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Synthesis of silver nanoparticles from Annona diversifolia Safford and their

potential use as a green alternative to control of pathogenic microorganisms

Article  in  JOURNAL OF RENEWABLE MATERIALS · May 2020

DOI: 10.32604/jrm.2020.09845

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Journal of Renewable Materials Tech Science Press
DOI:10.32604/jrm.2020.09845
Article

Green Synthesis of Silver Nanoparticles Using Annona diversifolia Leaf Extract

and Their Antimicrobial Application
Rogelio Solorzano-Toala1, Daniel Gonzalez-Mendoza2,*, Benjamin Valdez-Salas3, Vianey Mendez-
Trujillo4, Federico Gutierrez-Miceli1, Ernesto Beltran-Partida3 and Olivia Tzintzun-Camacho2

1
Tecnológico Nacional de México-Campus Tuxtla Gutiérrez, Tuxtla Gutiérrez, 03940, México
2
Instituto de Ciencias Agrícolas de la Universidad Autónoma de Baja California, Mexicali, 21705, México
3
Instituto de Ingeniería de la Universidad Autónoma de Baja California, Mexicali, 21100, México
4
Facultad de Medicina de la Universidad Autónoma de Baja California, Mexicali, 21100, México
*Corresponding Author: Daniel Gonzalez-Mendoza. Email: [email protected]
Received: 21 January 2020; Accepted: 27 May 2020

Abstract: The aim of this study was the synthesis of silver nanoparticle using
Annona diversifolia Safford. The silver nanoparticles obtained were analyzed
by spectroscopic methods and dynamic light scattering methods. The inhibition
of AgNPs was evaluated against Bacillus cereus, Klebsiella pneumoniae and
Enterobacter aerogenes. The results showed that AgNPs have high values at
3 keV and particle size between 45 to 58 nm with a homogenous morphology.
The AgNPs showed growth inhibition against Klebsiella pneumoniae and Enter-
obacter aerogenes. Therefore studies are needed to confirm the potential antimi-
crobial of different AgNP from A. diversifolia in Gram negative and Gram
positive bacteria.

Keywords: Green chemistry; AgNPs; plants; antimicrobial; biotechnology

1 Introduction
Currently, the nanotechnology opens the possibility for a wide variety of applications in agronomy
sciences. Recent reports have shown that silver nanoparticles (AgNPs), due to their antimicrobial activity,
could be considered as an alternative route for the design of a new generation of antimicrobial agents
[1,2]. The nanoparticles have different mechanism of action against bacterial cells: (1) cell wall and
membrane disruption; (2) AgNPs penetration and intracellular damage disrupting metabolic pathways; (3)
biomolecules damage (e.g., DNA or proteins); and (4) free radicals production (e.g., reactive oxygen
species generation) which may cause disruption in lipid membrane [3]. Generally, metallic nanoparticles
are prepared using a great variety of chemical and physical methods which are quite expensive and
potentially hazardous to the environment [4]. In contrast, green synthesis is a biotechnology optional to
chemical and physical methods [5]. Today, the use of plants as source of metabolites for the reduction of
different metals has been emphasized for the synthesis of metallic-nanoparticles [4,6]. Although there
have been numerous studies about the toxicity of metallic nanoparticles obtained from chemical or
physical methods on pathogenic bacteria, research on green synthesis of silver nanoparticles and their
antimicrobial activities are insufficient [7]. In this sense, certain studies have proposed the synthesis of

This work is licensed under a Creative Commons Attribution 4.0 International License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original
work is properly cited.
2 JRM, 2020, vol.XX, no.XX

