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Phytochemical Screening, Antimicrobial and Antioxidant Activities of Ficus natalensis.

Byline: Muhammad Ajaib, Muniza Almas, Khalid Mohammed Khan, Shahnaz Perveen and Shazia Shah

Summary: Phytochemical screening, antimicrobial and antioxidant potential of the bark and leaves extracts of Ficus natalensis were carried out by using various techniques. Phytochemical analysis showed the presence of terpenoids, alkaloids, flavonoids, tannins, saponins, cardiac glycosides and reducing sugars in different extracts of Ficus natalensis. The antibacterial potential against S. aureus was reported as most promising amongst all. The petroleum ether extract of leaves with a zone of inhibition 50 0.51 mm and bark extracts with a zone of inhibition 55.7 1.15 mm inhibited S. aureus. The chloroform leaves extract also showed an inhibition zone of 50 2 mm against S. aureus. The antifungal potential of methanol bark extract at 43.7 1.527 mm and petroleum ether extracts of bark with zones of inhibition 37 0.577 mm against A. niger showed most prominent activity. By using different assays, the extracts were screened for the antioxidant potential.

The estimation of antioxidant activity by metal chelating activity revealed that water extract of leaves was most active with a value of 74.673 0.302 percentage bound iron. The chloroform extract of bark showed highest flavonoid content (1005.53 0.503 mg/mL of quercetin), whereas chloroform extract of leaves exhibited maximum phenolic content (21.626 0.545 mg/g of GAE). In ABTS assay, water extract of leaves showed maximum TEAC value (7.713 0.7 mM of trolox equivalent). The highest free radical scavenging DPPH percentage was observed with distilled water extract of bark (91.92 0.08 %).

Keywords: Ficus natalensis, Antibacterial activity, Antifungal activity, Antioxidant activity.

Introduction

The use of medicinal plants is earliest, either by directly consuming their parts or processed them for healthcare preparations. This speculation can be supported by the ancient texts like Vedas and Bible, which contain descriptions of herbal remedies [1].

Throughout the history of human civilization, bacteria are causative agents of numerous life-threatening epidemics. Tuberculosis, typhus, plague, diphtheria, typhoid, cholera, dysentery and pneumonia are some highlighted examples of the bacterial diseases. [2]. 25% of the human world population is suffering from various skin, hair or nail fungal infections [3].

Plants produce secondary metabolites and the medicinal importance of plants is attributed to these metabolites [4]. The major phytochemical groups which impart biological activities against infections are phenols, polyphenols, quinones, flavonoids, flavonols, tannins, terpenoids, essential oils, alkaloids, polypeptides and other compounds. [5].

Free radicals, highly reactive chemical species produced exogenously or by aerobic respiration, cause several diseases and disorders of varying intensity. The reactive oxygen species (ROS) superoxide anion, hydroxyl radical and hydrogen peroxide- hold a pivotal role in the establishment of diseases such arthritis diabetes, aging, immunosuppression, asthma, dementia, mongolism, carcinoma and parkinson's disease [6]. Free radicals oxidize and damage DNA, lipids, proteins and other biomolecules. In a healthy individual, there exists equilibrium between the free radicals and antioxidants [7]. The antioxidants synthesized by our body are not sufficient to counterpoise the deleterious effects of free radical; hence an exogenous supply of antioxidants become necessary [8]. Flavonoids, tannins, lignin, phenolics, and other secondary metabolites of plant origin are reported to possess antioxidant properties [9].

Crude plant derived drugs, vegetables, fruits, oil seeds, cereal crops, barks and roots of different plants are reported as potential sources of antioxidant compounds [10].

Ficus natalensis is belong to family moraceae, it is a semi-scandant (erect) and small tree.

Moraceae or fig family is a large family of 40 genera and 1400 species. 24 species of genus Ficus L. have been reported in Pakistan [11]. Ficus natalensis is used to treat toothache, backache and joint pain [12]. This species is reported in Pakistan (Botanic Garden, GCUL and Bagh-e-Jinnah, Lahore) [13].

Experimental

Plant Material

The bark and leaves of Ficus natalensis sub sp. leprieurii (Miq.) C.C. Berg was collected at the botanic garden, Government College University, Mall road, Lahore. The plant was identified by Dr. Sultan Ahmad Herbarium, Government College University, Lahore, with a voucher no. GC. Herb. Bot. 2941.

Micro-Organisms

The bacterial strains (Escherichia coli, Bacillus subtilis, Pseudomonas aeruginosa and Staphylococcus aureus) were collected by department of the pathology, Punjab institute of cardiology, jail road, Lahore. The fungal strains (Aspergillus niger and Aspergillus oryzae) were collected by the institute of industrial biotechnology and microbiology, GC University, Lahore.

