times to ensure better separation of free entities from the metal NPs. The obtained NPs were freeze-dried to obtain a powder and stored.

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Characterization of AgNPs and AuNPs The synthesized AgNPs and AuNPs were scanned for maximum absorption of the reaction mixtures between 200 and 800 nm. SEM–EDS (JEOL-64000, Japan) was used to confirm the formation of AgNPs and AuNPs. The morphologies and size distributions of AgNPs and AuNPs were analyzed using transmission electron microscopy (TEM) (Hitachi, H-n650, Japan). X-ray diffraction (XRD) measurements of AgNPs and AuNPs were analyzed on a dropcoated glass substrate and were measured in a Rigaku instrument for the conformation of a crystalline nature. FTIR spectra of AgNPs and AuNPs were obtained with a Perkin-Elmer FTIR spectrophotometer (Norwalk, USA) set in the diffuse reflectance mode at a resolution of 4 particles/cm in KBr pellets. Analysis of antibacterial activity of AgNPs against food pathogens Bacterial strains Cultures of staphylococcus spp., Listeria spp. and Bacillus spp. were obtained from the Department of Microbiology, Periyar University, Tamil Nadu, India, and were used as model strains for antibacterial testing. Strains were maintained on nutrient agar. Agar well diffusion assay The well diffusion method was used to study the antibacterial activity of the synthesized AgNPs [20]. Bacterial suspensions were prepared by growing a single colony overnight in Luria–Bertani broth with a turbidity of 0.5 McFarland standards. Mueller–Hinton agar plates were inoculated with each bacterial suspension and 0.1 mg of the AgNPs dissolved in 1 mL deionized water. Approximately 50 lL of the resulting solution was added to the center of each well with a diameter of 8 mm. Control plates were made using wells containing Z. officinale root extract alone. The antibiotic tetra-cycline was used as a positive control. The plates were incubated at 37 °C for 24 h in a bacteriological incubator, and the zone of inhibition (ZOI) was measured by subtracting the well diameter from the total inhibition zone diameter. Replicates were maintained in all experiments. Minimal inhibitory concentration/minimum bactericidal concentrations The minimal inhibitory concentrations (MICs) and minimum bactericidal concentration (MBC) of the AgNPs nanoparticles were determined by MTT assay using a

96-well microtiter plate [21]. The Z. officinale root extract was used as negative control in all experiments at a concentration of 0.5 mL/mL. Five mL of Luria–Bertani broth medium containing 10–100 lg/mL of AgNPs were prepared by dilution. For the determination of MIC, a single isolate from the Luria–Bertani agar plates was suspended and inoculated in 50 lL of Luria–Bertani broth. After 24 h of incubation, suspensions were diluted in Milli-Q Ultrapure water to obtain final inoculums of 5 9 105–5 9 106 colony-forming units (CFU)/mL. Purity examinations of the isolates were performed by gram-staining and colony morphology assessment throughout the study. Two-fold serial dilutions of the AgNP solution were prepared in Luria–Bertani broth in 98-well plates starting from a stock solution of 10-2 M. A microtiter plate containing 0.05 mL of the serial compound dilution was filled with an equal volume of each bacterial inoculum. After incubation for 24 h at 35 °C, MIC was determined with a POLARstar OPTIMA microplate reader (BMG LABTECH GmbH, Germany). The absorbance was compared with the negative control wells that contained broth with AgNPs, without inoculum, and with the lowest concentration of the compound [22]. The results are expressed as mean values of three independent replicates. Statistical analysis Each experiment was conducted in triplicate, and the resulting bacterial growth on each replicate is reported as the mean ± standard deviation (n = 3). The experimental analysis was based on three independent sample analyses for MIC.

