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Green Synthesis and Biological Activities of Gold Nanoparticles Functionalized with Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis.

Byline: Nazar Ul Islam, Fahim Ahsan, Ikhtiar Khan, Muhammad Raza Shah, Muhammad Shahid and Muhammad Atif Khan


In the present study, gold nanoparticles (GNPs) were prepared at boiling temperature (90-95oC) by treating gold ions with Citrus fruit extracts. The effect of mixing ratios of the reactants and concentration of gold hydrochloride was studied. In the standardization process, 10-3 M solution of HAuCl4.3H2O was reacted with fruit extracts for half an hour at 90-95oC in different ratios. GNPs were characterized by UV-Vis spectroscopy (UV-Vis) and atomic force microscopy (AFM). Their stability was evaluated against varying pH solutions and volumes of sodium chloride along with metals and antibiotics sensing ability. The gold nanoparticles were tested for antibacterial and antifungal activities against various pathogenic strains. The UV-Vis spectra of gold nanoparticles gave surface plasmon resonance at about 540 nm while the AFM images revealed the particle size within the range of 70-100 nm.

GNPs showed remarkable stability in varying pH solutions and salt volumes as well as high detection ability towards cobalt, copper, ceftriaxone and penicillin. Moreover, the GNPs possessed moderate antibacterial and good antifungal activity. These results concluded that the Citrus fruit extracts can be utilized for large scale synthesis of cost-effective nanoparticles which may have compatibility for biomedical and pharmaceutical applications.

Key words: Gold nanoparticles, Citrus reticulata, Citrus aurantium, Citrus sinensis, Citrus grandis, Biological activities.


Advancement in nanotechnology has led to extensive development of nano-size materials which find important applications in different areas [1-2]. Noble metal nanoparticles especially those of copper, gold and silver have shown promising applications in various fields like medicine [3-5], photography [6], biological labeling [7], photonics [8], catalysis [9] and optoelectronics [10]. The importance of these nanoparticles is due to the occurrence of broad extinction bands in the visible region of the electromagnetic spectrum [11]. Their solutions have very intense colors as compared to their bulk material and individual atoms [12]. Due to distinctive and fascinating properties, gold nanoparticles are considered as the most stable metal nanoparticles [13]. Their optical properties and intense electromagnetic fields make these nanoparticles very attractive for sensing, diagnostics, and photothermal therapeutic applications among other important areas [14].

Nanoparticles have been synthesized and stabilized by a number of physical and chemical processes [15-17]. Most of these techniques are costly and often involve the use of synthetic organic compounds such as sodium borohydride [18], hydroxylamine [19] and triethyl amine [20] which have been investigated to harmfully effect the environment [21-23]. The use of these hazardous reagents has detrimental effect as the presence of even trace quantities of these residual chemicals will limit the applications of gold nanoparticles especially in the medical field [24-26]. Therefore, there is an increase demand for green synthesis of nanoparticles which signify the importance of environment friendly and bio-inspired methods [27]. From a green chemistry perspective, the main steps in the preparation of nanoparticles include the choice of the solvent medium, reducing agent and a stabilizing agent for nanoparticles [28].

Green synthesis of nanoparticles including the use of plant extracts has received great attention as alternative to the physical and chemical methods [29]. Several plants have been successfully employed for efficient and rapid synthesis of silver and gold nanoparticles [30]. The genus Citrus of the family Rutaceae which includes Indian wild orange (Citrus indica), Melanesian papeda (Citrus macroptera), bitter orange (Citrus aurantium), shaddock (Citrus grandis), Mandarin orange (Citrus reticulata), sweet orange (Citrus sinensis), lemon (Citrus limon) and grapefruit (Citrus paradise) are distributed throughout the tropical and temperate regions and are widely consumed as fresh fruits [31]. The major chemical constituents reported in Citrus fruits are flavonoids including hesperitin, hesperidin, neohesperidin, naringenin, tangeritin, auranetin, quercetin, nobiletin [32], limonene, myrcene [33], AY- sitosterol [34] and adrenergic amines including synephrine, octopamine and tyramine [35].

