Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P.

95–100
DOI: 10.1007/s13131-017-1099-7
http://www.hyxb.org.cn
E-mail: [email protected]

Biogenic synthesis of silver nanoparticles using ginger (Zingiber

officinale) extract and their antibacterial properties against
aquatic pathogens
YANG Nan1, LI Fuyan1, JIAN Tiancai1, LIU Chongchong2, SUN Hushan1, WANG Lei1*, XU Hui2
1 School of Life Sciences, Ludong University, Yantai 264025, China

2 School of Chemistry and Materials Science, Ludong University, Yantai 264025, China

Received 22 February 2017; accepted 6 April 2017

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2017

Abstract
With the development of aquaculture, there is an urgent demand for an alternative antibacterial agent to reduce
the drug resistance and environmental pollution caused by the abuse of antibiotics. Recently, silver nanoparticles
(AgNPs) have been viewed as a novel type of antimicrobial agents due to their unique advantages. In this study,
AgNPs were biosynthesized with the ginger rhizomes extract. The biosynthesized AgNPs were characterised by
UV–visible spectroscopy, transmission electron microscopy, X-ray diffraction and fourier transform infrared
spectroscopy. Furthermore, the antimicrobial activities of the AgNPs were fully analyzed against six typical
aquatic pathogens. The results indicated that the components in ginger extract could function as the chemical
reductant to synthesize AgNPs. Moreover, compared with the AgNPs synthesized by chemical methods, the
biosynthesized AgNPs were smaller, and had higher stability and antibacterial activity. Therefore, the
biosynthesized AgNPs using ginger extract may have prospective applications in aquaculture.
Key words: ginger, silver nanoparticles, biosynthesis, antibacterial activity, aquatic pathogen
Citation: Yang Nan, Li Fuyan, Jian Tiancai, Liu Chongchong, Sun Hushan, Wang Lei, Xu Hui. 2017. Biogenic synthesis of silver
nanoparticles using ginger (Zingiber officinale) extract and their antibacterial properties against aquatic pathogens. Acta Oceanologica
Sinica, 36(12): 95–100, doi: 10.1007/s13131-017-1099-7

1  Introduction and compatibility for biomedical applications. Moreover, the

With the development of aquaculture, aquatic animal dis- bioactive compounds in the extract are supposed to improve the
eases caused by pathogens have become one of the biggest risk characteristics of the nanoparticles (NPs). For example, the pro-
factors in the aquaculture industry (Francis et al., 2001). Among teins in Aspergillus oryzae var. viridis extracts could cap the AgN-
these pathogens, a substantial proportion accounted for the con- Ps and prevent their aggregation (Binupriya et al., 2010). There-
ditions of pathogenic bacteria. Fish farmers have been forced to fore, the biosynthesis of AgNPs would provide a new way for the
use antibiotics to inhibit the infections. However, abuse of antibi- development of novel antimicrobial agents.
otics could not only pollute environment, but could also lead to Ginger (Zingiber officinale) is not only a well-known spice
serious drug resistance of pathogens on a very large scale plant, but also a traditional oriental medicine used to treat many
(Schmidt et al., 2000). Thus, there is an urgent demand for an al- diseases such as cough, nausea and vomiting, colds, rheumatism,
ternative antibacterial agent to effectively control the aquatic cardiac disorders, inflammation and tumours (Leach and Kumar,
pathogenic bacteria. 2008; Dehghani et al., 2011; Ding et al., 2013). Ginger has been
As effective antibacterial agents, silver nanoparticles (AgNPs) found to contain a variety of bioactive compounds, including al-
have attracted much attention in the past decade (Martinez-Gu- kaloids, flavonoids, zingiberene, gingerols and shogaols, most of
tierrez et al., 2010; Pavagadhi et al., 2014). AgNPs can be synthes- which exhibit antioxidant activities (Shukla and Singh, 2007; Park
ized by a variety of methods, among which chemical reduction et al., 2008; Butt and Sultan, 2011). Given that ginger is rich in an-
are the most commonly used (Darroudi et al., 2011). However, tioxidants, the biomolecules in ginger extract are supposed to
during the process, toxic chemicals are unavoidable as reducing play a crucial role in the reduction of silver ions (Ag+) to metallic
agent and stabilising agent. Recently, the green synthesis of AgN- AgNPs (Ag0). Velmurugan et al. (2014) synthesized AgNPs using
Ps has been developed via different biological systems, including ginger root extract and proved their antimicrobial activity against
bacteria, fungi, yeasts, algae or plants (Narayanan and Sakthivel, food pathogens of Staphylococcus spp., Listeria spp. and Bacillus
2010; Hebbalalu et al., 2013; Miri et al., 2015). The extracts from spp. However, to the best of our knowledge, there are no reports
living organisms can act as reducing and stabilising agents. There on antibacterial investigation of the ginger mediated AgNPs
are many advantages in the synthesis of AgNPs via biological ex- against aquatic pathogens.
 tract, such as eco-friendliness, low cost, mild reaction conditions
 