Standard Discs

The antibiotic discs were amikacin, cephalaxin and erythromycin, while griseoflavin and terbinafin were used as the antimycotic discs.

Extraction

After shade drying and grinding (250 g) the plant material was subjected to extraction in solvents (1000 mL) in increasing order of polarity (petroleum ether, chloroform, methanol and distilled water) and concentrated on rotary evaporator. The resulting extracts were stored at 4 C to prevent fungal attack.

Phytochemical Analysis

Plant extracts were qualitatively analyzed for different phytochemicals by following the protocol adopted by Ayoola et al. [14].

Antimicrobial Activity

Preparation of Culture Media and Culture Plates

In accordance with the protocol adopted by Cruick-Shank et al. culture media were prepared [15]. For the preparation of 1L (potato dextrose agar) PDA medium, 39 g of PDA was dissolved in distilled water and final volume was raised up to 1L. For the preparation of nutrient agar medium, 8 g of NB and 14 g of agar was dissolved in distilled water and final volume was made up to 1L. The pH of PDA medium and nutrient medium was maintained at 5.6 0.2 and 6.8 0.2, respectively. Once prepared, media were autoclaved for 15 minutes at a temperature of 120 C and 15 lb/psi pressure. Under the aseptic condition of laminar air flow, 20 mL of medium was poured in each plate which then solidified at room temperature.

Agar Well Diffusion Method

Inoculum was prepared and the turbidity of bacterial inoculum was adjusted to 1.5x108 CFU/ml by contemplating/comparing it with McFarland 0.5 Barium Chloride turbidity standard. The consistency of fungal inoculum was homogenized by employing 0.5 McFarland turbidity standards and the density was maintained within a range of 1x103-5x103 CFU/mL [16]. Under the laminar air flow, plates were loaded with the inoculum by streak plate method. For the purpose of streaking, sterile cotton swabs were used. With the help of a cork borer no.4, well was bored in the center of the medium. The well was then filled with 1mL of plant extract by employing Drummond's capillary tube. The plates with fungal test organisms were incubated at 25 2 C for 48 h, whereas the plates containing bacterial inoculum were incubated at 35 2 C for 24 h.

The incubation temperature was ensured to be constant; otherwise, the bacterial and fungal growth would have been delayed or too early. After the incubation period, zone of inhibition for each plate was measured and photographed.

Minimum Inhibitory Concentration (MIC)

For the evaluation of minimum inhibitory concentration, agar dilution method was employed in accordance with Joshua and Takudzwa [17]. Four dilutions, 10, 0.5, 0.25, and 0.125 mg/mL were made for the methanol extracts of leaf and bark. Maintaining a ratio of 9:1, 18 mL of autoclaved medium was poured in each plate and 2 mL of extract was added into it and mixed well to ensure an even distribution. On the surface of solidified medium, the inoculum (fungal or bacterial) was streaked. The inoculated plates were incubated. The inhibition of growth was represented as "-", whereas the growth without any inhibitory effect by extract was represented as "+".

Antioxidant Activity

For the quantification of the antioxidant activity of the plant extracts, following assays were executed:

Total Flavonoid Content (TFC)

The total phenolic content was determined according to the protocol formulated by Dewanto et al., [18]. In 0.25 mL (250 uL) plant extract, 1.25 mL (125 uL) of distilled water and 75 of 5% NaNO2 solution were added. After vigorous shaking and 6 minutes long rest, 0.15 mL (150 uL) of a 10% AlCl3.6H2O solution was added. Following vigorous agitation and 5 minutes stay, 0.5 mL (500 uL) of 1M NaOH and 0.27 mL (270 uL) of distilled water were added so that the total volume was brought to 2.5 mL. After proper mixing, absorbance of each sample and control was measured at the wavelength of 510 nm. The total flavonoid contents (TFC) was estimated from the standard curve of quercetin and values were expressed as mg of quercetin equivalents in per gram of sample.

Total Phenolic Content (TPC)

Total phenolic content of extracts was estimated by method proposed by Singleton and Rossi [19]. In 40 uL of extract (10 mg/mL), 3.16 mL of distilled water and 20 uL of Folin- Ciocalteu reagent were added. After proper shaking and a stay of 8 minutes, 600 uL of Na2CO3 solution was added and the sample was incubated for 30 minutes at 40 C By using a standard curve, the total phenolic contents of the sample extracts were determined and were expressed as mg of gallic acid equivalents per gram of fresh weight (mg/g).