Citrus fruit extracts and their active constituents are widely studied for their anti-obesity [36-37], antifungal [31, 38], antibacterial [39], antiviral [40], anxiolytic and sedative [33, 41], antioxidant [34, 42], anti-diabetic [43-44], anti-allergic [45], anti-inflammatory [46], anticancer [47], antihypertensive and diuretic [48- 49], anti-hypercholesterolemic [50], platelet anti- aggregation and anti-adhesive [51] activities. Different species of Citrus including Citrus unshiu [52], Citrus limon [53-55], Citrus sinensis [56-57] and Citrus reticulata [58] are being successfully used for efficient synthesis of gold and/or silver nanoparticles.

In this report gold nanoparticles (GNPs) were prepared through green route by the reduction of gold ions with fruit extracts of Citrus reticulata L., Citrus aurantium L., Citrus sinensis L., and Citrus grandis L. The biosynthesized GNPs were characterized with UV-Visible spectroscopy (UV- Vis) and atomic force microscopy (AFM). The effect of pH and salt on stability of GNPs was studied and their sensing ability towards different metals and antibiotics was evaluated. Moreover, the GNPs were investigated for antibacterial and antifungal activities against different clinically important pathogenic microbial strains.



All chemicals and reagents used in this study were of analytical grade. Hydrogen tetrachloroaurate (III) trihydrate (HAuCl4.3H2O: 99.9%); obtained from Merck was used as a source of AuIII ions for the synthesis of GNPs. Fresh Citrus fruits including Citrus reticulata, Citrus aurantium, Citrus sinensis, Citrus grandis were purchased from the local markets of Peshawar, Pakistan. The fruits were squeezed and the obtained extracts were passed through a fine pore mesh and then filtered to remove large particles. The filtered juice was centrifuged at 10,000 rpm for 10 min to remove any undesired impurities. For sensing applications, lead acetate, nickel chloride, cobalt chloride, copper sulphate and iron sulphate were purchased from Merk, while ceftriaxone, cefuroxime, cephradine and penicillin were obtained from local pharmaceutical industries.

Synthesis of Gold Nanoparticles

An aqueous solution of 10-3 M HAuCl4.3H2O was prepared. Accurately measured 5 ml of gold hydrochloride solution was taken in a reaction flask and heated at 90-95oC on a hot plate with stirring for 10 minutes. 1 ml of each Citrus extract was added and the solution was heated for few minutes. The reaction mixture was then transferred to a vial and stirred on a magnetic stirrer for additional 4 hours. Gold chloride solution and Citrus fruit extracts were mixed in different ratios. The absorption peaks for all the ratios were observed in the range of 530-540 nm. The ratio that gave the best absorption peak for each Citrus extract was then prepared in bulk and used for further studies. The bioreduction of AuCl4- ions was monitored by UV- Vis spectra of solution in 10 mm optical path length quartz cuvettes with a UV-Vis spectrophotometer (Hitachi U-3200, Japan). The size of GNPs was characterized by atomic force microscope (Agilent Technologies 5500, USA).

Stability and Sensing Ability of Gold Nanoparticles

The stability of nanoparticles was checked by measuring the UV-Vis spectra at varying pH values and different volumes of NaCl. For the effect of pH on the stability of GNPs, the nanoparticles solutions of different Citrus fruits were taken in vials and pH was adjusted to different values (2-3, 4-5, 6- 7, 8-9, 10-11, 12-13) by drop wise addition of 1 M HCl or NaOH solutions. These were kept for some time and their absorption were recorded.

The effect of NaCl on the stability of GNPs was checked by preparing 1 mM solution of NaCl in distilled water. Accurately measured 3 ml nanoparticles solutions of each extract were taken in vials. Different volumes of 1 mM NaCl solution were added to vials and kept for 1 hour to ensure thorough mixing of both solutions. Their UV-Vis spectra were then recorded.

The sensing ability of the biosynthesized GNPs towards different metals and antibiotics was investigated by reacting the nanoparticles with different volumes of 10-1 mM salt solutions of metals (lead, nickel, copper, cobalt, iron) and 10-1 mM solutions of antibiotics (cefatriaxone, cefuroxime, cephradine) respectively in vials. The effect was noted by recording their UV-Vis absorption spectra.

