Next Article in Journal
Optimization and Performance Evaluation of Foam Acid Systems for Plugging Removal in Low Pressure Oil and Gas Reservoirs
Next Article in Special Issue
In Vitro Cytotoxicity Assessment of Abutilon pannosum Chloroform Fraction and Its Phytoconstituents Analysis
Previous Article in Journal
Process-Specific Topology Optimization Method Based on Laser-Based Additive Manufacturing of AlSi10Mg Components: Material Characterization and Evaluation
Previous Article in Special Issue
Protective Effect of Annona muricata Linn Fruit Pulp Lyophilized Powder against Paracetamol-Induced Redox Imbalance and Hepatotoxicity in Rats
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Processes
Volume 11
Issue 3
10.3390/pr11030650
processes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Phytochemical Composition and Insight into Antibacterial Potential of Origanum vulgare Essential Oil from Saudi Arabia Using In Vitro and In Silico Approaches

by
Omkulthom Al kamaly
1,
Ashwag S. Alanazi
1,
Raffaele Conte
2 and
Hamada Imtara
3,*
1
Department of Pharmaceutical Sciences, College of Pharmacy, Princess Nourah bint Abdulrahman University, P.O. Box 84428, Riyadh 11671, Saudi Arabia
2
Research Institute on Terrestrial Ecosystem (IRET), CNR, Via Pietro Castellino 111, 80131 Naples, Italy
3
Faculty of Arts and Sciences, Arab American University Palestine, Jenin P.O. Box 240, Palestine
*
Author to whom correspondence should be addressed.
Processes 2023, 11(3), 650; https://doi.org/10.3390/pr11030650
Submission received: 18 December 2022 / Revised: 9 February 2023 / Accepted: 14 February 2023 / Published: 21 February 2023
(This article belongs to the Special Issue Bioactive Compounds from Natural Plants)
Browse Figures
Versions Notes

Abstract

:
In Saudi Arabia, Origanum vulgare is widely disseminated. In the present work, we used GC-MS analysis to identify the components of Origanum vulgare essential oil. The disc diffusion assay was used to assess the essential oil’s in vitro antibacterial efficacy against Gram-positive and Gram-negative Staphylococcus aureus and Escherichia coli. The antimicrobial efficacy against many microbial proteins, including tyrosyl-tRNA synthetase (TyrRS), DNA gyrase, and dihydrofolate reductase (DHFR), was further evaluated using molecular docking. Eighteen compounds were identified using GC-MS analysis, which constituted 99.81% of the total essential oil content. Terpinen-4-ol (34.3%), Beta-Terpineol (16.96%), 3-Epimoretenol (11.84%), and Alpha-Terpineol (3.86%) were the main substances identified. According to the antibacterial investigation, the inhibition zone against Staphylococcus aureus was 8 mm and 6 mm against Escherichia coli. High affinities were found between 3-Epimoretenol and tyrosyl-tRNA synthetase (TyrRS) and dihydrofolate reductase (DHFR) compared to positive controls (Clorobiocin, SCHEMBL2181345); the affinity values were −8.3 Kcal/mol and −9.2, respectively. The results of the present study indicate that Origanum vulgare essential oil can be used as a nutraceutical to treat infectious diseases.