Metal Chelating Activity

The protocol developed by Dinis et al. [20] was followed in this study to determine the chelation of ferrous ions and standards. In 100 uL (0.1 mL) of the plant extract's aliquot (10 mg/mL), 50 uL (0.05 mL) of ferrous sulphate (2 mM FeSO4.7 H2O) and 200 uL (0.2 mL) of 5 mM ferrozine solution were added. By adding 3.65 mL of methanol, the final volume was made up to 4 mL. After vigorous agitation and incubation (for 10 minutes) at room temperature, absorbance of sample solution was noted at 562 nm. From the absorption value, percentage bound iron was quantified by applying the following equation:

Percentage bound iron =(1-A sample / A control) x 100

The values of percentage bound iron, for each sample, were represented in the form of a bar graph.

ABTS Assay

ABTS (2,2'-Azino-bis-3-ethylbenzothiazoline-6-sulphonic acid) assay was performed in accordance to the protocol formulated by Re et al. [21]. 25 mL of (phosphate-buffered saline) PBS buffer was taken in beaker, 1-2 drops of ABTS reagent were added in it and absorbance was taken at 734 nm. Absorbance was to be maintained within a range of 0.68-0.72. If the pH was more than 0.72 then PBS buffer was added and if it was less than 0.68, then ABTS reagent was added. 2.99 mL of this solution (with adjusted pH) was taken in a test tube.10 uL of sample was added in this reagent. After 8 minutes, absorbance was measured at 734 nm.

DPPH Radical Scavenging Activity

For this assay, the method followed by Shimada et al. [22]. The stock solution of DPPH (2,2-diphenyl-1-picrylhydrazyl) radical cation was prepared (25 mg/mL) in methanol and absorbance was adjusted to 1.00 + 0.02 at 515 nm by diluting it with methanol. Appropriate quantity of sample was added to 2.5 mL of this diluted reagent and change in absorbance was measured after every 5 minute interval for 30 minutes. The percentage of DPPH radical remaining was calculated by applying the following formula:

% DPPH remaining= (Af / A0) x 100

where: Af = Absorbance of sample A0= Absorbance of control

A kinetic curve was plotted showing decrease in absorbance of DPPH with time and IC50 value was also calculated for each sample.

Results and Discussion

Phytochemical analysis was carried out for investigation of compounds present in plant material. Phytochemical screening of leaves and bark extracts revealed the presence of alkaloids, flavonoids, tannins, cardiac glycosides, saponins, anthraquionones, terpenoids and reducing sugar (Table-1).

Table-1: Qualitative phytochemical analysis of the leaves and barks extracts of Ficus natalensis.

Phytochemicals###Leaves###Bark

###Petroleum ether###Chloroform###Methanol Distilled###Petroleum ether###Chloroform###Methanol###Distilled

###water###water

###Reducing sugars###+###+###+###+###+###+###+###+

###Flavonoids###+###-###+###+###+###-###+###+

###Tannins###-###-###+###-###+###+###-###-

###Cardiac glycosides###+###+###-###+###+###+###-###+

###Saponins###+###+###+###+###+###+###+###+

###Alkaloids###+###-###+###+###+###+###-###+

###Anthraquinones###+###+###+###+###+###+###+###+

###Terpenoids###+###+###-###+###+###+###-###+

Antimicrobial potential were carried out by using four bacterial strains Escherichia coli, Pseudomonas aeruginosa (Gram negative), Staphylococcus aureus and Bacillus subtilis (Gram positive) and two fungal strains Aspergillus niger and Aspergillus oryzae. The standard discs were used for comparison between zones of inhibition produced by plant extracts and commercially available discs (Table-2).

Table-2: Zone of inhibition (mm) exhibited by standard discs against bacterial and fungal strains.

###Microbial###Standard disc###Concentration of###Zone of

###strain###standard disc (g)###inhibition

###(mm)