Antimicrobial Activities

The antibacterial and antifungal activities of GNPs functionalized with Citrus fruit extracts were evaluated by using the well diffusion method [59-60]. The activities were performed against bacterial strains of Klebsiella pneumonia, Bacillus subtilis and Staphylococcus aureus and fungal strains of Alternaria solani, Aspergillus niger and Aspergillus flavus. The bioassays were performed in triplicate.

Statistical Analysis

Data were expressed as mean SEM. Correlation analysis of detection ability towards metals and antibiotics was carried out using the Pearson's correlation and regression program in Minitab version 17.1.0 (Minitab Inc. State College, PA 16801 USA).

Results and Discussion

Characterization of Gold Nanoparticles

Nanoparticles formed by the reduction of gold ions were checked and monitored by measuring the UV-Vis absorption spectra after reaction of gold solution with Citrus fruit extracts in different ratios. The surface plasmon resonance of noble metal nanoparticles can be easily monitored with UV-Vis spectroscopy [61], which directly determines the size and concentration of gold nanoparticles [62]. In the first step, the volume of gold solution was kept constant while the volume of each Citrus extract was altered. Better results were obtained up to a certain ratio for different Citrus fruit extracts. In the next step, the volume of gold solution was increased but no significant changes were observed. The initial indication for the synthesis of GNPs was the sharp color change of the reaction mixture which was blue in the beginning but turned to purple and then to reddish with changing gold solution and Citrus extracts ratio as shown in the insets of Fig. 1.

Due to the collective oscillations of electrons in the conduction band that are excited by light of appropriate frequencies, the noble nanoparticles exhibit bright colors [63]. The UV-Vis spectra for the GNPs of Citrus fruit extracts are given in Fig. 1. The best peaks for Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis, were obtained at ratios of 5:3.5, 5:2, 9:1 and 7:1 gold-extract respectively. The sharpness of UV-Vis peak varies with the type of Citrus fruit. As shown in Fig. 2, the best peaks having the maximum absorbance for each Citrus fruit are drawn together for comparison. The intensity of the UV-Vis absorption spectra for the Citrus fruits decreased in the order of: Citrus grandis greater than Citrus aurantium greater than Citrus sinensis greater than Citrus reticulata.

Among the four Citrus fruits, the best nanoparticles appeared for Citrus sinensis which was also confirmed by its corresponding AFM image in which the particle size was in the range of 70-100 nm with well-dispersed, heterogeneously shaped gold nanoparticles as shown in Fig. 3. The peaks at other ratios of Citrus fruit extracts and gold solution are either having low intensity or showed significant peak broadening with red shift, which might be due to formation of greater number of large anisotropic GNPs. The UV absorption spectra of gold nanoparticles significantly depend on the sizes of GNPs and show a dramatic red shift with an increase in their diameter [64]. Particle size influences the position of surface plasmon band. Deviations from spherical geometry and an increase in diameter promote a red-shift. Moreover, inter-particle interactions can also play a fundamental role in the optical absorption of nanoparticles systems [65].

Sujitha and Kannan biosynthesized a mixture of gold nanoprisms and spheres by the reduction of aqueous gold chloride using Citrus limon, Citrus reticulata and Citrus sinensis. They reported that the possible reducing agent was citric acid whereas the proteins present in the Citrus fruit extracts efficiently cap the nanoparticles and are responsible for stabilization [58]. Furthermore, Prathna et al synthesized silver nanoparticles by treating silver ions with Citrus limon extract and found that the citric acid present in Citrus limon was the principal reducing and stabilizing agent [53]. The nanoparticles size, shape or configuration [66], their inter-particle distances and the surrounding media [67] are known to play an important role in determining the surface plasmon resonance sensitivity. However, further characterization studies like transmission electron microscopy or zetasizer are warranted to validate the formation and particle size analysis of GNPs of Citrus fruit extracts.