In this study, the AgNPs were biosynthesized with the aid of
Foundation item: The Scientific Research Projects of Shandong University under contract No. J15LE03; the Key Research and
Development Program of Shandong Province under contract No. 2016GNC111016; the Key Research and Developement Program of
Yantai under contract No. 2016ZH059.
*Corresponding author, E-mail: [email protected]
 
96 YANG Nan et al. Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P. 95–100  

ginger extracts at moderate temperatures within a short period of colony-forming units) was spread evenly on nutrient agar plates
time. Moreover, antibacterial analysis showed that the biosyn- (tryptone 5.0 g/L, yeast extract 1.0 g/L, ferric phosphate 0.1 g/L,
thesized AgNPs exhibited powerful antimicrobial activities agar 15 g/L, and seawater 1.0 L). Oxford cups (8 mm in diameter)
against all tested aquatic pathogens, which revealed their new were gently placed on the inoculated agar plates, and 20 μL of the
potential in aquaculture field. respective AgNPs samples was added to the cups. Sodium citrate
and ginger extract served as controls. All plates were incubated at
2  Materials and methods 28°C overnight. The zones of inhibition were measured and re-
ported as an average. Experiments were performed in quadrup-
2.1  Materials licate.
The dried rhizomes of experimental material ginger (Z. offi- Minimum inhibition concentration (MIC) of synthesized Ag-
cinale) were purchased from a local market of Yantai, China. The NPs was determined by broth dilution assay. V. anguillarum was
ginger was washed thoroughly with tap water followed by dis- chosen as the model organism. The samples were diluted and ad-
tilled water, shade-dried for a week and stored at 4°C for further ded to 4 mL of 2216E liquid culture medium with tested bacterial
study. Silver nitrate (AgNO 3 ) and sodium citrate (Na 3 C 6 H 5 O 7 · concentrations of 106 cfu/mL (the final concentration of the sil-
2H 2 O) were purchased from China National Pharmaceutical ver sample was 0.8–50 µg/mL). The 2216E medium was used as
Group Corporation as analytical grade. Nutrient agar and nutri- negative control and 106 CFU/mL bacterial suspensions as posit-
ent broth were purchased from Sangon Biotech (Shanghai) Co., ive control. Bacterial growth was observed after 24 h of incuba-
Ltd. Deionised water was used throughout the experimental pro- tion at 28°C. The lowest concentration of the prepared AgNPs at
cedure. which no bacterial growth was observed in the culture suspen-
sions was defined as the MIC. To ensure accuracy of results, the
2.2  Chemical synthesis of AgNPs experiment was repeated three times.
The AgNPs were prepared by chemical reduction. In brief, 2 For the bacterial inhibition kinetic test, V. anguillarum was
mL of 0.01 mol/L AgNO3 was added to 16 mL of deionised water. also selected as the index bacterium and incubated overnight at
After the solution was boiled, 2 mL of 0.002 g/mL sodium citrate 28°C. The bacterial culture suspension was adjusted to 10 6
was added drop by drop to the AgNO3 solution with constant stir- cfu/mL, and then the two obtained AgNPs as well as ginger ex-
ring. Boiling was continued for 1 h until the colourless mixed tract and sodium citrate was added at a final concentration of 10
solution turned dark brown. μg/mL, respectively. The bacteria solution was incubated at 28°C
while being shaken at 150 r/min. Bacterial growth rates were
2.3  Biosynthesis of AgNPs measured by monitoring the optical density at 600 nm (OD600) at
Ginger extract was prepared by cutting 5.0 g of rhizome into different time intervals using a UV–vis spectrophotometer (Shi-
