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BY 4.0 license Open Access Published by De Gruyter Open Access April 19, 2023

GC-MS analysis and antibacterial activities of some plants belonging to the genus Euphorbia on selected bacterial isolates

  • Mohamed A. Al Abboud , Khatib Sayeed Ismail , Abdullah Mashraqi , Saad Albishi , Ali A. Al-Namazi and Yahya S. Masrahi EMAIL logo
From the journal Open Chemistry

Abstract

Plant extracts have always been used as an alternative source of antimicrobial compounds. The recent spread of multi-drug-resistant bacteria and their increased treatment costs necessitated the study of alternative, cheap sources. The family Euphorbiaceae has over 300 genera and is widely used in traditional medicine. Euphorbia triaculeata, E. fractiflexa, and E. inarticulata were selected to study the antibacterial activity of the methanolic extract against 13 Gram-positive Staphylococcus aureus strains (including methicillin-resistant S. aureus) and 2 Gram-negative isolates, Escherichia coli and Klebsiella pneumoniae, by the Kirby Bauer Disc diffusion test. Paper discs with different concentrations of the extracts (100, 50, and 25 µg mL−1) were prepared, along with the methanol control and standard antibiotic control. A gas chromatography-mass spectrometry (GC/MS) analysis was done to study the phytochemical components present in the plant methanolic extracts. A total of 50 different phytochemical compounds with antibacterial activity were detected by GC/MS analysis of the plants. Twenty-five compounds were detected in E. inarticulata, 24 in E. triaculeata, and 21 in E. fractiflexa. Out of 37 compounds found in E. inarticulata and E. triaculeata, 12 (32.43%) were common to both. Eleven (22%) compounds were unique to E. inarticulata, while 9 (18%) compounds were unique to E. triaculeata, and 13 (26%) compounds were unique to E. fractiflexa. E. fractiflexa showed the best antibacterial activity against MRSA and Gram-negative bacteria. It also showed higher unique compounds with antibacterial activity (26%), followed by E. inarticulata (11, 22%). This is the first GC/MS analysis and antimicrobial activity report of E. triaculeata and E. fractiflexa.

1 Introduction

Infectious diseases are a major public health problem in the world. They are one of the leading causes of death. The increased use of antibiotics in the past few years, both in appropriate and inappropriate ways, has led to increased antibiotic resistance. Bacteria are able to resist various antibiotics through horizontal gene transfer or mutation [1]. It is expected that by 2050, 10 million lives will be lost per year, and a cumulative 100 trillion USD of economic output will be at risk due to the rise of drug-resistant infections if we do not find proactive solutions now to slow down the rise of drug resistance [2]. Methicillin-resistant Staphylococcus aureus (MRSA) is a recent problem that needs swift resolution. Although extensive research is carried out worldwide on drug discovery, very few new candidates are being discovered. The increasing failure of antimicrobials and antibiotic resistance shown by pathogenic microbial infectious agents has led to the screening of several medicinal plants for their potential antimicrobial activities [3]. Adverse reactions shown by some drugs also encourage using local medicinal plants as possible candidates for alternative medicine [4]. Traditional medicines have been the preferred choice in Saudi Arabia for minor ailments [5].

Euphorbiaceae is one of the largest families of angiosperms, with over 300 genera and 8,000 species, distributed mostly in subtropical and tropical regions [6]. Euphorbiaceae represents one of the chemically most diverse angiosperms, with many economic and medicinal uses [6,7]. Euphorbia L. is the largest genus in the family, with more than 2,000 species [6]. Euphorbia species is widely distributed in arid habitats of Africa and the Arabian Peninsula [8]. They have been known as annual, biennial, or perennial herbs with thorns and milky latex. Previous studies on some Euphorbia species (E. granulata, E. helioscopia, E. hirta, E. inarticulata, and E. royleana) showed varied antimicrobial activities [9,10,11]. Different phytochemicals have been found in Euphorbiaceae species mainly terpenoids, diterpenoids, flavonoids, alkaloids, tannins, etc. [12].