AgNPs using aqueous extract of plants as bioreducing agents and their antimicrobial activity against Gram-
positive and Gram-negative bacteria [4].
The genus Annona L. is the most important of the Annonaceae family due to its tasty flavor, high pulp
content, and nutritional value and antioxidant properties. This genus is native from Southwestern Mexico and
Central America. A previous research indicates that the region of Southeast Mexico and Guatemala is known
as the center of origin of A. diversifolia [8]. This plant occupies a relevant position in Mexican fruticulture
mainly Southeast region due to their significant content of total phenols, flavonoids and their antioxidant
activity in leaves [9].
However, even though the biochemical and medicinal properties effects of A. diversifolia leaves have been
previously studied the use of A. diversifolia to synthesize silver nanoparticles has been scarcely evaluated. It is
important for the aqueous extract of the leaves of A. diversifolia to be studied, especially since the information
can be used for its properties that can be employed as a disinfectant solution for vegetables which can be
transformed into solution for sanitizers. Therefore, in the present study, we report the synthesis of silver
nanoparticles using leaves of Annona diversifolia and their antimicrobial activity against bacteria (Bacillus
cereus, Klebsiella pneumoniae, Enterobacter aerogenes) causing of diseases in vegetables.

2 Experimental
2.1 Materials
Samples of fresh and healthy leaves of Annona diversifolia were obtain from a native population in
Comitan, Mexico. The aqueous extract of leaves was prepared by taking 30 g of each plant leaves and
mixed with 300 mL of distilled water. Then, the mixture was kept in agitation to 2.5 g for 24 h at
constant temperature. The samples were then centrifuged at 5000 g for 10 min to remove particulate
matter and to get clear solutions, which were then stored under refrigeration at 4°C until use.

2.2 Biosynthesis of Silver Nanoparticles (AgNPs)

For biosynthesis of AgNPs an aqueous solution of silver nitrate (10 mM) was prepared and mixed with
the leaf extract of A. diversifolia at a ratio of 4:1 (v/v). This solution was placed on a shaker in a dark chamber
to minimize photo-activation of silver nitrate at room temperature with constant rotation at 40 ± 2°C for
30 min. The bio-reduction of Ag+ to Ag0 was confirmed by the color changing of the solution, which
went from colorless to a brown shade. Its formation was also confirmed by measuring the absorbance of
the AgNPs in solution from A. diversifolia leaf extract at 300–700 nm in a UV/V is spectrophotometer.
The AgNPs were purified by centrifugation at 6000 g for 10 min and the precipitate was lyophilized for
their used in antibacterial activity.

2.3 Characterizations of Biosynthesized AgNPs

Dynamic Light Scattering (DLS) and laser Doppler velocimetry (LDV) for characterization of size and
zeta potential of AgNPs in solution from A. diversifolia, was performed using a nanotrac wave instrument
(Microtrac) [10].

2.4 Scanning Electron Microscopy (SEM) and Energy Dispersive Spectroscopy (EDS)
To identify the size, morphology and composite homogeneity of AgNPs from A. diversifolia a scanning
electron microscope (SEM) JEOL 6010 was employed according to Abdelmoteleb et al. [2]. For EDS analysis,
the AgNPs were drop-coated on to a carbon film and analyzed using instrument Bruker Quantax 400.

2.5 Antimicrobial Analysis

The antimicrobial activity of AgNPs was analyzed with disk diffusion method according to Gonzalez-
Mendoza et al. [11]. 50 µl of aliquots of Bacillus cereus, Klebsiella pneumoniae, Enterobacter aerogenes at a
JRM, 2020, vol.XX, no.XX 3

concentration of 10 × 105 cells/mL were inoculated on sterile nutrient agar petri dishes. Then 20 μl of
synthesized AgNPs solution at 25%, 50%, 75% and 100% were prepared in distilled water and dropped
on 7 mm sterile filter paper discs. Dried filter paper disks containing the different concentrations of
AgNPs were placed in petri dishes and an absolute control (only leaf extract), negative control (discs with
only water) and positive control (AgNO3 solution) were separately prepared. Finalized, the period of
incubation of each treatment (30°C ± 2°C for 24), the inhibition zones were visualized.