small pieces, which were refluxed with 100 mL of 70% ethanol at madzu UV-2550). Normal saline was used as control. To ensure
70°C for 2 h. After cooling, the obtained extract was filtered accuracy of results, the experiment was repeated three times.
through Whatman No. 1 filter paper and centrifuged. The super-
natant was collected and stored at 4°C. 2.6  Stability experiment
For the biosynthesis of AgNPs, 1 mL of ginger extract was ad- The stability of the AgNP hydrocolloid was determined by
ded to 20 mL of the AgNO3 solution (1 mmol/L) in a round-bot- visual inspection after 90 days of storage in 4°C, followed by
tom flask. The mixture was heated at 85°C and color change of UV–vis spectroscopy and the agar well diffusion method.
the solution was recorded within 20 min.
3  Results and discussion
2.4  Characterization
The as-prepared AgNPs were characterised by UV–visible 3.1  Characteristics of AgNPs
(vis) spectroscopy on a Shimadzu UV-2550 spectrophotometer in We synthesized two kinds of AgNPs: C-AgNPs by sodium cit-
the range of 200–800 nm. The size and shape of AgNPs were ana- rate and B-AgNPs by ginger extracts. As shown in Fig. 1a, the col-
lyzed by transmission electron microscopy (TEM, JEM 1011) at our of the reaction solution changed to dark brown with sodium
an acceleration voltage of 100 kV. The freeze-dried powder of the citrate and golden yellow with ginger extracts, indicating the
resulting AgNP solution was used for X-ray diffraction (XRD; formation of AgNPs (Fig. 1a). The colour change is attributed to
Rigaku D/max-2500VPC) with Ni-filtered Cu Kα radiation at a the excited surface plasmon resonance (SPR) of the AgNPs and
scanning rate of 0.02°/s from 25° to 80°. The Fourier transform in- the colour depth is dependent on the concentration and size of
frared spectroscopy (FTIR) spectra of the samples were recorded the NPs (Mulvaney, 1996). The formation of AgNPs was further
by FTIR (Nicolet Nexus 670). examined by UV–vis spectroscopy. As shown in Fig. 1b, the ab-
sorption spectrum of C-AgNPs displayed a strong peak at 415 nm,
2.5  Antibacterial activity studies whereas the B-AgNPs at 423 nm. Both of the characteristic peaks
The antibacterial activity of the synthesized AgNPs was as- located in 400–500 nm, which was the λmax range of typical AgN-
sayed by the agar well diffusion method (Wang et al., 2016). Six Ps (Sadeghi and Gholamhoseinpoor, 2015). These results indic-
typical aquatic pathogenic strains of Vibrio anguillarum, Vibrio ated that the components in ginger extract could function as the
alginolyticus, Aeromonas punctata, Vibrio parahaemolyticus, Vi- chemical reductant to synthesize AgNPs.
brio splendidus and Vibrio harveyi (stored in the Department of The morphology and size of the prepared AgNPs were evalu-
Marine Biological Technology, Ludong University) were used to ated by high-magnification TEM. The C-AgNPs were heterogen-
determine the antibacterial activity of the AgNPs. The test bac- eously dispersed with the size range of 20–80 nm, the majority of
teria were cultivated at 28°C overnight in 2216E liquid culture which were polygonally shaped (Fig. 2a). By contrast, B-AgNPs
medium (tryptone 5.0 g/L, yeast extract 1.0 g/L, ferric phosphate were spherical and almost monodispersed with an average
0.1 g/L, and seawater 1.0 L). About 100 μL of the bacterial culture particle size of 10 nm (Fig. 2b). It is known that as for the AgNPs,
suspensions with final concentrations of 10 6 cfu/mL (cfu is the morphology and size are important criterions for any kind of
  YANG Nan et al. Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P. 95–100 97