Not much information is found in the literature about the antimicrobial activities of many Euphorbia species. Furthermore, very little information is available about their activity against multi-drug-resistant bacteria. The spines on these Euphorbia species are particularly sharp and the latex is toxic in nature; hence it is extremely difficult to work with these plants. Many plants from this family are listed on the poisonous database of the United States Food and Drug Administration (USFDA 2019) [13]. Therefore, this work aimed to study the antimicrobial activities of three Euphorbia species (Euphorbia triaculeata, E. fractiflexa, and E. inarticulate from Jazan province, southwestern Saudi Arabia) against Gram-positive, Gram-negative, drug-resistant, and drug-sensitive bacteria, and their phytochemical components. Gas chromatography mass spectrometry (GC/MS) analysis of their methanol extracts to examine their probable active compounds was also studied. This is the first GC/MS analysis and antimicrobial activity report of E. triaculeata and E. fractiflexa.

2 Materials and methods

2.1 Collection, identification, and extraction of plant materials

The three Euphorbia species of this study are stem succulents, wildly growing in rocky habitats in Jazan province, southwestern Saudi Arabia.

Stem branches of E. triaculeata Forssk., E. inarticulata Schweinf., and E. fractiflexa S.Carter & J.R.I.Wood were collected from different localities of rocky habitats, in Jazan province. The plants were identified, and a specimen was deposited in the Herbarium of the Department of Biology. The branches were thoroughly washed for 5 min with 2% of commercial sodium hypochlorite (NaOCl) and then five times with sterile distilled water. Samples were dried in an air oven at 55°C, powdered, and soaked in 60–80% (1:4 w/v) petroleum ether for 24 h; they were then filtered through Whatman paper No. 1. Plant materials were extracted with methanol (95%). Forty grams of the plant material were dissolved in 400 mL of 95% (1:10 w/v) methanol in a dark bottle of 1 L. The bottle was sealed and shaken for 1.5 h in a shaker water bath at 110 rpm and 30°C for 24 h at room temperature. This procedure was repeated five times. After 5 days, the contents of the bottle were filtered through filter paper Whatman No.1. The obtained solution of the plant methanol extract was evaporated to a thick mass in a shaker water bath at 50 rpm and 45°C and kept in a refrigerator till further analysis [14].

2.2 Microorganisms

Fifteen bacteria isolates, including 13 Gram-positive S. aureus (12 MRSA and 1 sensitive strain) and 2 Gram-negative bacteria (Klebsiella pneumonia and Escherichia coli), were included in the antimicrobial sensitivity testing. All microorganisms were obtained from the Biology Department, College of Science, Jazan University [15]. The fresh culture was used for antimicrobial sensitivity testing by the Kirby Bauer Disc diffusion test [16].

2.3 Plant extract working solution

Different concentrations of plant methanolic extracts (100, 50, and 25 µg mL−1) and the blank methanol control were used. A total of 200 mg of the plant extract was dissolved in 20 mL of methanol (10 µg mL−1); from this, 10 mL was transferred to the next conical flask containing 10 mL of methanol (5 µg mL−1). After mixing thoroughly, 10 mL was transferred to the next flask containing 10 mL of methanol to give a 2.5 µg mL−1 concentration. About 10 mL from the last flask was discarded, and 10 mL of methanol was used as the blank. Different concentrations of the plant extracts and the blank were poured on sterile filter paper discs kept in different sterile Petri plates and allowed to dry in a bacteriological hood. These paper discs were used for the Kirby Bauer disc diffusion test.

2.4 Antibiotic sensitivity testing

Antibiotic sensitivity testing of the methanolic plant extract was carried out using Kirby Bauer’s disc diffusion testing method on sterile Muller and Hinton agar plates [16]. A 24 h fresh culture of the test isolates was used to prepare a saline suspension to match the 0.5 McFarland turbidity standard tubes (1.5 × 108 colony forming units/mL). Each isolate was spread on sterile MHA plates using sterile cotton swabs. Different concentration discs were placed on the MHA plates, and a standard antibiotic disc of 5 µg rifampicin was also placed along with it as a control for comparison. The plates were kept in an incubator at 37°C for 24 h. The zone of inhibition was measured using a zone-measuring ruler (Himedia, India) in millimeters (mm). All test procedures followed the recommended standards of the Clinical and Laboratory Standard Institute [17]. All the tests were done in triplicates.

