Green Synthesis of Ag Nanoparticles from
Aqueous Extracts of Leaves and Fruit of Casuarina equisetifolia against Candida albicans and other
Clinical Isolates
Mahmoud Moustafa1,2*,
Ahmed Al-Emam3,4, Mahmoud Sayed5,6, Saad Alamri1,7,
Huda Alghamdii1, Ali Shati1, Sulaiman Alrumman1,
Mohamed Al-Kahtani1, Eman Khalaf8, Thanaa Maghraby2
and Hanan Temerk2
1Department of Biology, College of Science, King Khalid University,
9004, Abha, Kingdom of Saudi Arabia
2Department of Botany and Microbiology, Faculty of Science, South Valley
University, Qena, Egypt
3Department of Pathology, College of Medicine, King
Khalid University, Abha, Saudi Arabia
4Department of Forensic Medicine and Clinical Toxicology, Faculty of
Medicine, Mansoura, University, Mansoura, Egypt
5Physics Dep., Faculty of Science, King Khalid University, P. O. Box
9004, Abha, Saudi Arabia
6Physics Department, Faculty of Science, Al-Azhar University, P. O.
71452, Assiut, Egypt
7Prince Sultan Bin Abdulaziz Center for Environmental and Tourism
Research and Studies –King Khalid University, Kingdom of Saudi Arabia
8Department of Microbiology and Immunology, Faculty of Pharmacy,
Damanhour University, Damanhour, Egypt
*For correspondence:
mfmostfa@kku.edu.sa; mfmostfa@kku.edu
Received 10 August 2020; Accepted 09 September 2020;
Published 10 December 2020
Abstract
The prevalence of the infectious diseases caused by
Candida species and other human pathogenic microbes has led to the discovery of
some natural agents against multidrug resistant microbes. Therefore, this
research was designated to determine the capability of synthesized
nanoparticles (NPs) from aqueous extract of leaves and fruits of Casuarina
equisetifolia as anticandidal and antibacterial against some microbes.
Silver NPs (AgNPs) were successfully gained from aqueous leaves and fruit
extracts of C. equisetifolia which is defined on the basis of UV–visible
spectroscopy, X-ray diffraction analysis and scanning electron microscope. The
results showed that leaves and fruits extracts of C. equisetifolia acts
as an excellent capping agent. XRD based on the FWHM analysis showed that AgCl
and Ag had an average NPs size of 90.97 nm and 71.28 nm, respectively for
fruits and 15.33 nm and 14.01 nm, respectively for leaves. UV–visible spectroscopy showed a maximum absorbance at
442 nm for fruits and 433
nm for leaves. SEM showed that the size of NPs from leaves lied in
between of (30 to180 nm) and for fruits (70 to 250 nm). Candida albicans
was severely affected by NPs of leaves with inhibition zone (3.03± 1.61 cm) and
NPs of fruits had (1.37± 0.15 cm) inhibition zone. Nanoparticles from leaves
exhibited maximum activity against P. mirabilis (3.52± 0.13 cm) and low
activities against M. luteus (1.50±0.18 cm) inhibition zones. In
conclusion, these eco-friendly synthesized AgNPs from leaves and fruits of C.
equisetifolia could be used as competitive alternative natural drugs than
conventional synthetic chemicals. © 2021 Friends Science Publishers
Keywords: Casuarina equisetifolia; AgNPs; Anticandidal; Antibacterial; Aqueous extracts
Introduction
The construction of functional molecule
at micro level is of great interest for nanotechnology techniques.
Nanomaterials (NPS) are used extensively in the area of medicine for the
purpose of drug delivery, diagnosis, treatment of cardiovascular disorders,
wound healing and production of antimicrobial agents. They exhibit unique
physico-chemical properties, which are not observed in either single molecules
or bulk metals itself (Dauthal and Mukhopadhyay
2016). They are used for multiple purposes for industrial and in
medicinal applications (Thakkar et al. 2010; Linic et al. 2015). Silver nanoparticles (AgNPs) were more
concerned than other metallic nanoparticles (MNPs) because of their special
properties such as magnetic, optical polarization, electrical conductivity (EC)
and prominent antimicrobial activity (Evanoff and
Chumanov 2005). Considering the presence of various metals in nature,
only some of them, such as silver, gold, palladium and platinum, are
extensively synthesized in nanostructured form (Yoon et al. 2010; Yang et al. 2017). Three different methods of synthesis for NPs
developed are chemical, physical and green synthesis (Oves et al. 2018; Saratale et al. 2018).