a b
ginger extracts
0.6 B-AgNPs
sodium citrate
C-AgNPs

Absorbance/a.u.
0.4
sodium citrate C-AgNPs
solution

0.2

0
300 400 500 600 700
ginger extract B-AgNPs Wavelength/nm
 
Fig. 1.   Production of AgNPs using sodium citrate and ginger extract (a), and UV–vis absorption spectra of synthesized AgNPs (b).

a b

50 nm 50 nm

 
Fig. 2.   TEM micrographs of C-AgNPs (a) and B-AgNPs (b).

application (Panáček et al., 2005). Previous studies also showed ans (Vidhu et al., 2011). The calculated grain sizes of the C-AgN-
that spherical AgNPs with smaller size were anticipated to exhib- Ps and B-AgNPs were about 18.7 nm and 9.2 nm, respectively,
it higher antibacterial properties (Pal et al., 2007; Singh et al., which were in agreement with the results of TEM analysis.
2008). Hence, the results above indicated that the prepared B-Ag- The FTIR spectra of C-AgNPs, B-AgNPs and ginger extract in
NPs were at an ideal state as antimicrobial agents. the range of 4 000–500 cm–1 were shown in Fig. 4. The ginger ex-
The crystalline structure of the synthesized AgNPs was invest- tract had peaks at 3 425.07, 2 919.28, 2 850.16, 2 361.78, 2 341.32,
igated by XRD analysis (Fig. 3). In the case of C-AgNPs, four dis- 1 735.22, 1 639.13, 1 382.13 and 1 083.70 cm–1. Notably, the strong
tinct diffraction peaks at 2θ=38.1°, 44.3°, 64.4° and 77.4° corres-
ponded to the (111), (200), (220) and (311) planes of the face-
centred cubic crystalline structure of Ag (JCPDS file No. 65– (111)
2 871). Thereby, the XRD pattern revealed that the sample was
composed of crystalline face centered cubic (fcc) lattice struc-
tures of elemental silver. For B-AgNPs, two weak peaks centred at
2θ of 38.1° and 44.3° were observed because of the low concentra-
Intensity/a.u.

tion of AgNPs, which was consistent with the aforementioned

results of UV–vis spectroscopy. Some of the unassigned diffrac- (a) (200)
tion peaks might be related to the crystallisation of bioorganic (220) (311)
phases that attached to the surface of the NPs. C-AgNPs
(b)
The size of the NPs was thus determined based on Scherer’s
equation:
B-AgNPs

D = k λ / β cosθ ,
10 20 30 40 50 60 70 80
where D is the average crystal size, k is the Scherer coefficient 2θ/(°)
(0.89), λ is the X-ray wavelength (λ=1.540 6×10–10 m), θ is Bragg’s  
angle (2θ), β is the full width at half maximum (FWHM) in radi- Fig. 3.   XRD patterns of C-AgNPs (a) and B-AgNPs (b).
98 YANG Nan et al. Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P. 95–100  