2.5 GC-MS

Methanol extracts of plants were analyzed using the GC-MS apparatus (model; QP2010 Ultra, Shimadzu Corporation, Kyoto, Japan), as described by Almalki et al. [11]. The separation was achieved on the Rtx5MS capillary column (30 m length × 0.25 mm i.d. coated with a 0.25 μm film thickness stationary phase; Restek Corporation, USA). Helium was employed as the carrier gas at a constant linear velocity of 36.3 cm s−1. A sample volume of 1.0 μL was injected using the AOC-20i + s auto-injector. The injection port was set at 290°C in a split-less mode. The temperature of the GC oven was programmed as follows: 5 min at 50°C, heated at 5°C min−1 to 310°C, and held for 10 min. The ion source temperature in the MS was set at 230°C and the interface at 280°C. A total ion chromatogram was created for the m/z range of 50–700. The GC peaks were identified by comparing their mass spectra with the database of the National Institute of Standards and Technology version 11. The relative amount of each component was calculated by comparing its peak area with the total area of peaks in the chromatogram.

2.6 Statistical analysis

Statistical analysis was carried out with SPSS V12 using appropriate analysis. Differences were found between the control and treated organisms. In triplicate, the results were interpreted as mean ± SEM (standard error of the mean) for each experiment or an average of three separate experiments (n = 3). The P-value obtained was statistically significant.

3 Results and discussion

Plants indigenous to a region have always been studied for their antimicrobial properties. They also give a natural alternative to chemotherapeutic agents. With the ever-increasing burden of drug resistance and the need for newer antibiotic molecules, the race is always on to find a cure for multi-drug-resistant bacteria. MRSA is one of the drug-resistant bacteria causing problems worldwide. Considering this, antimicrobial sensitivity was carried out for methanolic extracts of three Euphorbiaceae plants, mainly E. triaculeata, E. inarticulata, and E. fractiflexa against 13 Gram-positive S. aureus, of which 12 isolates were MRSA and 2 Gram-negative bacteria, E. coli and K. pneumoniae. As not much information was available against these three plant species, GC/MS analysis was carried out to see the probable compounds present in the methanolic extract. A literature search was done on the compounds found by GC/MS analysis and previously reported antibacterial activity.

3.1 Antibacterial sensitivity testing

Table 1 shows the effect of E. triaculeata methanol extracts at concentrations of 2.5, 5, and 10 µg mL−1 on the growth of bacterial species by using the paper assay disc method. The data exhibited that E. triaculeata methanol extracts had antibacterial activities against S. aureus (R4), S. aureus (R6), S. aureus (R8), and S. aureus (R11). MIC was found to be 2.5 µg mL−1 against all four isolates. No antibacterial activity was seen against Gram-negative bacteria. Of the 12 MRSA isolates, the extract showed activity against 4 (33.33%) samples. No activity was observed against Gram-negative isolates. No previous literature was reported against this specie.

Table 1

Antibacterial activities of E. triaculeata, E. inarticulate, and E. fractiflexa extracts on bacterial isolates