2.6 Total Phenol and Flavonoids Contents

The content of total phenolic compounds and flavonoids contents of the leaf extract and AgNPs from A.
diversifolia were determined by colorimetric methods, according to proposed by Cervantes-Garcia et al. [12].
The content of phenolic compounds was expressed as mg GAE (equivalent of gallic acid)/gram of dry extract
(DE) at 760 nm against blank. On the other hand, the flavonoids were calculated as mg quercetin equivalents
(QE) per gram of DE at 510 nm.

2.7 Statistical Analysis

Differences between the treatments were compared using Tukey’s test (p ≤ 0.05), and Statistica Version
9.0 was used. Significant differences were accepted if p ≤ 0.05. Results are indicated with the average of the
values determined ± standard deviation (SD).

3 Results and Discussion

3.1 UV-VIS Spectrometry
In the present study, the synthesis of AgNPs was primarily confirmed by the formation of pale yellow color
suggests the presence of silver nanoparticles due to the interaction of phytochemicals of aqueous extract of A.
diversifolia that reduces silver ions into Ag-nanoparticles (Fig. 1). The formation of AgNPs by reduction of
aqueous Ag during exposure to A. diversifolia extract was characterized by UV-Visible spectroscopy.
As shown in Fig. 2, the surface plasmon resonance (SPR) of the AgNPs was centered at approximately 460 nm.

Figure 1: Green synthesis of AgNPs using extracts of A. diversifolia

3.2 SEM and EDS

The morphology and size of AgNPs from A. diversifolia was analyzed using SEM, as shown in Fig. 3a.
The SEM analysis clearly show AgNPs agglomerated, forming spherical-shaped particles with smaller size
(45 to 58 nm). On the other hand, the EDS of AgNPs (Fig. 3b) revealed the presence of pure silver (45.92%)
4 JRM, 2020, vol.XX, no.XX

0.9
A.diversifolia leaf aqueous extract
0.8 Silver nanoparticles (AgNPs)

0.7

0.6

Absorbance
0.5

0.4

0.3

0.2

0.1

0.0

-0.1
300 330 360 390 420 450 480 510 540 570 600 630 660 690
Wavelength (nm)

Figure 2: UV-Vis absorption spectrum of AgNPs and aqueous extract of A. diversifolia

a)

b) cps/eV
Mass percent (%)
18
Spectrum C O Si Cl Ag
---------------------------------------
16
Objects 1 9.94 1.95 80.36 - -
14 Objects 2 9.38 5.10 29.11 1.48 57.88
Objects 3 15.42 3.05 57.62 2.52 33.96
---------------------------------------
12 Mean value: 11.58 3.37 55.70 2.00 45.92
Sigma: 3.34 1.60 25.68 0.74 16.92
10 Cl Sigma mean: 1.93 0.92 14.83 0.43 9.77
Ag
C O Si Cl Ag
8

0
1 2 3 4 5 6 7 8 9 10
keV

Figure 3: Scanning electron microscopy (a) and Energy dispersive X-ray spectrometer image of AgNPs
produced from A. diversifolia (b)

followed by peaks of silicon (55.70%) and carbon (11.58%) atoms, that suggested the interaction of
biomolecules and AgNPS which might have come from the plant leaf extract [2]. In this sense, the
reduction studies in other plants have reported the participation of carbonyl, phenolic and flavonoids
in the stabilization of NPs [10,11]. The results suggested that the biomolecules in leaves extract may
be responsible for the reduction of AgNO3 and stabilization of nanoparticles. Alegria et al. [13] reported
JRM, 2020, vol.XX, no.XX 5

that presence of phenolic compounds from tea extracts may play an important role in the reduction and
stability of AgNPs.
In this sense, total phenols and flavonoids present in A. diversifolia could be considered as an important
reducing and stabilizing agent for AgNPs production [14]. Similar results were observed in Sargassun
vulgare and Yucca schidigera after the applications of silver to aqueous extract of leaves [11,15].
Therefore, experiments about role of metabolites in AgNPs synthesis from A. diversifolia will be needed
to know the exact mechanism of their formation. Some studies reported that the negative surface charge
of AgNPs could be due to the adsorption of bioactive components present in the aqueous extract onto the
nanoparticles surface [2]. Similar results were found by Salvioni et al. [16] who showed that the negative
surface charge could be attributed to the interaction of metabolites with the NPs.