at 2 919.28 and 2 850.16 cm–1 were caused by the C-H stretching

vibrational mode, whereas the peaks at 1 632.28 and 1 735.22
cm –1 were attributed to the C=O stretching vibration of alde-
ginger extract hydes and flavonoid. The peak at 1 382.13 cm–1 was attributed to
the O-H deformation vibration of tertiary C-OH groups. Another
weak peak near 1 083.70 cm–1 represented the C-O stretching vi-
Transmittance/%

bration. The FTIR spectra of B-AgNPs shared very similar absorp-

tion peak positions with that of the ginger extract, which indic-
B-AgNPs ated the presence of ginger extract on the surface of the AgNPs.
Besides, the peaks both at 3 400 cm–1 and 1 631.38 cm–1 of the B-
AgNPs were obviously stronger than those of the C-AgNPs, which
C-AgNPs further confirmed that the compounds in ginger extract interac-
ted with the surface of AgNPs.

1 000 2 000 3 000 4 000 3.2  Antimicrobial activities of synthesized AgNPs

Wavenumbers/cm-1 The antibacterial activity of synthesized AgNPs against six
 
typical aquatic pathogens was evaluated by the agar well diffu-
Fig. 4.   FTIR spectra of C-AgNPs, B-AgNPs and ginger extract. sion method. As shown in Fig. 5 and Table 1, sodium citrate solu-
tion did not produce any inhibition zone against the tested bac-
and wide band at 3 425.07 cm–1 referred to the strong stretching teria; the ginger extract and C-AgNPs showed the inhibition
vibrations of the O-H functional group. The corresponding peaks zones which were slightly larger than the oxford cup, indicating

Vibrio anguillarum Vibrio alginolyticus

4 1
4 1

3 2 3 2

Aeromonas punctata Vibrio parahaemolyticus

4 1 4 1

3 2 3 2

Vibrio splendidus Vibrio harveyi

4 1
4 1

3 2 3 2

 
Fig. 5.   Antibacterial effect of synthesized AgNPs against six different aquatic pathogens. 1. C-AgNPs, 2. B-AgNPs, 3. sodium citrate
solution, and 4. ginger extract.
  YANG Nan et al. Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P. 95–100 99

both of them had weak antibacterial activities. By contrast, B-Ag- were incubated with equal volumes of V. anguillarum, respect-
NPs exhibited the significant inhibition zones against all of the ively. After 24 h of incubation, bacterial growth was studied by
tested bacteria, indicating that the B-AgNPs had a broad spec- visual inspection. The MIC value of B-AgNPs was defined as 12.9
trum of antibacterial activities and was promising in the treat- μg/mL and C-AgNPs was 50.0 μg/mL (Table 2). The result indic-
ment of aquatic pathogenic bacteria. ated that B-AgNPs showed relatively higher antibacterial activity
For the MIC tests, gradiently diluted B-AgNPs and C- AgNPs than C-AgNPs.

Table 1.   Diameter of inhibition zone (mm) of the synthesized AgNPs against various aquatic pathogenic bacteria
Inhibition zone
Pathogenic bacteria Test Control
C-AgNPs B-AgNPs Sodium citrate Ginger extract
Vibrio anguillarum 8.4±0.03 15.8±0.05 NA 8.1±0.19
Vibrio alginolyticus 8.8±0.09 14.1±0.10 NA 8.0±0.00
Aeromonas punctata 8.5±0.04 13.5±0.07 NA 8.5±0.41
Vibrio parahaemolyticus 8.8±0.10 14.9±0.09 NA 8.2±0.21
Vibrio splendidus 8.4±0.08 11.1±0.02 NA 8.1±0.09
Vibrio harveyi 8.3±0.03 13.6±0.03 NA 8.2±0.12
          Note: Values are expressed as the mean±standard error of the mean (n=3). NA means not appearing.
Table 2.   Comparison of the MIC values of different samples (n=3)
Concentration of Ag/μg·mL–1 B-AgNPs C-AgNPs Sodium citrate Ginger extract
50.0 – – + +
25.0 – + + +
12.9 – + + +
6.5 + + + +
3.3 + + + +
1.6 + + + +
0.8 + + + +
0.4 + + + +