No. Bacterial isolates Control (0 µg mL−1) Plant extract concentrations (ppm)
2.5 µg mL−1 5 µg mL−1 10 µg mL−1
Zone of inhibition (mm) (+SD)
ET EI EF ET EI EF ET EI EF
1 S. aureus (s) 0 5 ± 0 5 ± 0 10.3 ± 1.5 5 ± 0 5 ± 0 12.6 ± 1.15 5 ± 0 5 ± 0 25.3 ± 0.57
2 S. aureus (R1) 0 5 ± 0 5 ± 0 6.3 ± 0.57 5 ± 0 5 ± 0 12.3 ± 0.57 5 ± 0 5 ± 0 21 ± 1.7
3 S. aureus (R2) 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 10 ± 1 5 ± 0 5 ± 0 17.6 ± 0.57
4 S. aureus (R3) 0 5 ± 0 5 ± 0 7 ± 1 5 ± 0 5 ± 0 10.6 ± 0.57 5 ± 0 5 ± 0 12.3 ± 0.57
5 S. aureus (R4) 0 6 ± 0 5 ± 0 6 ± 0 8 ± 1 5 ± 0 10.3 ± 0.57 9.7 ± 0.57 5 ± 0 19 ± 1.7
6 S. aureus (R5) 0 5 ± 0 5 ± 0 9.3 ± 1.15 5 ± 0 11.3 ± 1.1 15 ± 1 5 ± 0 13.3 ± 0.57 21.6 ± 0.57
7 S. aureus (R6) 0 8 ± 1 5 ± 0 5 ± 0 10.3 ± 1.5 5 ± 0 6.6 ± 0.57 12.3 ± 1.15 5 ± 0 14.3 ± 1.15
8 S. aureus (R7) 0 5 ± 0 5 ± 0 6.6 ± 0.57 5 ± 0 5 ± 0 10.3 ± 0.57 5 ± 0 5 ± 0 16 ± 1
9 S. aureus (R8) 0 7.3 ± 0.57 5 ± 0 5 ± 0 9.3 ± 0.57 5 ± 0 12.3 ± 0.57 13.3 ± 0.57 5 ± 0 21.3 ± 2
10 S. aureus (R9) 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 8.6 ± 0.57 5 ± 0 5 ± 0 16.3 ± 0.57
11 S. aureus (R10) 0 5 ± 0 7.3 ± 0.57 9.3 ± 1.15 5 ± 0 9.3 ± 1.1 11.3 ± 2 5 ± 0 12.6 ± 1.1 19.6 ± 1.5
12 S. aureus (R11) 0 6 ± 0 7 ± 1 5 ± 0 7 ± 1 8.6 ± 0.57 11.3 ± 2 8.6 ± 1.1 12.3 ± 0.57 20.3 ± 2
13 S. aureus (R12) 0 5 ± 0 5 ± 0 6 ± 0 5 ± 0 5 ± 0 9.3 ± 0.57 5 ± 0 5 ± 0 18.6 ± 1.15
14 K. pneumonia 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 9 ± 1 5 ± 0 5 ± 0 11.6 ± 0.57
15 E. coli 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 5 ± 0 10.6 ± 0.57 5 ± 0 5 ± 0 18.6 ± 2

ET = Euphorbia triaculeata, EI = Euphorbia inarticulate, EF = Euphorbia fractiflexa, SD = standard deviation (+).

The data exhibited in Table 1 also indicate that E. inarticulata methanol extracts have antibacterial activities against S. aureus (R5), S. aureus (R10), and S. aureus (R11). Of the 12 MRSA isolates, the extract showed activity against 3 (25.00%) samples. MIC was found to be 5 µg mL−1 for isolate number 5 and 2.5 µg mL−1 against isolates 10 and 11. No activity was seen against Gram-negative bacteria. Only one report was found previously on the E. inarticulata plant [11], in which they reported activity against Gram-positive and Gram-negative bacteria. In their study, except for E. coli, all other isolates tested were different. They found that the methanolic extract was the best extract to study the GC/MS analysis. The overall findings agreed with the previous literature. Being a strong polar solvent, methanol is considered highly efficient in extracting active compounds.

Different concentrations (2.5, 5, and 10 µg mL−1) of E. fractiflexa methanol extracts were used to evaluate their antibacterial activities against some Gram-positive and Gram-negative bacteria by using the paper assay disc method. Table 1 shows the inhibitory effect of the studied concentrations of the E. fractiflexa methanol extract against a sensitive strain of S. aureus, 12 strains of S. aureus (MRSA), K. pneumonia, and E. coli. The results indicated that the inhibitory effect of the E. fractiflexa methanol extract increased with increasing concentrations of E. fractiflexa methanol extracts. The extract at a concentration of 2.5 µg mL−1 showed antibacterial activity against S. aureus (s), S. aureus (R1), S. aureus (R3), S. aureus (R4), S. aureus (R5), S. aureus (R7), S. aureus (R10), and S. aureus (R12). The maximum inhibition zone for E. fractiflexa methanol extracts was recorded against S. aureus (s) (25.3 mm), followed by Staphylococcus aureus (R5) (21.6 mm) and S. aureus (R8) (21.3 mm). The methanolic extract of E. fractiflexa was shown to have a 100% antimicrobial effect on all 15 indicators, including the susceptible strain of S. aureus and all 12 strains of MRSA. It was also active against E. coli and K. pneumoniae. Figure 1 shows the antibiotic sensitivity testing of different methanolic extracts of the plants used.