1. Introduction

Pharmacological industries have created new antibiotics during the past three decades [1]. However, these medicines have not been able to stop the spread of many bacteria with the genetic capacity to spread and develop drug resistance [2]. Therefore, infections with these bacteria are linked to substantial morbidity and death, particularly in individuals who are immunocompromised [3,4].
As a result, interest in alternative and natural antibacterial agents is developing. Alternative agents, such as essential oils (EOs) extracted from fragrant plants, have been suggested [5]. Numerous papers in the literature [6,7] discuss the antibacterial activity of essential oils against a variety of microorganisms. The main mechanisms and sites of action of the different constituents of essential oils are: alteration of the cell wall, degradation of the cytoplasmic membrane, alteration of membrane proteins, leakage of cellular contents, coagulation of the cytoplasm and exhaustion of the force of proton motion [8,9]. In addition, The fundamental benefit of using these natural compounds is that, unlike prolonged use of synthetic antibiotics, they do not increase antibiotic resistance [10]. In addition to having antimicrobial qualities, essential oils and their constituents have also been demonstrated to have antiviral, antimycotic, antitoxic, antiparasitic, and insecticidal qualities, which may be connected to how these substances work in plants [11]. These activities are due to the fact that essential oils contain a complex mixture of volatile compounds that are characterized by their low molecular weight and hydrophobicity. Among them are carbides (ex. limonene), alcohols (ex. geraniol), aldehydes (ex. cinnamaldehyde), ketones (ex. carvone), acids (ex. cinnamic acid), esters (ex. bornyl acetate), ethers (ex. 1,8-cineole), peroxides (ex. ascaridole), and phenols (ex. thymol and carvacrol) [12].
Origanum vulgare (oregano), one of numerous Origanum species from the Lamiaceae family are widely distributed. Oregano is a herbaceous or sub-woody plant at the base, 30 to 90 cm tall, with square stems bearing about forty branches with small, oval dark green leaves [13]. The inflorescences are spike-like and united in compound inflorescences. The calyx of oregano is tubular with five short teeth, bilabiate or not. The corolla is white, pink or purple [14]. The genus Origanum is mainly distributed around the Mediterranean basin. Of the Origanum species, 81% (35 out of 43 species) are found exclusively in the eastern Mediterranean, mainly in Turkey, Greece, and the Middle East. The species Origanum vulgare is also widely found in Eurasia and North Africa [15]. In this context, Origanum vulgare is one of the most common spices used in many foods. In addition, its oil and its compound are not limited to the use of aroma and flavor, but rather it has shown its effectiveness in many biological activities, including antioxidants (as a result of containing phenols, which play a role in neutralizing free radicals and also in the decomposition of peroxides) [16], antifungal [17], antibacterial [18], anticancer (explained by the potential of HE21 to inhibit the penetration of mutagens into cells; inactivating mutagens by trapping; directly capturing radicals produced by a mutagen or activating cellular antioxidant enzymes; to inhibit the metabolic conversion of cytochrome P450 by mutagens; or to activate the enzymatic process of detoxification of mutagens) [19], insecticidal [20], herbicidal [21], and nematicidal [22] properties. According to several studies, oregano essential oil has been shown to be analgesic, emmenagogue, decongestant, diaphoretic, vermicidal, antipyretic, anti-inflammatory, sedative, antimutagenic, larvicidal, laxative, nacritic, pectoral, tonic, and diuretic [23]. As a result, oregano essential oil is used in the composition of several pharmaceutical and parapharmaceutical preparations [24]. Its volatile oil contains up to 70% monoterpenoids (thymol and carvacrol) and sesquiterpenoids, dependent on geographic origin and plant developing stage [22,25].
The aim of the present study was to determine the main compounds in the essential oil of Origanum vulgare plant that was harvested from Saudi Arabia using GC-MS analysis and compare it with other studies, as well as investigate its antibacterial activity on antibiotic-resistant strains and clarify the antibacterial mechanism through in silico receptor-ligand docking study.

2. Materials and Methods

2.1. Chemicals

Mueller–Hinton agar and Mueller–Hinton broth were purchased from Biokar Diagnostics, Beauvais, France; dimethyl sulfoxide (DMSO) and Hexane were purchased from Sigma-Aldrich, Darmstadt, Germany.

2.2. Plant Material and Essential Oil Extraction

Origanum vulgare aerial portions were taken in March from Altaif city in Saudi Arabia’s southern area during the spring season (2022). The plant was harvested, dried in the shade at room temperature, and powdered. The essential oil of Origanum vulgare plant was extracted using a Clevenger-type hydrodistillation equipment for 3 h (100 g plant material in 1 L water). The essential oil produced was stored at +4 °C until tested and evaluated.