Physical
methods require expensive equipment, high temperature and high pressure. For
the synthesis of nanoparticles using chemical processes, harmful substances are
used, which can cause significant harm to the atmosphere and to living
organisms. Due to these disadvantages, the use of chemical and physical methods
is limited and gradually is replaced by green synthesis, which is a more environmentally
friendly and cheaper method. Green synthesis in all process is similar to
chemical reduction where costly chemical reducing agent is substituted by a
natural product extract, such as leaves, root or fruits are applied for NPs
synthesis of metal or metal oxide (Hussain et al. 2016). Natural product
NPs are considered to be environmental friendly and safe (Jayaseelan et
al. 2012; Gopinath et al. 2014),
free from environmental pollution (Chandran et al. 2006; Huang et al. 2007), cheaper (Mittal et al. 2013) and ideal for mass
manufacturing (Iravani 2011). In
addition, biologic development of NPs makes it possible to recycle expensive
metal salts such as silver and gold contained in waste streams (Wang et al.
2009).
Plants,
bacteria, fungi, algae, etc. are commonly used for green nanoparticle synthesis
(Chen et
al. 2015; Khan et al. 2016;
Agarwal et al. 2017). The
ability of pathogenic candida and bacteria to resist against various drugs is a
major obstacle in medical practice that restricts the effectiveness of such
normal medications (Quelemes et al. 2013). Such disadvantages give researchers enormous
opportunities to create new substances, such as AgNPs, to counter such problem.
Casuarina
equisetifolia L. is predominantly a monoecious
species belonging to the Casuarinaceae family (Binggeli et al. 1999). It is planted as
ornamental in the street side or as a fence around house or may be growing
wildly in abandoned area. It is found in many climatic regime, usually grow
near sea level but succeeding under cultivation at heights up to 1,400 meters
and can grow under saline environments (Jensen
1995; Garrity et al. 2006).
The plant contains several phytochemical components such as glycosides,
quercetin, triterpenoids, tannins, rutin and casuarine, catechol derivatives etc. (Ramanathan et al. 2012). The existence of
natural secondary metabolites shows the tree species as important source for
use as an astringent, diuretic agent for coughing, diarrhea, beri-beri, colic
and as toothache. Biological properties such as hypoglycemic anticancer
activity of this tree species have been characterized (Han 1998; Parekh et al. 2006).
Candidiasis is caused by various
Candida species and considered as one of the most prevalent fungal
infections to humans, especially by C. albicans. There are no reports
till date about the biosynthesis of (AgNPs) by applying aqueous extract of leaf
and fruit of the Casuarinaceae family. Herein, an effort
has been made to examine NPs from leaf and fruit extract of the C.
equisetifolia against C. albicans isolates and against a
range of human pathogenic microbes as potential drugs for pharmaceutical
application. Also, in the present study NPs from leaf and fruits had been
characterized using various techniques. This research was based on a rather
simple hypothesis that plant aqueous extracts contain a group of polar
compounds rather than secondary metabolites. Thus, depending on that fact,
simple preparation of AgNPs from leaves and fruits of C. equisetifolia
have been relaying on water extraction.
Materials and Methods
Collection of plant materials
Leaves and fruits samples of C.
equisetifolia were collected from Abha region, KSA during the month of May
in 2019 (Latitude: 18.2114609; Longitude: 42.4999752). The obtained materials
were thoroughly rinsed in flowing tap water to remove adhesive particles, and
then with distilled water until no traces of foreign material remained.
Preparation of plant extract
A 30 g of fresh leaves and fruits of C.
equisetifolia was crushed thoroughly with a blender (Philips, Germany) to a
homogeneous mass with the addition of 30 mL of DW (1 g/mL). Then extract was
filtered using Whatman No 1 filter paper, and the supernatant was collected and
stored at 4°C for further analysis.
Synthesis of silver nanoparticle
Silver nitrate reagent (0.5 mM) was made using
deionized water, to synthesis silver nanoparticle from leaves and fruits
extract of C. equisetifolia. Ten mL from each was added to 90 mL of 0.5
mM AgNO3 (Saranya and Gowrie
2016). The mixture was heated at 70°C for 3 min. The reduction of
aqueous silver ions by both extract to form stable AgNPs was noted with the
formation of yellow, brown and then blackish colored solution (Kirthika et al.
2014).
Characterization of silver
nanoparticles
UV-Vis Spectrophotometer: Reduction of Ag+
ions was spectrophometrically monitored using double-beam UV-Vis spectroscopy
(Hitachi, U-3010) by dissolving a small aliquot of the reaction solution into
distilled water. The wavelength of 350–500 nm was measured and the peak was
recorded.