Figure 1 
                  Antibiotic sensitivity testing of methanolic extracts of Euphorbiaceae: (a) methanolic extract of E. fractiflexa on S. aureus R3 (MRSA), (b) ethanolic extract of E. inarticulata on S. aureus R5 (MRSA), (c) methanolic extract of E. triaculeata on S. aureus R8 (MRSA). Disc concentrations from 10, 5, 2.5 µg mL−1, and methanol control.
Figure 1

Antibiotic sensitivity testing of methanolic extracts of Euphorbiaceae: (a) methanolic extract of E. fractiflexa on S. aureus R3 (MRSA), (b) ethanolic extract of E. inarticulata on S. aureus R5 (MRSA), (c) methanolic extract of E. triaculeata on S. aureus R8 (MRSA). Disc concentrations from 10, 5, 2.5 µg mL−1, and methanol control.

Figure 2 shows the GC-MS chromatogram of the methanolic extract of E. inarticulata; 65 peaks were detected. Detected by utilizing total ion concentration vs. time (in minutes). As seen in Table 2, 25 phytochemical components were detected by the GC/MS analysis of methanol extracts of E. inarticulata showing antibacterial activity. Only one study on methanol extracts of E. inarticulata has been reported by Almalki et al. [11]. The major difference between the two studies was that they did not study the effect of the plant extract on MRSA, while our study showed a high level of activity against MRSA.

Figure 2 
                  GC-MS chromatogram of the methanolic extract of E. inarticulata.
Figure 2

GC-MS chromatogram of the methanolic extract of E. inarticulata.

Table 2

Phytochemical components identified in the methanol extracts of E. inarticulata by GC-MS analysis

No. Name of the compound RT SI (%) MW (g mol−1) Peak area (%) Activity References
1 Glycerin 3.150 91 92 0.29 Bactericidal [23]
2 2,2′-Bioxirane 3.550 94 86 0.90 Antibacterial [24]
3 1-Hydroxy-2-butanone 3.860 88 88 0.05 Antibacterial [25]
4 2-Methyl[1,3,4]oxadiazole 4.525 83 84 0.53 Antimicrobial [26]
5 Maleic anhydride 5.425 83 98 0.18 Antibacterial [27]
6 Furfural 5.515 98 96 3.65 Antibacterial [28]
7 Nonanal dimethyl acetal 5.805 82 188 0.10 Antibacterial [29]
8 2-Furanmethanol 6.320 97 98 2.38 Antibacterial and antiviral [30]
9 4-Cyclopentene-1,3-dione 7.280 92 96 0.38 Antibacterial and antifungal [31]
10 2(5H)-Furanone 8.360 94 84 0.24 Antibiotic [32]
11 1,2-Cyclopentanedione 8.710 87 98 0.68 Antibacterial [33]
12 2-Furancarboxaldehyde, 5-methyl- 10.095 97 110 3.75 Antioxidant and antimicrobial [34]
13 2,4-Dihydroxy-2,5-dimethyl-3(2H)-furan-3-one 10.645 95 144 0.80 Antimicrobial [35]
14 Benzeneacetaldehyde 12.875 96 120 0.75 Antibacterial [36]
15 2,5-Dimethyl-4-hydroxy-3(2H)-furanone 13.615 92 128 1.16 Antimicrobial [37]
16 2-Furancarboxylic acid, hydrazide 14.215 93 126 0.69 Antibacterial [38]
17 Benzeneacetic acid 19.540 89 136 1.28 Antibacterial [39]
18 4-Hydroxy-3-methylacetophenone 21.250 87 150 1.84 Antimycobacterial [40]
19 Blumenol C 30.885 88 210 1.25 Antimicrobial [41]
20 n-Hexadecanoic acid 36.020 95 256 2.13 Antimicrobial [42]
21 Phytol 38.835 97 296 1.58 Antibacterial [43]
22 9,12-Octadecadienoic acid (Z,Z)- (Linoleic) 39.215 97 280 2.33 Antimicrobial [44]
23 Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester 45.445 90 330 1.07 Antibacterial [45]
24 γ-Sitosterol 56.770 89 414 4.79 Antibacterial [46]
25 β-Amyrin 57.395 97 426 4.73 Antibacterial [47]

As seen in Figure 3, the GC-MS chromatogram of the methanolic extract of E. triaculeata showed 49 peaks corresponding to different phytochemical compounds which were detected. A total of 24 phytochemical components (Table 3) were detected by GC/MS analysis of methanol extracts of E. triaculeata that showed antibacterial activity as previously reported by various studies. Though none of the previous literature was on E. triaculeata, the compounds were studied from various other plant sources.