2.3. Gas Chromatographic Analysis

The essential oil of Origanum vulgare plant was diluted with hexane at a ratio of 1:10 [26]. The GC-MS analysis to determine the volatiles compounds was performed at the research center of College of Pharmacy, King Saud University, Riyadh, by using a Clarus 500 PerkinElmer (30 m × 0.25 mm ID × 1 µm of capillary column) gas chromatograph equipped and coupled to a mass detector Turbo Mass Gold according to method described by Khalil et al. [27]. The initial column temperature was programmed to 110 °C and maintained for 2 min. At an increment rate of 5 °C/min, the temperature was increased to 280 °C and kept for a period of 9 min. A volume of 1 μL of diluted oil was injected in temperature ensured as 250 °C with helium gas flow at rate 1 mL/min. The ionization voltage was 70 eV and the mass spectral scan range was set at 45–450 (m/z). By contrasting the mass spectra obtained with the mass spectra from the Adams Library [28] and the Wiley GC/MS Library (McLafferty and Stauffer, 1989) [29], the chemical makeup of the Origanum vulgare essential oil was determined.

2.4. Antimicrobial Activity Determination

2.4.1. Micro-Organism Tested

Gram-positive (Staphylococcus aureus: ATCC 25923) and Gram-negative (Escherichia coli: ATCC 25922) strains were used in this study. The strains are clinical isolates which are an important opportunistic pathogens in humans and isolated in Seattle, United States. The strains are commonly used in many studies as a quality control strains for antibiotics sensitivity and commercial products [30,31].

2.4.2. Preparation of Culture Media

Muller–Hinton agar medium (MH) was obtained by dissolving 38 g of Muller–Hinton agar medium in 1 L of distilled water (pH is 7.5 ± 0.2) and Muller–Hinton broth (21 g/L in distilled water). Each medium was sterilized in an autoclave at a temperature of 115 °C for 15 min.

2.4.3. Inoculum Preparation

Colonies were taken from 24 h cultures and suspended in sterile saline (0.9% NaCl). After vortexing for 15 s, the density of suspended was adjusted to a turbidity of 0.5 McFarland by using a spectrophotometer method. The final concentration of the inoculum was approximately 108 cfu/mL [32,33,34].

2.4.4. Disk Diffusion Assay

The antibacterial activity of Origanum vulgare essential oil was determined using the disc diffusion assay. A volume of 100 μL of suspensions (108 CFU/mL) in the growing phase was spread on Mueller–Hinton agar medium [35]. A volume of 20 μL of Origanum vulgare essential oil (dissolved in dimethyl sulfoxide (DMSO 2%); v:v) was added to 6 mm filter paper disk and placed on the inoculated Petri dishes. Then, the dishes were incubated at 37 °C for 24 h. The inhibition zone was measured to evaluate the antibacterial activity against the microorganism studied.

2.5. Molecular Docking

2.5.1. Preparation of the Ligand

From PubChem, we acquired the SDF format of beta terpineol (CID: 8748), terpinen-4-ol (CID: 11230), and 3-epimoretenol (CID: 604951). Using MyPol software, the SDF file was converted to PDB format and then to PDBQT by using AutoDock Tools v1.5.7. The nonpolar hydrogen atoms were combined, Gasteiger partial charges were added, and rotatable bonds were established for the finished ligand production.

2.5.2. Preparation of the Receptors

The PDB file for each receptor was downloaded from the Protein Data Bank website. The X-ray crystal structures of the receptors were chosen due to their completeness, resolution, and suitability for our research objective. Table 1 gives details about the chosen receptors. To prepare the receptors in the form of PDBQT, Discovery Studio Visualizer v19.1.0 was used at the beginning, which removes water molecules and heteroatoms. After that AutoDock Tools v1.5.6 was used to add Gasteiger charges and polar hydrogen atoms.