3.3 DLS and Zeta Potential

The DLS analyses showed a major particle size distribution peak at 34 nm and a second peak at 134 nm,
which represented the existence of interaction between Ag ions and biomolecules from A. diversifolia and
their aggregation (Fig. 4). On the other hand, zeta potential was found to be –20.2 mV for synthesized
AgNPs indicating stability and tendency to form short particles. The average particle diameter determined
by SEM was found to be 45–58 nm and 34–134 nm by DLS, this difference is according to reported by
Ruiz-Romero et al. [15] who observed that hydrodynamic diameter determined by DLS was smaller than
the SEM diameter.

Figure 4: Particle size distribution of AgNPs from dynamic light scattering measurements

3.4 Antibacterial Activities of AgNPs

The results showed that different concentrations of AgNPs were significantly more effective against
Klebsiella pneumoniae, and Enterobacter aerogenes (Gram negative microorganisms) compared with the
positive control (Tab. 1). The mean growth inhibition zone diameters for K. pneumoniae with 25%, 50%,
75% and 100% of AgNPs were 10.5, 11.1, 11.5 and 11.5 mm, respectively; these diameters for E.
aerogenes were 11.4, 11.0, 12.0 and 11.5 mm, respectively, while for the positive control group was 9.5
and 8.5 mm. Although the antimicrobial activity of AgNPs started at 25% for both microorganisms, there
was not an increase in the inhibitory effect on both bacterial species with an increase in the concentration
of AgNPs (Tab. 1 and Fig. 5).
In contrast, the results showed that means of growth inhibition for all the concentrations of AgNPs were
less than those in the positive control group in B. cereus (p < 0.05). In diverse studies, the AgNPs have
demonstrated their broad spectra of inhibition against Gram-positive and Gram-negative bacteria [17].
Kędziora et al. [18] suggest that positive particle surface charge is essential to increase the antibacterial
efficacy. However, this effect contrasted with our results, which showed a significantly inhibitory effect of
AgNPs against Gram negative microorganism but not with Gram positive with respect to positive control
6 JRM, 2020, vol.XX, no.XX

Table 1: Inhibition of microorganisms by AgNPs from A. diversifolia

Zone of inhibition (mm)
Microorganisms AgNPs from A. diversifolia A. diversifolia AgNO3
25% 50% 75% 100% 100% 10 mM
a a a a
Bacillus cereus 8.5 ± 0.07 9 ± 0.24 9 ± 0.07 9 ± 0.06 0 9.2 ± 0.54a
Klebsiella pneumoniae 10.5 ± 0.05b 11 ± 0.10b 11.5 ± 0.05b 11.5 ± 0.07b 0 8.5 ± 0.12a
c
Enterobacter Aerogenes 11 ± 0.35 11 ± 0.24b 12.0 ± 0.42c 11.5 ± 0.15b 0 9.5 ± 0.36a
Results are expressed as mean ± standard deviation of values from triplicate experiments. Values with the same letter (a, b or c) within each line are
equal according to the Tukey test at p ≤ 0.05.