Stability of gold Nanoparticles

Since nanoparticles were synthesized by heating the reaction mixture to 90-950C, therefore these biosynthesized GNPs were considered as thermally stable. Heating favors the synthesis of nanoparticles. Without heating, nanoparticle synthesis was worse and the synthesized nanoparticles were unstable. The nanoparticles solutions were kept at room temperature and samples were withdrawn periodically and checked for stability by observing their respective UV-Vis absorption spectra. No change in the absorption spectra was observed, indicating the thermal stability of these nanoparticles. The synthesis of GNPs increases with increasing reaction temperature [68]. There is an inverse correlation between temperature i.e. kinetic energy, of a nanoparticle ensemble and the degree of aggregation [69].

Change in temperature of a reaction system greatly affect the reaction components capability in reduction, surfactant adsorption/desorption and complexing stability, the formation and growth rate and hence the shape, size, and size distributions [70].

From the UV-Vis absorption spectra it was observed that the GNPs of Citrus fruits were stable in varying pH solutions, however enhanced stability was observed at an acidic pH of 4-5 for Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis as shown in Fig. 4. Citrus aurantium also showed enhanced stability at pH 2-3. As the pH increased, a decrease in the peak intensity of the UV- Vis spectra was observed for all the Citrus fruits. Peak broadening and a red shift was observed at all the pH values for Citrus grandis. Citrus reticulata, Citrus aurantium and Citrus sinensis showed enhanced stability at pH 4-5. Citrus aurantium was also found stable at pH 2-3. A gradual decrease in the peak intensities for all the Citrus fruits was observed as the pH increased to 12-13. The reduction in peak intensity for each Citrus fruit GNPs with varying pH values might be due to an increase in the particle size resulting from agglomeration.

The UV-Vis spectra for the effect of pH on GNPs of Citrus grandis have broad peaks with red shift. Variation in the reaction pH greatly affects the size of nanoparticles rather than their shape. At pH of 3 and 4, more functional groups are available for higher number of Au(III) complexes to bind with the plant biomass and allows the subsequent formation of larger amounts of small diameter nanoparticles [71]. The influence of pH on nanoparticles depends on the dissociation equilibrium of complexing agent, the protonation of ionic groups and nanoparticles interfacial free energy [72].

The GNPs of Citrus fruit extracts were found stable at varying volumes of 1 mM NaCl solution. As the volume of adding NaCl was increased, a slight change in the peak intensity was observed. The UV-Vis spectra of Citrus aurantium showed a prominent change after addition of 200 L salt solution which was exhibited by a decrease in the sharpness of GNPs peak as compared to 200 L distilled water. The spectra of other Citrus fruits extract i.e. Citrus reticulata, Citrus sinensis and Citrus grandis remained unaffected at this volume. The UV-Vis spectra for the effect of NaCl on stability of Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis GNPs are shown in Fig. 5. No significant deviation in the UV-Vis spectral peaks of Citrus reticulata, Citrus sinensis and Citrus grandis was observed.

Furthermore, their peaks are centered at the surface plasmon resonance characteristic for GNPs, thus showing that increase volumes of NaCl solution have little effect on the overall stability of GNPs. Citrus aurantium, showed a decrease in peak intensity at 200 l. Gold nanoparticles that are capped strongly do not show any color change as well as any red shift in the UV- Vis spectral peaks even after the addition of very high amount of salt [73]. The stability of nanoparticles in solution is mainly dependent on the surface properties of nanoparticles with an increase in electrostatic repulsion and steric hindrance of the nanoparticles surfaces significantly improve their stability in solution [64]. Panday et al synthesized gold nanoparticles using Citrus limon and observed their high stability in an acidic pH and elevated temperature [55]. Understanding the stability over a wide range of environmental conditions is essential, which likely exhibits the fate of nanoparticles in biological medium.

Table-1: Comparative antibacterial bioassay of Citrus fruit extracts and their GNPs.

###Citrus sinensis###Citrus reticulata###Citrus grandis###Citrus aurantium

###Bacterial strain###Streptomycin


Klebsiellae pneumonia###NA###NA###NA###NA###NA###NA###10.3 0.17###12.4 0.20###26.0 2.00

###Bacillus subtilis###9.93 0.15 11.9 0.20###NA###NA###NA###NA###11.9 0.15###14.1 0.20###27.0 3.00

Staphylococcus aureus###11.9 0.20 13.3 0.20###14.9 0.15###16.0 0.15###11.9 0.15###14.1 0.17###12.0 0.15###11.9 0.11###27.0 1.00

Table-2: Comparative antifungal bioassay of Citrus fruit extracts GNPs.