2.5.3. Docking Simulation

To run the docking simulations between receptors and molecules that used in this study, we used a AutoDock Vina 1.1.2 software.

2.5.4. Docking Validation Protocol

To examine the accuracy of the molecular docking algorithms, we compared the active sites experimentally produced by the X-ray diffraction method to the results of intermolecular interactions using the same previous methodology. Next, we applied the re-docking process, based on the overlay of the co-crystallized ligand bound to each target protein (coded 1JIJ, 1KZN, and 2FYV) on the docked co-crystallized ligand using the molecular docking simulation [36,37].

3. Results and Discussion

3.1. Phytochemical Analysis of Origanum vulgare

The Origanum vulgare essential oil was examined using a GC/MS system and the chromatogram results present in Figure 1.
The chemical composition of the essential oil of Origanum vulgare plant was analyzed by the gas chromatography–mass spectrometry (GC-MS) method. Table 2 and Figure 2 lists the elements along with their respective proportions (% of Area). A total of 18 compounds representing 99.98% of the total content were determined by GC/MS. The principal components of the essential oil of Origanum vulgare were terpinen-4-ol (43.32%), beta-terpineol (16.96%), 3-epimoretenol (11.84%), gamma-terpinen (6.35%), and alpha-terpieol (3.86%). These compounds constituted 82.33% of the total content, while the rest of the compounds constituted 17.65%. It should be noted that terpinen-4-ol was the higher content in this essential oil with an important concentration compared to the others. The results in the present work are consistent with those conducted by Busatta et al., which showed that terpinen-4-ol is the main compound with a ratio of 21.43% [38]. However, Imtara et al. found that the main constituents in Origanum vulgare essential oil from Morocco were carvacrol (48.38%), thymol (26.55%), and γ-terpinene (7.90%) [26]. In the same country, Hayani et al. identified thymol (38.59%), carvacrol (26.65%), and o-cymene (14.33%) as the main compounds in this essential oil [39]. Similarly, Origanum vulgare essential oils from Italy are characterized by a high percentage of thymol, carvacrol, linalyl acetate, and γ-terpinene in greater quantities [40]. However, Portuguese researchers found that carvacrol, thymol, γ-terpinene, and β-fenchyl alcohol are considered the main molecules present in Origanum vulgare essential oil [41]. In 2018, a study conducted by Stešević et al. on Origanum vulgare essential oil from Montenegro showed that β-caryophyllene, linalyl acetate, and α-terpineol are the main compounds [42]. However, the variation seen in the percentages of the main components of the essential oils analyzed in this and several studies could be attributed to the origin of the plant, different environmental influences (geographical, seasonal and climatic conditions, sunlight, and salinity, as well as the effect of crop, and time of harvest), genetic background, and the extraction method of the plants [43,44,45]. As a result, the influence of these factors on biosynthetic pathways causes differences in the qualitative and quantitative terms of the characteristic majority chemicals, which result in the existence of several chemotypes distinguishing essential oils from various origins [46].

