Bioprocess Biosyst Eng (2014) 37:1935–1943
DOI 10.1007/s00449-014-1169-6
ORIGINAL PAPER
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 / Published online: 26 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: btoh@jbnu.ac.kr
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: ksbang@jbnu.ac.kr
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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1936
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 (http://en.wikipedia.org/
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
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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
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.
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
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,
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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
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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
Bioprocess Biosyst Eng (2014) 37:1935–1943
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.
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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].
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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
None
–
–
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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
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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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