Powder X-ray Diffraction (XRD): Powdered
silver nanoparticles were mounted on a microscopic slide and air dried at 24°C
overnight. The crystalline form, phase detection and grain size using XRD
(Shimadzu, 6000 Diffractometer, Japan) were achieved.
Scanning electron microscope
(SEM): The AgNPs morphology images from leaves and fruits extracts from C.
equisetifolia were studied via SEM (JSM-7500 F; JOEL-Japan). Some drops
from the sample colloidal solution were dried at 60°C in a high stability
furnace on microscopic sheet and then observed.
Anticandidal and antibacterial
activities
In vitro antimicrobial behavior of processed silver
nanoparticles using leaves and fruit extracts of C. equisetifolia was
investigated. Candida albicans and other
six human pathogens viz., Proteus
mirabilis, Psedomonas aeruginosa,
Staphylococcus aureus, Shigella flexneri, Klebsiella pneumoniae and Micrococcus luteus were used for anticandidal and
antibacterial studies, which were obtained from the Department of
Microbiology, King Khalid University, Saudi Arabia. These microbes were grown
in nutrient broth for 48 h. Agar well diffusion method was used to screen the
antibacterial and anticandidal activities of NPs gained from aqueous extract of
leaves and fruits of C. equisetifolia (Daoud et al. 2019). Potato Dextrose
Agar and nutrient agar media were prepared for C. albicans and for bacterial strains respectively and from each 20
mL were poured into sterilized Petri dish. Upon solidification, 1 mL from fresh
candida and bacterial culture was pipetted in the center of sterile Petri dish
and swapped uniformly upon the surface of solid media using Sterile Cotton
swabs. In each plate two wells were punctured by autoclaved cork borer (6 mm in
diameter) into agar plates containing inoculums. Then 100 μL AgNPs
of each extract was applied to the respective well. Plates were refrigerated
for 30 min to allow the extracts to spread well into the agar. The plates were
then incubated at 37°C for 48 h. Anticandidal and
antibacterial activities were detected by measuring the inhibition zone
(including the well diameter) that occurred during the incubation period. DMSO
at a concentration of 10% was employed as a negative control and Cefoxitin (30
mcg) disc was used as positive control. Each plate was examined after
incubation and the diameters of the inhibition zone were determined using the
millimeter ruler. A region of inhibition of about 9 mm or more around the holes
was defined that the extracts have antimicrobial substance (Alamri and Moustafa 2012). All experiment was
performed in three replicates.
Statistical analysis
Results were subjected to one-way analysis of variance
(ANOVA) followed by Least Significant Difference (LSD) Post Hoc test of three replicates ± standard deviation (SD).
Differences between means in relation to positive control were considered
significant at p-value < 0.05.
Results
Antimicrobial activity
The antimicrobial activity behavior of the
biosynthesized AgNPs is shown in Fig. 1. There was remarkable inhibition
activity of AgNPs against C. albicans, Gram-positive and Gram-negative
bacteria. The maximum inhibitory effects of AgNPs were
observed against all tested microbial strains
Fig. 1: AgNPs anticandidal and antibacterial
activities from leaves and
fruits of C. equisetifolia aqueous extracts against C. albican,
P. aeruginosa,
K. pneumoniae,
S. flexneri, P. mirabilis, S. aureus and M. luteus.
PC, positive control. Significant differences (*P ≤ 0.05; **P
≤ 0.01), between treatments in relation to PC ± SD of the mean for n
= 3
when prepared
from C. equisetifolia leaf extract. While AgNPs from fruits extract of C.
equisetifolia showed low antimicrobial activities against all tested
microbial strains. For C. albicans the zone of inhibition from AgNPs of
aqueous fruits was (1.37±0.15cm). With an inhibition zone between 1.5–1.35 cm,
it was considered that all the tested strains were susceptible to AgNPs from
fruits extract of C. equisetifolia, which implied that the extract have
antimicrobial properties (Nascimento et al. 2000; Alamri and Moustafa 2012).