3.2. Antimicrobial Activity

The disc diffusion method is acknowledged as a practical semi-quantitative approach for assessing the susceptibility of bacteria to various chemicals [38,47]. By examining the existence of inhibitory zone values, the antibacterial activity of Origanum vulgare essential oil against the pathogens taken into account in this investigation was determined. The results show that the greatest inhibition zones (8 mm) and the highest activity were seen against Staphylococcus aureus (Table 3). However, the essential oil antibacterial activity was effective against Escherichia coli as well (6 mm). These results support Gram-positive bacteria being more sensitive than Gram-negative bacteria [48]. Also shown in Table 3, it was observed that Staphylococcus aureus strain was resistant to two types of antibiotics (Penicillin G and Fusidic acid), while Escherichia coli strain was resistant to five antibiotics, namely, ciprofloxacin, trimethoprim/sulfamethoxazole, cefotaxime, amoxicillin, and cefuroxime. The essential oils are characterized mainly by their hydrophobicity. This allows their solubilization in the membranes, which causes a destabilization of the structure and an increase in the membrane permeability [49]. These changes lead to leakage of ions and intracellular compounds. Loss of cytoplasmic material results in cell bursting [50]. The mode of action of certain antibacterial molecules has been described in the literature. Chemical compounds of essential oils known for their antimicrobial effectiveness and broad spectrum are phenols (thymol, carvacrol, and eugenol), alcohols, (α-terpineol, terpinen-4-ol, and linalool), aldehydes, ketones, and, more rarely, carbides [51]. Terpinen-4-ol is the main compound identified in the present work and this compound is known for its antibacterial activity. This compound acts on many bacterial species, including Gram-positive and Gram-negative bacteria, and is highly effective against MRSA (Methicillin-resistant Staphylococcus aureus) infection [52]. In addition, according to Lambert et al., the combination of the main active compounds would act synergistically by potentiating the antimicrobial action of the essential oil [53].
A study was carried out by Sahin et al. on 24 bacteria, including two types of Staphylococcus aureus, one of which was found to be resistant to the antibacterial activity of Origanum vulgare essential oil, and the other had a diameter of inhibition 10 mm, which is consistent with our results. Another study conducted by Busatta et al. on nine types of bacteria showed that all of these species are sensitive to the antibacterial effect of Origanum vulgare essential oil, with the exception of Pseudomonas aeruginosa [38]. In addition, the inhibition zone of Origanum vulgare essential oil in his study on Escherichia coli was 17.33 mm and on Staphylococcus aureus was 26.8 mm and these results are better than those in our study. The reason for this difference may be due to the fact that Origanum oil, in a Busatta et al. study, contained carvacrol and thymol compounds, which is known to antibacterial activity [54,55]. A study carried out on Bacillus cereus has elucidated the mode of action of carvacrol. This compound crosses the lipid bilayer and is localized between the chains of fatty acids. This deformation of the structure increases the membrane fluidity, leading to a modification of the passive permeability. A decrease in intracellular ATP was noted in bacteria exposed to carvacrol, as well as a decrease in membrane potential [8]. Concerning thymol mechanism action, a study showed that thymol alters membrane permeability, causes loss of intracellular substances, and interacts with intracellular sites [8]. However, it is important to note that several factors can affect the diameter of the inhibition zones of essential oils among them the diffusion and viscosity of the essential oils [8]. In 2018, Hamada et al. conducted a study on the synergistic effect of Origanum vulgare essential oil with different types of honey of different plant origin. The study showed that when mixing the oil with honey, it enhances the antibacterial activity of honey. At the same time, this mixture reduces the toxicity of essential oils [31].

3.3. Docking Validation

The results presented in Figure 3 demonstrate that ASP195, ASP40, Tyr170, GLN174, ASP80, ASP177, and TYR36 amino acids residues are the active sites of 1JIJ.pdb protein in A-chain. Two of these intermolecular interactions are obtained computationally using molecular docking simulation as ASP40 and ASP195 amino acids residues. In addition, the result of superposition show that root mean square deviation (RMSD equal to 1.375 Å) is minimal and less the threshold 2 Å.
The results presented in Figure 4, show that ASN46, ASP73, and ARG136 amino acids residues, are the active sites of 1KZN.pdb protein in A-chain. ASN46 amino acid is one of these three intermolecular interactions, which is produced computationally using molecular docking simulation. In addition, the result of superposition shows that root mean square deviation (RMSD equal to 1.987 Å) is minimal and below the threshold 2 Å.
The results presented in Figure 5 show that LEU5, PHE92, and ASP27 amino acids residues are the active sites of 2FYV.pdb protein in X-chain. ASP27 and PH92 amino acids residues are two of these three intermolecular interactions, which are produced computationally using molecular docking simulation. In addition, the result of superposition show that root mean square deviation (RMSD equal to 1.948 Å) is minimal and below the threshold 2 Å. Consequently, the process of molecular docking is successfully validated.