Figure 3 
                  GC-MS chromatogram of the methanolic extract of E. triaculeata.
Figure 3

GC-MS chromatogram of the methanolic extract of E. triaculeata.

Table 3

Phytochemical components identified in the methanol extracts of E. triaculeata by GC-MS analysis

No. Name of the compound RT SI (%) MW (g mol−1) Peak area (%) Activity References
1 2-Furancarboxaldehyde, 5-methyl- 10.090 97 110 1.72 Antibacterial and antifungal [34]
2 Benzeneacetaldehyde 12.875 96 120 0.42 Antimicrobial and antibiofilm [48]
3 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl- 16.290 92 144 0.19 Antimicrobial [49]
4 2-Furfurylthiol 6.095 86 114 0.51 Antibiotic [50]
5 4-Cyclopentene-1,3-dione 7.280 86 96 0.64 Antibacterial and antifungal [31]
6 2(5H)-Furanone 8.355 95 84 6.76 Antimicrobial [32]
7 Butanoic acid, 4-hydroxy- 8.290 95 104 1.03 Antimicrobial [51]
8 6-Oxa-bicyclo[3.1.0]hexan-3-one 8.710 86 98 1.20 Antibacterial [52]
9 2,4-Dihydroxy-2,5-dimethyl-3(2H)-furan-3-one 10.635 95 144 0.26 Antibacterial and antifungal [35]
10 2H-Pyran-2,6(3H)-dione 11.215 89 112 0.55 Antibacterial [53]
11 2,5-Dimethyl-4-hydroxy-3(2H)-furanone 13.590 86 128 1.19 Antimicrobial [37]
12 2-Furancarboxylic acid, hydrazide 14.220 91 126 1.27 Antibacterial [54]
13 Benzeneacetic acid, methyl ester 17.245 85 150 0.49 Antimicrobial [55]
14 Sulfurous acid, hexyl heptyl ester 15.750 84 264 1.50 Antimicrobial [56]
15 Benzofuran, 2,3-dihydro- 18.555 90 120 4.04 Antibacterial [57]
16 Benzeneacetic acid 19.625 91 136 1.30 Antimicrobial [58]
17 2-Methoxy-4-vinylphenol 21.250 83 125 3.49 Antimicrobial [59]
18 Heptyl caprylate 21.485 74 242 1.64 Antimicrobial [60]
19 Hexadecanoic acid, methyl ester 35.290 94 270 6.17 Antimicrobial [61]
20 n-Hexadecanoic acid 36.020 95 256 1.70 Antibacterial [42]
21 Phytol 38.835 97 296 1.72 Antimicrobial [62]
22 9,12-Octadecadienoic acid (Z,Z)- 39.220 97 280 2.19 Antimicrobial [42]
23 Stigmasterol 52.210 70 412 0.48 Antimicrobial [63]
24 γ-Sitosterol 56.765 89 414 1.75 Antimicrobial [46]

As observed in the GC-MS chromatogram (Figure 4) of the methanolic extract of E. fractiflexa, 39 phytochemical components were detected. A total of 21 phytochemical components were detected by GC/MS analysis of methanol extracts of E. fractiflexa and they showed antibacterial activity as previously reported by various studies (Table 4). Though none of the previous literature was on E. fractiflexa, the compounds were studied from various other plant sources.

Figure 4 
                  GC-MS chromatogram of the methanolic extract of E. fractiflexa.
Figure 4

GC-MS chromatogram of the methanolic extract of E. fractiflexa.