NPs of aqueous fruits extract showed maximum antibacterial activities against M.
luteus, followed by P. aeruginosa and moderate activity against S.
aureus, P. mirabilis, K. pneumoniae and S. flexneri (Fig. 1). AgNPs from aqueous
leaves extract of C. equisetifolia showed potent antimicrobial
activities against all tested microbial strains more than fruits extract
between 61.06 and 52.97%. C. albicans was severely affected by AgNPs
leaves extract with a zone of inhibition of 3.03±1.61 cm. AgNPs of aqueous
leaves showed maximum antibacterial activities against P. mirabilis (3.52±0.13
cm), followed by K. pneumoniae (3.24±0.06
cm) and M. luteus (3.40±0.14
cm). S. flexneri, P. aeruginosa and S. aureus demonstrated susceptibility in the range
between (3.27±0.11 cm and 3.03±0.21 cm with AgNPs from leaves extract. The
percentage susceptibility differences among various bacterial strains between
AgNPs of leaves and fruits extracts was; P. mirabilis > S. aureus
> S. flexneri > K. pneumoniae > M. luteus > P. aeruginosa. C. albican was very sensitive to AgNPS
from leaves and fruits extract as the maximum differences between them was
found to be 61.06%. DMSO showed no antimicrobial activities against all tested
microbes while positive control inhibited microbial growth in the range between
3.10 and 2.55 cm increased as compared to AgNPs of fruits extract which was 3.1
to 1.93%. Efficacy of AgNPs from leaves extract was higher than positive
control by 39.96% against P. mirabilis to 15.48% against P. aeruginosa.
Remarkable differences were also found
against C. albicans by AgNPs of leaves extract of C. equisetifolia being more
than positive control (Fig. 1).
Fig. 2: X-ray diffraction pattern of AgNPs from C.
equisetifolia aqueous leaves extract (CEALE) and aqueous fruits extract
(CEAFE)
Fig.
3: The UV/Vis
absorption spectra of AgNPs from C. equisetifolia aqueous leaves extract
(CEALE) and aqueous fruits extract (CEAFE)
NPs characterizations using XRD
Fig. 2 shows
the XRD pattern of NPs from C. equisetifolia leaves aqueous extract
(CELAE) and fruits aqueous extract (CEAFE).
There was similarity to some extent between the positions of the diffraction
peaks for both patterns. For CEAFE, the
diffraction peaks were found at 2-theta values at 38.20˚ (111),
44.40˚ (200), and 64.55˚ (220), corresponded to the crystal
Table 1: Experimental diffraction angles, FHWM, d-spacing,
diffraction planes and particles size of silver (Ag) and silver chloride (AgCl)
extracted by aqueous extracts from fruits (CEAFE) and leaves (CEALE) of C.
equisetifolia
Sample |
Crystalline
phases |
Diffraction
angle (degree) |
FHWM
in radians |
Lambda
(nm) |
d-spacing
(nm) |
Diffraction
plane |
Particle
size (nm) |
CEAFE |
AgCl |
38.20 |
0.001587 |
0.154 |
0.275 |
(200) |
90.97 |
Ag |
32.49 |
0.002058 |
- |
0.235 |
(111) |
71.28 |
|
CEALE |
AgCl |
32.37 |
0.00942 |
0.154 |
0.276 |
(200) |
15.33 |
Ag |
38.08 |
0.010467 |
- |
0.236 |
(111) |
14.01 |
Fig.
4: SEM of AgNPs from C. equisetifolia aqueous
leaves extract (CEALE) and aqueous fruits extract (CEAFE)
planes of the
face-centered cubic(fcc) Ag (JCPDS card No. 04-0783); whilst, five additional
diffraction peaks appearing at 2-theta values of 27.78˚ (111), 32.49˚
(200), 46.37˚ (220), 54.47˚ (311), 57.31˚ (222) and 67.10˚
(400) correspond to the crystal planes of the face-centered cubic (fcc) AgCl
(JCPDS file:31-1238). Similarly, for CELAE extraction,
the diffraction peaks at 2-theta values at 38.08˚ (111), 43.93˚
(200), and 64.74˚ (220), correspond to the crystal planes of the
face-centered cubic(fcc) Ag (JCPDS card No. 04-0783); but, five additional
diffraction peaks appearing at 2-theta values of 27.81˚ (111), 32.37˚
(200), 46.41˚ (220), 55.10˚ (311), 57.96˚ (222) and 67.22˚
(400) correspond to the crystal planes of the face-centered cubic(fcc) AgCl
(JCPDS file:31-1238). These data confirmed that Ag/AgCl nanoparticles are
synthesized via both extraction of plant. Other peaks occured in the XRD
pattern that could be due to the crystallization of bio-organic particles on
the surface of the AgNPs. Furthermore, the average crystal size (Table 1) was
determined by the Debye-Scherrer formula: 𝐷=(0.9 𝜆)/(𝛽cos𝜃), where D is the average size of the crystals, 𝜆 is the wavelength of radiation, 𝛽 is the full width at half the maximum height (FWHM) and
𝜃 is the position of the maximum diffraction peak. Based
on the FWHM of the diffraction peak (200) of the AgCl crystals and (111) the
diffraction peak of the Ag crystals, the AgCl and Ag average nanoparticle size
was determined and found as 90.97 and 71.28 nm, respectively for CEAFE, whereas D was reduced to 15.33 and 14.01
nm for CELAE.