###E. coli###Amikacin###20###16.9 0.9

###B. subtilis Cephalaxin###20###19 1.02

Bacterial

strains

###P. aeruginosa Erythromycin###20###15.3 0.57

###S. aureus###Amikacin###20###18.3 1.15

###Griseoflavin###20###20.6 1.53

###A. niger

###Terbinafin###20###21 2.64

Fungal

strains

###Griseoflavin###20###22.6 1.15

###A. oryzae

###Terbinafine###20###20.3 2.52

The maximum antibacterial activity against S. aureus were observed by petroleum ether extract of leaves and bark with a zone of inhibition of 50 0.51 mm and 55.7 1.15 mm respectively. The chloroform leaves extract also revealed an inhibition zone of 50 2 mm against S. aureus. The petroleum ether extract of leaves showed significant activity with an inhibition zone of 40 0.4 mm against B. subtilis. The petroleum ether extract of leaves showed an inhibition zone of 44.7 0.57 mm against E. coli. The petroleum ether extract of bark and distilled water extract of leaves also exhibited good inhibition 30 0.57 mm and 30 0.26 mm respectively against E. coli. The results of antibacterial activity against P. aeruginosa were reported by the petroleum ether extract of bark (47 0.4 mm). Chloroform and methanol extracts of bark and petroleum ether and methanolic extracts of leaves gave promising results (Table-3).

The MIC value of the methanol extracts of bark and leaves at concentration 1.25 mg/mL and 5 mg/mL against E. coli showed less affective, whereas methanolic extracts of bark against P. aeruginosa inhibited the growth up to concentration of 0.625 mg/mL but the leaves extract of methanol against P. aeruginosa lost its activity beyond at concentration of 5 mg/mL. The methanolic extracts of bark and leaves reduced the growth of S. aureus up to 0.625 mg/mL and B. subtilis was grow only below the concentration of 0.625 mg/mL (Fig. 1).

Assessment of antifungal activity revealed that A. niger was inhibited by all the extracts with variable potency. The methanol extract of bark was found to be most potent against A. niger with a zone of inhibition 43.7 1.527 mm. The petroleum ether extract of leaves was least effective against fungal strain (9 0 mm). The petroleum ether extract of bark showed a considerably high activity with a zone of inhibition 37 0.577 mm. All extracts showed a moderate level of inhibition against A. oryzae between 23 2.645 mm to 34.8 1.607 mm (Table-3).

The estimation of MIC also supported the activity of methanol extract of bark. The methanol extract of bark showed inhibition of A. niger and A. oryzae up to the concentration of 0.625 mg/mL. The methanol extract of leaves showed low inhibition towards both fungal strains (10 mg/mL against A. niger and 5 mg/mL against A. oryzae). A. niger was more susceptible to the extracts of the plant, whereas A. oryzae, was somewhat resistant against the tested extracts (Fig. 2). It was also concluded that methanolic extract of bark was potentially a promising candidate to be used as a natural source of antifungal medicine.

The antioxidant potential was screened by using different assay. The antioxidant potential by metal chelating activity was estimated at concentration of 10 mg/mL. The distilled water extract of leaves showed highest potential 74.673 0.302%. The petroleum ether extract of bark exhibited metal chelating activity 61.5 0.5% (Table-4).

Table-3: Zone of inhibition (mm) exhibited by leaves and bark extracts of F. natalensis against fungal and bacterial strains

Plant part###Extracts###Zone of inhibition (mm)

###E. coli###P. aeruginosa###S. aureus###B. subtilis###A. niger###A. oryzae

###Bark###Petroleum ether###30 0.57###47 0.4###55.7 1.15###38###1.52###37###0.57###23.7 0.57

###Chloroform###27 0.72###30.5 1.28###50.9 0.9###29.7 0.3###25###1.0###25.2 0.28

###Methanol###23 1###30.8 0.34###25.6 0.63###20.8 0.72###43.7 1.52###26.7 1.15

###Distilled water###26 0.97###28 0.76###23###0.6###26.8 0.4###27###1.52###26.2 0.76

###Petroleum ether###44.7 0.57###33 0.28###50###0.51###40###0.4###9###0###23###2.64

###Chloroform###27 0.85###27 0.4###50###2###36###0.9###28###1.52###25.2 1.25

###Leaves###Methanol###21 1.52###31 1.52###26.7 1.53###16###1###19###1###34.8 1.60

###Distilled water###30.7 0.26###21.7 0.57###23###2.08###22.9 0.11###29.8 1.04###28###1.73

###LSD###1.53###1.42###2.29###1.38###1.97###2.48

Table-4: Metal chelating activity of crude extracts of leaves and bark of Ficus natalensis.

###Plant part###Extraction solvent###Concentration of extract(mg/mL)###Absorbance at 562 nm###Percentage bound iron(%)

###Petroleum ether###10###0.691###61.5 0.5

###Chloroform###10###1.838###49.73 0.2867

###Bark

###Methanol###10###1.245###30.08 0.102

###Distilled water###10###1.055###41.01 0.42

###Petroleum ether###10###0.905###49.22 0.737

###Chloroform###10###2.094###38.36 0.572

###Leaves

###Methanol###10###1.273###28.41 0.645

###Distilled water###10###0.451###74.673 0.302a

###LSD###0.914

The maximum flavonoid content was observed by chloroform extract of bark 1005.53 0.503 mg/mL of quercetin. The petroleum ether extract of bark also showed a significantly high value 836.06 0.763 mg/mL of quercetin. Remaining extracts contained reasonable to satisfactory levels of flavonoid contents (Table-5).