Table 4

Phytochemical components identified in the methanol extracts of E. fractiflexa by GC-MS analysis

No. Name of the compound RT SI (%) MW (g mol−1) Peak area % Activity References
1 Glycerin 3.14 92 92 0.11 Antibacterial [22]
2 2,4-Dihydroxy-2,5-dimethyl-3(2H)-furan-3-one 10.645 90 144 0.07 Antimicrobial [35]
3 Benzeneacetaldehyde 12.9 90 120 0.04 Biological [64]
4 Thymine 14.065 85 126 0.07 Biological [65]
5 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl- 16.55 93 144 0.30 Biological [49]
6 Benzoic acid 17.165 98 122 1.53 Antibacterial [66]
7 Benzofuran, 2,3-dihydro- 18.54 90 120 0.69 Biological and antifungal [67]
8 2-Methoxy-4-vinylphenol 21.245 88 150 0.54 Antimicrobial [67]
9 Benzeneethanol, 4-hydroxy- 24.29 90 138 0.63 Antibacterial and antioxidant [68]
10 Benzoic acid, 2-(1-oxopropyl)-, methyl ester 24.960 75 192 0.12 Antibacterial, antifungal, and antioxidant [69]
11 1-Heptadecene 28.160 95 238 0.14 Antibiotic [70]
12 1,2-Benzenedicarboxylic acid, butyl methyl ester 31.095 96 236 0.38 Antibacterial and antioxidant [71]
13 Lanosterol 31.615 89 426 0.23 Antimicrobial [72]
14 Olean-18-ene 31.794 81 410 0.68 Antibacterial [73]
15 D:B-Friedo-B′:A′-neogammacer-5-en-3-ol, (3β)- 32.290 82 426 0.36 Biological [74]
16 4-((1E)-3-Hydroxy-1-propenyl)-2-methoxyphenol 34.249 74 180 12.15 Biological [75]
17 1-Nonadecene 35.184 88 266 9.16 Antibacterial [76]
18 n-Hexadecanoic acid 36.010 94 256 1.01 Antibacterial [42]
19 1,2-Benzenedicarboxylic acid, butyl 2-ethylhexyl ester 36.240 91 334 1.02 Antibacterial and antioxidant [71]
20 β-Sitosterol 56.775 91 414 2.75 Antibacterial [77]
21 β-Amyrin 57.405 95 426 4.01 Antioxidant [78]

A total of 50 different phytochemical compounds were detected by GC/MS analysis of three plants. Twenty-five compounds were detected in E. inarticulata, 24 in E. triaculeata, and 21 in E. fractiflexa. Of the 37 compounds found in E. inarticulata and E. triaculeata, 12 (32.43%) compounds were common in both. Compounds 2, 8, and 11 were found in all three plants and showed antimicrobial activities, as reported by previous studies. Of the 41 compounds found in E. inarticulata and E. fractiflexa, just 5 (12.2%) compounds were common to both plants. E. triaculeata and E. fractiflexa shared just 6 (15.39%) common compounds of the 39, as detected by GC/MS analysis. Of the total 50 compounds, 11 (22.00%) compounds were unique to E. inarticulata, while 9 (18.00%) compounds were unique to E. triaculeata and 13 (26%) compounds were unique to E. fractiflexa.

As seen in Table 5, compound 2, furaneol (2,4-dihydroxy-2,5-dimethyl-3(2H)-furan-3-one), is an aroma molecule found in fruits. It is known for its antibacterial activity, as seen in previous studies [18]. Compound 8, benzeneacetaldehyde, a phenolic compound, is also known to have antibacterial activity [19], and compound 11, n-hexadecanoic acid and a methyl ester of fatty acid, also known as palmitic acid, is known to have antibacterial activity [20]. All three plants showed the presence of these three antibacterial compounds. β-Amyrin (compound 19), a triterpene, a known antibacterial agent, was found in E. inarticulata and E. fractiflexa, thereby indicating a strong antibacterial activity. Triterpenes have been shown to act as an efflux pump inhibitor and a growth inhibitor and cause cell membrane disruptions [21]. Compound 22, glycerin, was also reported to have antibacterial activity and was found in the above two plant extracts [22]. A total of 13 molecules present only in E. fractiflexa molecules (from 38 to 50 in Table 5) indicate a stronger antimicrobial response confirmed by 100% antimicrobial activity as seen in Table 3 against Gram-positive, including MRSA and Gram-negative bacteria. Further studies are required to analyze E. fractiflexa and study other extracts such as chloroform and acetone, as well as its application to control multi-drug-resistant bacteria. An overall positive indication toward action on MRSA has made this a very important study.