Figure 5: Inhibition of microorganisms by AgNPs from A. diversifolia: (a) microorganisms with different
doses of Ag-NPs; (b) microorganism with A. diversifolia extract and control negative (water) and positive (10
mM AgNO3)

(AgNO3) (Fig. 5). In the present study, dose dependent effect of AgNPs on the inhibition of bacteria was not
observed. In this sense, Achaira et al. [18] reveled that bacterial sensitivity to AgNPs was found to vary
depending on microbial species and emphasized the dependence on morphology and distribution with
reactive faces of the AgNPs for antibacterial activity. These authors reported that dose dependent effect of
AgNPs on the Gram-positive and Gram-negative bacteria on the basis of disc diffusion method,
suggested, that at low concentrations of NPs, the interaction of particles with the cell wall of bacteria
decreases, while at the high concentrations, aggregation probability of the particle increases causes less
interactions with bacteria and NPs. On other hand, Bankier et al. [20] compared effects of multiple
metallic nanoparticles against Staphylococcus aureus and Pseudomonas. aeruginosa. They concluded that
the inhibitory effect of nanoparticles could be due to a difference in cell wall structure between the two
pathogens and factors of nanoparticle, such as size, shape and charge. Although this study revealed that
AgNPs are a good antibacterial candidate. The variation in antimicrobial activity of AgNPs of plants
JRM, 2020, vol.XX, no.XX 7

extract obtain in different investigation may be attributed to their metabolites present in the plants as well as
microorganism strains used and synthesis of NPs [2,10]. Therefore studies are needed to confirm the potential
antimicrobial of different doses of AgNP from A. diversifolia in Gram negative and Gram positive bacteria.
Salvioni et al. [16] show that AgNPs with a 20 nm diameter and a negative zeta potential have a high
antibacterial activity in Gram negative bacteria compared to colloidal silver. In this sense, the phenolic
compounds could act as capping agents of NPs and this may affect the growth, considering the
divergence in basic structural design of cell walls between the bacterial groups. In this sense, the effect of
phenolic compounds could be explained by adsorption to cell membranes, interaction with enzymes,
substrate and metal ion deprivation [21,22]. As shown in Tab. 2, a significant difference was observed
among the respective values obtained. The total phenolic content was significantly different (p < 0.05)
among aqueous extract and AgNPs from A. diversifolia. As shown in the case of total phenolics, the
concentration of flavonoids in the extracts and AgNPs from A. diversifolia was significantly different. In
this case, the AgNPs from A. diversifolia similarly showed a higher (p < 0.05) flavonoid content than the
aqueous extracts (Tab. 2).

Table 2: Total phenolic and flavonoid content in extract and AgNPs from A. diversifolia
Polyphenols Leaf extract-A. diversifolia AgNPs from A. diversifolia
(mg GAE/g) (mg QE/g)
Total Phenolics 27 ± 0.05a 31 ± 0.04b
Total Flavonoids 0.26 ± 0.12a 3 ± 0.06b
Results are expressed as mean ± standard deviation of values from triplicate experiments. Values with the same letter (a or b) within each line are equal
according to the Tukey test at p ≤ 0.05.

Then, the differences in the inhibition of microorganisms by AgNPs and A. diversifolia extract may be
results of a major concentration of phenolic compounds in AgNPs with respect to only A. diversifolia extract.
Therefore, the increasing content of polyphenols after the reaction can be attributed to organic complexes
present in the extract and not involved in the Folin–Ciocalteu reaction [13,23].

4 Conclusion
In the present study, our results showed the capacity of aqueous extract of Annona diversifolia as
efficient and environment-friendly reducing agent in the synthesis of AgNPs. Characterization of green
AgNPs revealed that the particles were spheroidal in shape with a particle size distribution range of 45–
58 nm along with 45.92% silver content. These findings revealed that green AgNPs exhibited a
significantly inhibitory effect against Gram negative but not with Gram positive bacteria. These results
suggest that green AgNPs could be used for antibacterial treatment of vegetables. Although, future
studies are necessary to reveal the exact mechanism of toxicity of green silver nanoparticles in Gram
negative bacteria.
Conflicts of Interest: The authors declare that they have no known competing financial interests or personal
relationships that could have appeared to influence the work reported in this study
Funding Statement: This research was funded by Autonomous University of Baja California and National
Technological Institute of Mexico. Tuxtla-Gutierrez Technological Institute.
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