Results and discussion Optimization and characterization of Z. officinale extract-synthesized AgNPs and AuNPs The aqueous AgNO3 and HAuCl4 were added to the Z. officinale root extract, and the color of the reaction mixtures turned either a brown-yellow shade for AgNPs or purple for AuNPs (Fig. 1 inset). Further, the nanoparticles production was confirmed by the surface plasmon resonance (SPR) peak of the metallic AgNPs and AuNPs. The SPR peaks for AgNPs and AuNPs are recorded at 436–531 nm, respectively (Fig. 1). The size and shape of the AgNPs and AuNPs depend on different production conditions. The spherical shape of AgNPs and AuNPs also depend on single SPR bands, which are evidence of the Mie theory. Different pHs found to influence the biosynthesis of AgNPs and AuNPs are presented in Fig. 2a. In our study,


Bioprocess Biosyst Eng Fig. 1 UV–Vis absorption spectra and color change (inset) for AgNP and AuNP formation by Z. officinale root extract

Fig. 2 Effect of pH (a), metal ion concentration (b), temperature (c) and time (d) on AgNP and AuNP synthesis by Z. officinale root extract

absorbance increased when pH increased from 4 to 8 or 4 to 9 for AgNPs and AuNPs, respectively (Fig. 2a). The results indicate that an alkaline pH favored the formation of both AgNPs and AuNPs. Upon evaluating the effect of


different concentrations of silver and gold ions in the reaction mixture, the maximum optical density was found to be a 1.0 mM concentration for both silver and gold ions (Fig. 2b). The effect of temperature on the biosynthesis of

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Fig. 3 EDS spectrum of a AgNPs and b AuNPs prepared from either 1 mM AgNO3 or HAuCl4 ions, respectively

AgNPs and AuNPs is shown in Fig. 2c. As temperature increased from 20 to 50 °C, the absorbance of the reaction mixture increased. The results suggest that an elevated temperature accelerates the reduction process. In addition, we investigated the effect of various time intervals on AgNP and AuNP synthesis. We observed an increase in absorbance at 1.4–2.0 nm for AgNPs and AuNPs, respectively (Fig. 2d), with an increased incubation time (ranging from 10 to 210 min). Figure 2d illustrates that the formation of AgNPs and AuNPs began to take place within 10 min and the absorbance for both types of NP rose after 24 h of incubation. These results indicate that the reaction was very rapid and that particles were well dispersed in the solution. It also indicates that Z. officinale root extract has the potential to biosynthesize metal nanoparticles. Hence, our research proves a significant step in the development of green processes for the synthesis of AgNPs and AuNPs. Each experiment was conducted after obtaining optimal parameters in a step-by-step manner. The EDS graph confirms the presence of elemental silver and gold signals shown in Fig. 3a and b. The peaks at 2 keV can be attributed to AgNPs (a) and AuNPs (b), and the other small peaks may be attributed to the Z. officinale root extract present on the surface of the AgNPs and AuNPs. FTIR analysis was performed to identify the potential biomolecules present in Z. officinale root extract responsible for reduction in AgNPs and AuNPs.

Fig. 4 FTIR absorption spectrum obtained from a AgNPs by reduction in AgNO3 ions and b AuNPs by reduction in HAuCl4 ions through the use of Z. officinale root extract

Figure 4a and b show the FTIR spectra of Z. officinale root extract-capped AgNPs (a) and AuNPs (b). Absorption spectra recorded at 11,650/cm could be accredited to the stretching vibrations of –C=C (alkane). Strong peaks at 1,450/cm (stretching vibration of –C=C), 1,010, 1,033/cm (stretching vibrations –C=O), 850/cm and other peaks at 1,450, 1,500, 1,650, 1,200, 900, 800 and 700/cm are strong signals of heterocyclic compounds such as alkaloids and flavonoids, the active components of Z. officinale, which act as capping agents [12, 16, 17]. An absorption band at 2,950/cm is a characteristic of the –OH stretching of the phenolic group. The peak at 3,300/cm is a characteristic of N–H or C=O and C–H stretching vibrations for AgNPs and AuNPs, respectively. The reduced size of metals silver and gold were confirmed by TEM analysis and are presented in Fig. 5a–d for AgNPs, (a) 100 nm, (b) 20 nm, and AuNPs, (c) 100 nm, (d) 20 nm. The TEM images revealed the morphology and size of AgNPs and AuNPs formed in the reaction mixture, and shapes were observed as predominantly spherical with others being triangular, truncated triangular or hexagonal shapes. From Fig. 5a and b, it is clear that most of the AgNPs were spherical and their dimensions ranged from 10 to 20 nm with an average size of approximately 15 nm. Similarly, Fig. 5c and d depict the TEM images of AuNPs, which are mainly spherical in nature, but also