3.4. Molecular Docking

Based on the results of the GC/MS, the major abundant compounds (Beta-terpineol, Terpinen-4-ol and 3-epimoretenol) were selected to clarify their role in antibacterial activity by conducting a molecular docking analysis between these compounds and the receptors that were selected based on several studies [56,57,58]. The results of affinities between the compounds and receptors are shown in the Table 4. In addition, chlorobiocin and SCHEMBL2181345 were used as positive controls to evaluate the outcomes of the molecules with receptors.
The 3-epimoretenol and beta-terpineol compounds showed good affinities with the tyrosyl-tRNA synthetase (TyrRS) receptors with values of −8.3 Kcal/mol and −4.4 Kcal/mol, respectively, while there was no binding between terpinen-4-ol and the same receptor. (Figure 6). In addition, the value of the affinity between the positive control (Clorobiocin) and the tyrosyl-tRNA synthetase (TyrRS) was −8.2 Kcal/mol. This indicates that the interaction between the 3-epimoretenol compound and the tyrosyl-tRNA synthetase (TyrRS) receptor is almost similar to the interaction between the Clorobiocin and the tyrosyl-tRNA synthetase (TyrRS) receptor.
Among the tested compounds, 3-epimoretenol had the best affinity value with DNA gyrase receptor (−7.4 Kcal/mol), but it was less than that between the DNA gyrase receptor and the Clorobiocin (−9.1 Kcal/mol). Beta-terpineol had the lowest affinity value, which was −6.1 Kcal/mol (Figure 7). While the value of the affinity between terpinen-4-ol and DNA gyrase receptor is −6.6 Kcal/mol.
With regard to the dihydrofolate reductase (DHFR) receptor, it interacted with the three tested compounds; the highest value was for the 3-epimoretenol compound with a value of −9.2 Kcal/mol (Figure 8), followed by the terpinen-4-ol and beta-terpineol compounds with values of −6.1 Kcal/mol and −5.7 Kcal/mol, respectively. The value of the affinity between the SCHEMBL2181345 and the dihydrofolate reductase (DHFR) receptor was −6.3 Kcal/mol, which is less than that found with 3-epimoretenol. This indicates that the interaction between the 3-epimoretenol compound and the dihydrofolate reductase (DHFR) receptor is better than the interaction between the SCHEMBL2181345 and the dihydrofolate reductase (DHFR) receptor.

4. Conclusions

The aim of the present study was to determine the chemical compounds and antibacterial activity of Origanum vulgare essential oil. The GC-MS results in the present work showed that terpinen-4-ol, beta-terpineol and 3-epimoretenol are the main compounds of Origanum vulgare essential oil. The results of the antibacterial activity have indicated that Origanum vulgare essential oil can be considered a potent against the antibiotic-resistant bacteria that were used in the present study. In addition, the results of molecular docking showed that among the three main compounds, 3-epimoretenol had the best interaction with the tyrosyl-tRNA synthetase (TyrRS), DNA gyrase, and dihydrofolate reductase (DHFR) receptors followed by beta-terpineol, and this confirms the antibacterial activity of this essential oil. According to the findings, the present study indicates that Origanum vulgare essential oil can be used as a nutraceutical to treat infectious diseases.

Author Contributions

Conceptualization, O.A.k. and H.I.; methodology, O.A.k., H.I. and A.S.A.; formal analysis, O.A.k. and R.C.; resources, O.A.k. and A.S.A.; data curation, H.I.; writing—original draft preparation, O.A.k. and H.I.; writing—review and editing, R.C. and A.S.A. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Deanship of Scientific Research at Princess Nourah bint Abdulrahman University, through the Research Groups Program Grant no (RGP-1443-0043).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors are thankful to the Scientific Research at Princess Nourah bint Abdulrahman University for the support of this work through the Research Groups Program Grant no (RGP-1443-0043).