UV-vis spectrophotometer and SEM analysis
In the
present study, the solution of AgNO3 was immediately turned into
blackish after the addition of C. equisetifolia leaves and fruit extract
as reducing agents in all samples showing the formation of AgNPs. Fig. 3 shows
the typical UV spectra of the reaction solution with a localized surface
plasmon resonance (SPR) of about 442 and 433 nm for AgNPs synthesized using
extract of (CEAFE) and (CEALE), respectively, which strongly indicated
the formation of AgNPs. Moreover, there was SPR semi-flat peak, which resulted
from the presence of Ag/AgCl NPs.
Discussion
Based on
gained NPs antimicrobial analyses against tested microbes, it was noticed that
the mode of action included bactericidal effect against bacterial strains and
candidcidal against C. albicans of AgNPs were most
possibly due to the binding of AgNPs to the cell wall and the production of
free radicals (Pirtarighat et al. 2019). Our explanation why NPs prepared from leaves
more potent than fruits this probably due to leaves have more chemicals than
fruits. In addition, it was reported that AgNPs could disrupt the permeability
of the membrane by entering the cell membrane and inducing intracellular ATP
leakage and finally causing the cell death (Hajipour et al. 2012; Ajitha et al. 2014). Positively charged ions from Ag+
seem to have a strong tendency to act with phosphorus and sulfur in
biomolecules such as DNA and RNA, so that such attachment of small NPs from C.
equisetifolia leaves leads to the interruption of the roles of DNA and RNA
in the cell (Hajipour et al. 2012).
It has been
reported that the smaller the particle size of the AgNPs, the more microbial
cell damage will occur, due to oxidative stress response due to reactive oxygen
species (ROS). Again, ROS caused DNA damage, and the rupture of the cell
membrane of the microbial strains. In agreement with our findings that
nanoparticles have a greater surface area available for contact that improves
the bactericidal and candidcidal effect than large particles (Raffi et al.
2008). Previous works showed that various NPs from plant extracts had
promising candidcidal effect as Zn nanoparticles combined with fluconazole
could inhibit the vaginal candidiasis (Nazari
2020).
As the
particles size increase, the position of the absorption peak is shifted to the
long wave, and the larger the particle size, the more visible the phenomenon of
red transformation. By altering extraction using C. equisetifolia
aqueous leaves extract to aqueous fruits resulting
in a blue shift from the SPR range from 442 to 434 nm implied that smaller NPs
were found there. Small AgNPs may be due to higher nucleation rate with the
improved reduction process which supports more potent antimicrobial activities (Khan et al.
2013; Dong et al. 2019).
Agglomeration
of AgNPs in the form of nanoclusters may be due to the effect of plant extract
during sample preparation for SEM. Again, this supports the view that tiny size
of nanoparticles may assist in easy penetration of microbial cell wall and
destroy various organelles. Biosynthesized small NPs have been identified as
being able to inhibit/destroy microbial cells (Singh et al. 2019). In agreement with
previous experimental results (Saranya and
Gowrie 2016), this study suggested that the application of AgNPs
synthesized from leaves and fruits aqueous extract of C. equisetifolia,
could be used as an effective antimicrobial agent.
Conclusion
Using aqueous extract of C.
equisetifolia yielded stable AgNPs as confirmed by UV–Vis, XRD and SEM
techniques. Overall, AgNPs from aqueous leaves and fruits extracts from C.
equisetifolia possessed antibacterial and
anticandidal activities as they could inhibit the growth of
selected C. albicans and
bacterial strains. AgNPs from leaves of C. equisetifolia had more
potent antimicrobial activity than fruits which may be used as natural agent to
control the growth of many pathogenic
microbes. More research is needed to characterize NPs from C.
equisetifolia in order to find better antimicrobial activity.
Acknowledgments
The authors thank the Deanship of
Scientific Research at King Khalid University for funding this work through
Grant No. R.G.P.1/134/40
Author Contributions
MM, MS, EK, TM and HT planned and doing
the experimental works, AA and HA interpreted the results and MM, MS, MA, EK,
TM, SA, SUA, AS made the write up, analyzed the data and edited the review.
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