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Fig. 5 Representative TEM images illustrating the formation of AgNPs, a100 nm, b 20 nm, and AuNPs, c100 nm, d 20 nm, synthesized by Z. officinale root extract

irregular in shape. The diameters of spherical AuNPs are comparatively similar to AgNPs. The difference in shape control for AgNPs and AuNPs could be attributed to the protective and reductive biomolecules present in the Z. officinale biomass. The shape of nanoparticles is an important criterion for any kind of application, since it is directly related to its optical and electrical properties [23– 25]. As far as size is concerned, smaller-sized AgNPs are advantageous for effective targeted drug delivery, photo thermal therapy and the treatment of wounds (antimicrobial) [23, 26, 27]. As shown by XRD, different Bragg reflections patterns are displayed in Fig. 6a and b. Five distinct peaks were observed corresponding to the (110), (111), (200), (220) and (311) sets of lattice planes. They can be indexed as facecentered cubic structures of silver and gold crystals. The XRD patterns coordinate with earlier studies using Cinnamon zeylanicum, Z. officinale and Jatropha curcas for silver synthesis [23, 28, 29].


Antibacterial activity The synthesized AgNPs were tested against gram-positive food pathogenic bacteria, Staphylococcus spp., Listeria spp. and Bacillus spp. The antibacterial activity of AgNPs against food pathogens were observed after 24 h of incubation at 37 °C, and results are presented in Fig. 7 and Table 1. Silver NPs are effective for the inhibition of Staphylococcus spp. and Listeria spp., but not for Bacillus spp. A ZOI around 6.5 ± 0.4 mm (AgNPs) was observed for Staphylococcus spp. and 8.9 ± 0.6 mm for Listeria spp. Minimal inhibitory concentration/minimal bactericidal concentration We confirmed the bactericidal property of AgNPs via MIC/ MBC testing. The MIC was determined as the lowest concentration at which no visible growth of the food pathogen was observed. The MICs of AgNPs were found to be 30 ± 14.3 lg/

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mL for Staphylococcus spp., 20 ± 12.8 lg/mL for Listeria spp., and no inhibition was observed in Bacillus spp. (Table 1). The MBC value for Staphylococcus spp. was 40 ± 10.2 lg/

mL and Listeria spp. was 30 ± 11.5 lg/mL. No remarkable results were observed in Bacillus spp. Mechanism

Fig. 6 XRD patterns of synthesized a AgNPs and b AuNPs synthesized by Z. officinale root extract

The chemical composition of Z. officinale root extract is made up of gingerol, shogaols, zingerone, paradol, and starch. The rhizome, consisting of 6-gingerol and 6-shogaol, is the principal source of gingerol and shogaol, as previously reported [12, 30]. The key compounds responsible for the reduction in Au and Ag nanoparticles are water-soluble ingredients present in the Z. officinale root extract [12]. Ginger holds chemical compounds like oxalic acid, ascorbic acid, phenylpropanoids and zingerone. The AgNPs and AuNPs can be reduced by the ascorbic acid and/or oxalic acid present in the Z. officinale root extract [31]. The possible stages of the formation of AgNPs from ginger extract during the chemical reaction include nucleation, condensation, surface reduction and stabilization as previously described [31]. The color formation in reaction mixtures (Fig. 1 inset) for AgNPs and AuNPs indicate the excitation of surface plasmon vibrations within the AgNPs and AuNPs [31, 32]. The color of the silver solution changes from pale yellow to dark brown with a yellow shade within 150 min after the addition of ginger rhizome extract. The gold solution changes from pale yellow to purple within 180 min. The presence of free electrons in AgNPs and AuNPs has given rise to a SPR absorption band

Fig. 7 Bacterial cultures showing the inhibition zones around AgNPs in wells containing Staphylococcus spp., Listeria spp., and Bacillus spp. food pathogens Table 1 Antibacterial activity of Z. officinale root extractsynthesized AgNPs (ZOI, MIC and MBC) against food pathogens Staphylococcus spp., Listeria spp., and Bacillus spp.