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviation

GC-MSGas chromatography–mass spectrometry
TyrRSTyrosyl-tRNA synthetase
DHFRDihydrofolate reductase
EOEssential oil
DMSODimethyl sulfoxide
CFUColony forming unit
PDBProtein data bank
RTRetention time
mmMillimeter

References

  1. Aljuraifani, A. Antimicrobial Activity of Some Medicinal Plants Used in Saudi Arabia. Can. J. Pure Appl. Sci. 2011, 5, 1509–1512. [Google Scholar]
  2. Cohen, M.L. Epidemiology of Drug Resistance: Implications for a Post—Antimicrobial Era. Science 1992, 257, 1050–1055. [Google Scholar] [CrossRef] [PubMed]
  3. Del Toro, M.D.; Rodríguez-Baño, J.; Martínez-Martínez, L.; Pascual, A.; Pérez-Canoa, R.; Perea, E.J.; Muniain, M.A. Epidemiology, clinical features and prognosis of infections due to Stenotrophomonas maltophilia. Enferm. Infecc. Microbiol. Clin. 2006, 24, 4–9. [Google Scholar] [CrossRef] [PubMed]
  4. Driscoll, J.A.; Brody, S.L.; Kollef, M.H. The Epidemiology, Pathogenesis and Treatment of Pseudomonas Aeruginosa Infections. Drugs 2007, 67, 351–368. [Google Scholar] [CrossRef] [PubMed]
  5. Kordali, S.; Cakir, A.; Ozer, H.; Cakmakci, R.; Kesdek, M.; Mete, E. Antifungal, Phytotoxic and Insecticidal Properties of Essential Oil Isolated from Turkish Origanum Acutidens and Its Three Components, Carvacrol, Thymol and p-Cymene. Bioresour. Technol. 2008, 99, 8788–8795. [Google Scholar] [CrossRef] [PubMed]
  6. Longaray Delamare, A.P.; Moschen-Pistorello, I.T.; Artico, L.; Atti-Serafini, L.; Echeverrigaray, S. Antibacterial Activity of the Essential Oils of Salvia Officinalis L. and Salvia Triloba L. Cultivated in South Brazil. Food Chem. 2007, 100, 603–608. [Google Scholar] [CrossRef]
  7. Seydim, A.C.; Sarikus, G. Antimicrobial Activity of Whey Protein Based Edible Films Incorporated with Oregano, Rosemary and Garlic Essential Oils. Food Res. Int. 2006, 39, 639–644. [Google Scholar] [CrossRef]
  8. Imtara, H.F.I. Aromiels Du Maroc et de Palestine. Ph.D. Thesis, University of Sidi Mohamed Ben Abdullah, Fez, Morocco, 2018. [Google Scholar]
  9. Kalemba, D.; Kunicka, A. Antibacterial and Antifungal Properties of Essential Oils. Curr. Med. Chem. 2003, 10, 813–829. [Google Scholar] [CrossRef]
  10. Högberg, L.D.; Heddini, A.; Cars, O. The Global Need for Effective Antibiotics: Challenges and Recent Advances. Trends Pharmacol. Sci. 2010, 31, 509–515. [Google Scholar] [CrossRef]
  11. Burt, S. Essential Oils: Their Antibacterial Properties and Potential Applications in Foods—A Review. Int. J. Food Microbiol. 2004, 94, 223–253. [Google Scholar] [CrossRef]
  12. Couic-Marinier, F.; Lobstein, A. Composition chimique des huiles essentielles. Actual. Pharm. 2013, 52, 22–25. [Google Scholar] [CrossRef]
  13. Manuel des Corps Gras: 2 Volumes Inséparables KARLESKIND Alain. Available online: https://www.lavoisier.fr/livre/agro-alimentaire/manuel-des-corps-gras-2-volumes-inseparables/karleskind/descriptif-9782852066625 (accessed on 26 January 2023).
  14. Quézel, P.; Santa, S. Nouvelle Flore de L’algérie et des Régions Désertiques Méridionales; Editions du Centre National de la Recherche Scientifique: Paris, France, 1962. [Google Scholar]