The petroleum ether extract of bark showed highest phenolic content 21.626 0.545 mg/g equivalents of GAE. The chloroform extract of leaves also demonstrated a significant value 21.626 0.545 mg/g equivalent of GAE (Table-6).

The results of ABTS assay were expressed in terms of TEAC (trolox equivalent antioxidant capacity) value. The distilled water extract of bark demonstrated highest value 7.956 0.526 mM of trolox equivalent. The petroleum ether bark extract 7.183 0.241 and methanol bark extract 7.436 0.264 were also proved to be carrying significant antioxidant properties. The distilled water extract of leaves also showed significant value 7.713 0.7 mM of trolox equivalent (Table-7).

Table-5: Quantification of total flavonoid content of crude extracts of leaves and bark of Ficus natalensis

Plant part###Extraction solvent###Concentration of###Absorbance at 510###Amount of flavonoid content

###extract (mg/mL)###nm###(mg/l of Quercetin)

###Petroleum ether###10###3.913###135.76 0.208

###Chloroform###10###2.914###1005.53 0.503

###Bark

###Methanol###10###1.563###538.2 0.721

###Distilled water###10###0.765###264.51 0.501

###Petroleum ether###10###2.422###836.06 0.763

###Chloroform###10###0.869###310.23 0.681

###Leaves

###Methanol###10###2.011###695.06 0.902

###Distilled water###10###0.420###145.13 0.404

###LSD###3179.57

Table-6: Quantification of Total Phenolic Content of crude extracts of leaves and bark of Ficus natalensis.

###Pant part###Extraction solvent###Concentration of extract (mg/mL)###Absorbance at 765 nm###GAE (mg/g equivalents)

###Petroleum ether###10###1.989###34.93 0.391

###Chloroform###10###0.174###3.084 0.104

###Bark

###Methanol###10###0.731###12.751 0.282

###Distilled water###10###0.469###8.263 0.173

###Petroleum ether###10###0.806###14.096 0.746

###Chloroform###10###1.247###21.626 0.545

###Leaves

###Methanol###10###0.671###11.637 0.445

###Distilled water###10###0.491###8.538 0.504

###LSD###0.7691

Table-7: ABTS assay of crude extracts of leaves and bark of Ficus natalensis.

Pant part###Extraction solvent###Concentration of extract###Absorbance at 734 nm###TEAC value

###(mg/mL)###(mM of Trolox equivalent)

###Petroleum ether###10###0.129###7.183 0.241

###Chloroform###10###0.562###1.583 0.085

###Bark

###Methanol###10###0.102###7.436 0.264

###Distilled water###10###0.077###7.956 0.526

###Petroleum ether###10###0.3###4.81 0.327

###Chloroform###10###0.604###1.2 0.304

Leaves

###Methanol###10###0.155###6.44 0.382

###Distilled water###10###0.064###7.713 0.7

###LSD###0.6836

Conclusion

The plant material F. natalensis is a powerful source of antioxidants and antimicrobial agents. The results of antibacterial activity were more remarkable than antifungal activity. The petroleum ether extracts of bark and leaves were most effective against all four bacterial strains. S. aureus was most susceptible against all the crude extracts of the plant. In case of antifungal activity, methanol extract of bark was most promising against A. niger. The antioxidant potential also exhibited significant result which was determined by using different method. The antioxidant potential by metal chelating activity showed that water extract of leaves was most active (74.673 0.302 % bound iron).

The chloroform extract of bark showed highest flavonoid content (1005.53 0.503 mg/mL of quercetin), whereas maximum phenolic content (21.626 0.545 mg/g of GAE) was exhibited by chloroform extract of leaves. In ABTS assay maximum TEAC value (7.713 0.7 mM of trolox equivalent) was observed by water extract of leave. The maximum percentage DPPH free radical scavenging activity (91.92 0.08%) was observed by water extract of bark.

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Author:Ajaib, Muhammad; Almas, Muniza; Khan, Khalid Mohammed; Perveen, Shahnaz; Shah, Shazia
Publication:Journal of the Chemical Society of Pakistan
Article Type:Report
Date:Apr 30, 2016
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