Furthermore, antibacterial activity kinetics for the silver nan- 1.4

10 µg/mL C-AgNPs
oparticles samples as well as ginger extract and sodium citrate to-
10 µg/mL B-AgNPs
ward V. anguillarum were studied. The 10 μg/mL of each sample 1.2
10 µg/mL ginger extract
was incubated in bacterium suspensions, and bacterial growth
10 µg/mL sodium citrate
rate was monitored by measuring the optical density of the cul- 1.0
normal saline
ture solution at various time intervals (Fig. 6). For the negative
OD (600 nm)

0.8
control of normal saline, the optical density increased rapidly
during the bacteria log phase, indicating the reproduction of V. 0.6
anguillarum. The sodium citrate shared a similar growth curve of
V. anguillarum with the negative control, while both C-AgNPs 0.4
and ginger extract caused a growth delay of V. anguillarum and
the growth curve increased gradually with a longer lag phase. 0.2
Notably, V. anguillarum was completely inhibited as the optical
density was almost the constant when treated with 10 μg/mL B- 0
0 30 60 90 120 150 180
AgNPs. These results confirmed that the prepared B-AgNPs had
Time/min
powerful antibacterial activities against the aquatic pathogen.  
AgNPs have been found to attach to the surface of the bacteri- Fig. 6.   Growth curve of V. anguillarum in 2216E media. C-AgN-
al membrane, cause structural changes of the membrane, and fi- Ps, B-AgNPs, ginger extract and sodium citrate (10 μg/mL) was
nally lead to death of the microbe cells (Sondi and Salopek- added into the culture, respectively.
Sondi, 2004; Kim et al., 2007). Generally, smaller AgNPs have a
greater ability to penetrate cell membrane, and thus improve an- tibacterial activity (Teeguarden et al., 2007). Thus, we further
tibacterial activity (Singh et al., 2008; Dubey et al., 2010). In this evaluated the stability of C-AgNPs and B-AgNPs after 90 days.
study, B-AgNPs with smaller and more uniform size possessed The UV–vis absorption spectra showed that an obvious red-shift
significantly higher antibacterial activity than C-AgNPs, which is was observed in the surface plasmon peak of C-AgNPs, while the
consistent with the previous reports. Besides, as the previous shift was almost negligible in that of B-AgNPs (Fig. 7). The results
studies, the bioactive compounds in the ginger extract are sup- indicated that C-AgNPs were agglomerated and B-AgNPs were
posed to improve the characteristics of the B-AgNPs, thereby par- still well dispersed after 90 days. In addition, B-AgNPs still
tially contributing to the higher antibacterial activities of B-AgN- showed remarkable diffusion zones against the tested aquatic
Ps (Niraimathi et al., 2013). pathogens after 90 days, whereas C-AgNPs no longer produced
inhibition zones (data not shown). Velmurugan et al. (2014)
3.3  Stability study proved that the existence of phenolic compounds, terpenoids
The stability of AgNPs is a key factor that determines their an- and proteins in ginger extract may prevent agglomeration and
100 YANG Nan et al. Acta Oceanol. Sin., 2017, Vol. 36, No. 12, P. 95–100  

tracts, enzymes, bacteria, biodegradable polymers, and mi-

crowaves. ACS Sustainable Chemistry & Engineering, 1(7):
1.2 new synthesized C-AgNPs
703–712
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of silver nanoparticles using Prosopis farcta extract and its anti-
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4  Conclusions study of the gram-negative bacterium Escherichia coli Applied
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morphology. XRD and FTIR analyses confirmed that the active 16248–16253
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AgNPs. Moreover, the B-AgNPs showed higher antibacterial and [12]-gingerol isolated from ginger rhizome against period-
activities against aquatic pathogens than C-AgNPs. Besides, B- ontal bacterial. Phytotherapy Research, 22(11): 1446–1449
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