Bacterial strains

Gram class

ZOI (mm)

MIC (lg/mL)

MBC (lg/mL)

Silver nanoparticle Staphylococcus spp.

Gram-positive, cocci

6.5 ± 0.4

30 ± 14.3

40 ± 10.2

Listeria spp.

Gram-negative, rod

8.9 ± 0.6

20 ± 12.8

30 ± 11.5

Bacillus spp.

Gram-positive, rod



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[32–35] due to the collective vibration of electrons in metal nanoparticles in resonance with the light wave [34]. Usually, a few chemical molecules are sufficient to reduce metal ions into nanoparticles. However, in green synthesis of metal nanoparticles, natural material extract acts as a reducing agent for the generation of metal nanoparticles [33]. The concentration of the reducing materials might play a crucial role in the determination of shape, size and reaction time. The mechanistic actions of AgNPs against bacterial pathogens are not fully understood. However, a few possible mechanisms for the antimicrobial activity of AgNPs against gram-positive bacteria have been proposed. Generally, the three-dimensional thick peptidoglycan layer found in gram-positive bacteria possesses linear polysaccharide chains crosslinked by more short peptides. Thus, it forms a complex structure that leads to difficult penetration of AgNPs into gram-positive bacteria compared with that of gram-negative bacteria [21, 36–38]. Silver has been used for years in the medical field in antimicrobial applications due to its antimicrobial properties and even an ability to prevent HIV binding to host cells. Additionally, silver has been used in environmental applications like water and air filtration [32]. The mechanism and the bactericidal effect of silver and AgNPs were well known prior to this study. Few studies have reported that disturbing permeability and respiration functions of the cell by AgNPs might allow AgNPs to attach to the surface of the cell membrane [30, 31]. This same study describes how a larger surface area on smaller AgNPs may have a greater bactericidal effect than the larger AgNPs. Silver nanoparticles not only function through membrane interaction, but can also penetrate bacteria to disturb cell structure [1, 21].

Conclusion In conclusion, we present a simple and rapid approach for the synthesis of AgNPs and AuNPs through the use of Z. officinale root extract as a reducing agent. We have also demonstrated the antibacterial activity of AgNPs against foodborne pathogens. The synthesized AgNPs were exceptionally stable and showed antimicrobial activity. The strong antimicrobial activities of AgNPs have gained increasing interest due to cross-infection caused by microorganisms and rising health awareness. The application of AgNP nanotechnology in the food industry will have a profound impact on a number of products. Antimicrobial material use has increased in various industries such as food production, agriculture, and antimicrobial coatings for medical instruments. The results of this study have clearly demonstrated that AgNPs inhibited the growth and multiplication of the tested foodborne pathogens. Strong antibacterial activity was observed in gram-positive


bacteria. Further studies are needed in order to determine the atoms in the functional groups involved in the binding and stability of Z. officinale root extract-synthesized AgNPs. The ability to synthesize AgNPs as potential antimicrobial agents using Z. officinale root extract is highly promising for green, sustainable production of nanoparticles that have diverse industrial applications. Acknowledgments This research was supported by the Korean National Research Foundation (Korean Ministry of Education, Science and Technology, Award NRF-2011-35B-D00020). The preparation of this manuscript was supported by research funds from Chonbuk National University in 2013.

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Green synthesis of silver and gold nanoparticles using Zingiber officinale root extract and antibacterial activity of silver nanoparticles against food pathogens.

In the present study, we synthesized silver and gold nanoparticles with a particle size of 10-20 nm, using Zingiber officinale root extract as a reduc...
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