Table 5

Common phytochemical compounds showing antibacterial activity as detected by GC/MS in E. inarticulata, E. triaculeata, and E. fractiflexa

Sr. No Compounds E. inarticulata E. triaculeata E. fractiflexa
1 2(5H)-Furanone + +
2 2,4-Dihydroxy-2,5-dimethyl-3(2H)-furan-3-one + + +
3 2,5-Dimethyl-4-hydroxy-3(2H)-furanone + +
4 2-Furancarboxaldehyde, 5-methyl- + +
5 2-Furancarboxylic acid, hydrazide + +
6 4-Cyclopentene-1,3-dione + +
7 9,12-Octadecadienoic acid (Z,Z)-(Linoleic) + +
8 Benzeneacetaldehyde + + +
9 Benzeneacetic acid + +
10 γ-Sitosterol + +
11 n-Hexadecanoic acid + + +
12 Phytol + +
13 1,2-Cyclopentanedione +
14 1-Hydroxy-2-butanone +
15 2,2′-Bioxirane +
16 2-Furanmethanol +
17 2-Methyl[1,3,4]oxadiazole +
18 4-Hydroxy-3-methylacetophenone +
19 βAmyrin + +
20 Blumenol C +
21 Furfural +
22 Glycerin + +
23 Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester +
24 Maleic anhydride +
25 Nonanal dimethyl acetal +
26 2-Furfurylthiol +
27 2H-Pyran-2,6(3H)-dione +
28 2-Methoxy-4-vinylphenol + +
29 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl- + +
30 6-Oxa-bicyclo[3.1.0]hexan-3-one +
31 Benzeneacetic acid, methyl ester +
32 Benzofuran, 2,3-dihydro- + +
33 Butanoic acid, 4-hydroxy- +
34 Heptyl caprylate +
35 Hexadecanoic acid, methyl ester +
36 Stigmasterol +
37 Sulfurous acid, hexyl heptyl ester +
38 1,2-Benzenedicarboxylic acid, butyl 2-ethylhexyl ester +
39 1,2-Benzenedicarboxylic acid, butyl methyl ester +
40 1-Heptadecene +
41 1-Nonadecene +
42 4-((1E)-3-Hydroxy-1-propenyl)-2-methoxyphenol +
43 Benzeneethanol, 4-hydroxy- +
44 Benzoic acid +
45 Benzoic acid, 2-(1-oxopropyl)-, methyl ester +
46 β-Sitosterol +
47 D:B-Friedo-B′:A′-neogammacer-5-en-3-ol, (3β)- +
48 Lanosterol +
49 Olean-18-ene +
50 Thymine +
TOTAL 25 24 21

+, present; –, absent.

4 Conclusion

E. inarticulata, E. triaculeata, and E. fractiflexa showed varied antibacterial activities. E. fractiflexa showed the best antibacterial activity against multi-drug-resistant strains of S. aureus, MRSA, and Gram-negative bacteria. It also showed more unique compounds with antibacterial activity (26%), followed by E. inarticulata (11%, 22%). This is the first report on the antimicrobial activity of E. triaculeata and E. fractiflexa based on GC/MS analysis. More studies on extraction methods and antimicrobial activities of compounds are needed to better extract the active compounds found in the crude extract of the Euphorbiaceae family.


tel: +966-506552385

  1. Funding information: The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia, for funding this research work through project number ISP20-16.

  2. Author contributions: MAA: set up and performed the experimental lab data, planned the research project, interpreted the data results, and wrote the manuscript. KSl: contributed to the planning of the research project and supported the experimental lab data work. AM: contributed to the planning of the research project and supported lab experiments. SA: analyzed and inspected the data and edited the manuscript. AAN: edited the text, assisted in the experimental lab data collection, and participated in the study project design. YSM: set up and performed the experimental lab data, planned the research project, interpreted the data results, wrote the manuscript, and also supported the research project’s funding. All the authors read the final manuscript and agreed.

  3. Conflict of interest: The authors declare that there is no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: All data generated or analyzed during this study are included in this published article.

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Received: 2023-02-23
Revised: 2023-03-27
Accepted: 2023-04-11
Published Online: 2023-04-19

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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