Fungal strain###Citrus sinensis###Citrus reticulata###Citrus grandis###Citrus aurantium

Alternaria solani###NA###34.9 0.25###20.2 0.10###20.3 0.10

Aspergillus flavus###NA###39.9 0.15###19.9 0.15###40.2 0.11

Aspergillus niger###NA###40.1 0.30###39.9 0.15###40.2 0.15

Sensing Ability of Gold Nanoparticles

It was observed from the UV-Vis absorption spectra that the GNPs exhibited high detection ability for heavy metals and antibiotics. As shown in Fig. 6, a decrease in the intensities of UV-Vis absorption spectra with an increase in volume of cobalt, copper, ceftriaxone and penicillin solutions was observed with all the Citrus fruit extracts. The correlation coefficient (r) was measured on how well the regression line represents the data which shows the association between detection ability of Citrus fruits GNPs and varying volume of metals or antibiotics. As shown in the insets of Fig. 6, an excellent correlation coefficient value suggests a strong linear A correlation for cobalt (r = - 0.9765; P less than 0.01), copper (r = - 0.9788; P less than 0.05), ceftriaxone (r = - 0.9979; P less than 0.001) and penicillin (r = - 0.9870; P less than 0.05). The high degree of correlation suggests that the removal/detection efficiency of the Citrus GNPs increases with an increase in volume of metals and antibiotics.

In sensor applications, the changes in the plasmon resonance are monitored as a function of changing the physical and chemical environment of the surface of nanoparticles and therefore high sensitivity of the spectral response to changes in the refractive index of the surroundings is desired [66]. The gradual decrease in the surface plasmon resonance peaks intensities of Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis was found to be linearly correlated with a slight B change in volume of metals and antibiotics. Nanoparticles have been a popular tool for detecting heavy metal ions [74-75] and antibiotics [76-78]. Surface plasmons are now being investigated in optics, magneto-optic, photonics, chemical and biosensing applications [79]. Therefore, a nanoscale chemical or biosensor can be developed by monitoring the surface plasmon resonance wavelength in response to the adsorbate induced changes in the local environment of the nanoparticle [80].

Antimicrobial Assays

As shown in Table-1, Citrus fruit extracts and their GNPs were tested for antibacterial activity against Klebsiella pneumonia, Bacillus subtilis and Staphylococcus aureus. As compared to the standard streptomycin, Citrus aurantium extract as well as its GNPs exhibited moderate antibacterial activity against all the tested bacterial strains. Similar antibacterial activity was observed with both the extract and GNPs of Citrus sinensis against Klebsiella pneumonia and Bacillus subtilis. Moreover, good antibacterial activity against Staphylococcus aureus was noticed for Citrus reticulata and Citrus grandis fruit extracts as well as their GNPs. As shown in Table-2, GNPs of Citrus reticulata, Citrus aurantium, Citrus sinensis and Citrus grandis were tested for antifungal activity against Alternaria solani, Aspergillus niger and Aspergillus flavus. Good antifungal activity was exhibited by GNPs of Citrus reticulata, Citrus aurantium and Citrus grandis against all the tested fungal strains.

However, Citrus sinensis GNPs were inactive against these fungal strains. Silver nanoparticles of Citrus limon have shown to possess enhanced antifungal activity and is due to the synergistic effect of silver nanoparticles and essential oil components of lemon leaves [54]. The antimicrobial activity of nanoparticles is known to be a function of the surface area with a small size and high surface to volume ratio greatly enhances their interaction with the microorganisms [81]. Moreover, the GNPs can be used to coat a wide variety of surfaces for instance implants, fabrics for treatment of wounds and glass surfaces to maintain hygienic conditions [82].

Conflicts of Interest

The authors have no conflicts of interest to declare.


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Date:Aug 31, 2015
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