  15. Kintzios, S.E. (Ed.) Oregano: The Genera Origanum and Lippia; CRC Press: London, UK, 2004; ISBN 978-0-429-21897-2. [Google Scholar]
  16. Yan, F.; Azizi, A.; Janke, S.; Schwarz, M.; Zeller, S.; Honermeier, B. Antioxidant Capacity Variation in the Oregano (Origanum Vulgare L.) Collection of the German National Genebank. Ind. Crops Prod. 2016, 92, 19–25. [Google Scholar] [CrossRef]
  17. Soković, M.; Glamočlija, J.; Marin, P.D.; Brkić, D.; van Griensven, L.J.L.D. Antibacterial Effects of the Essential Oils of Commonly Consumed Medicinal Herbs Using an in Vitro Model. Molecules 2010, 15, 7532–7546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. De Falco, E.; Mancini, E.; Roscigno, G.; Mignola, E.; Taglialatela-Scafati, O.; Senatore, F. Chemical Composition and Biological Activity of Essential Oils of Origanum Vulgare L. Subsp. Vulgare L. under Different Growth Conditions. Molecules 2013, 18, 14948–14960. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Elshafie, H.S.; Armentano, M.F.; Carmosino, M.; Bufo, S.A.; De Feo, V.; Camele, I. Cytotoxic Activity of Origanum Vulgare L. on Hepatocellular Carcinoma Cell Line HepG2 and Evaluation of Its Biological Activity. Molecules 2017, 22, 1435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Abdelgaleil, S.A.M.; Mohamed, M.I.E.; Shawir, M.S.; Abou-Taleb, H.K. Chemical Composition, Insecticidal and Biochemical Effects of Essential Oils of Different Plant Species from Northern Egypt on the Rice Weevil, Sitophilus Oryzae L. J. Pest. Sci. 2016, 89, 219–229. [Google Scholar] [CrossRef]
  21. De Mastro, G.; Fracchiolla, M.; Verdini, L.; Montemurro, P. Oregano and Its Potential Use as Bioherbicide. In Proceedings of the I International Symposium on the Labiatae: Advances in Production, Biotechnology and Utilisation, Sanremo, Italy, 22 February 2006; Volume 723. [Google Scholar]
  22. Barbosa, P.; Faria, J.M.S.; Mendes, M.D.; Dias, L.S.; Tinoco, M.T.; Barroso, J.G.; Pedro, L.G.; Figueiredo, A.C.; Mota, M. Bioassays against Pinewood Nematode: Assessment of a Suitable Dilution Agent and Screening for Bioactive Essential Oils. Molecules 2012, 17, 12312–12329. [Google Scholar] [CrossRef] [Green Version]
  23. Dhifi, W.; Bellili, S.; Jazi, S.; Bahloul, N.; Mnif, W. Essential Oils’ Chemical Characterization and Investigation of Some Biological Activities: A Critical Review. Medicines 2016, 3, 25. [Google Scholar] [CrossRef] [Green Version]
  24. Rostro-Alanis, M.d.J.; Báez-González, J.; Torres-Alvarez, C.; Parra-Saldívar, R.; Rodriguez-Rodriguez, J.; Castillo, S. Chemical Composition and Biological Activities of Oregano Essential Oil and Its Fractions Obtained by Vacuum Distillation. Molecules 2019, 24, 1904. [Google Scholar] [CrossRef] [Green Version]
  25. Stoilova, I.; Bail, S.; Buchbauer, G.; Krastanov, A.; Stoyanova, A.; Schmidt, E.; Jirovetz, L. Chemical Composition, Olfactory Evaluation and Antioxidant Effects of an Essential Oil of Origanum Vulgare L. from Bosnia. Nat. Prod. Commun. 2008, 3, 1934578X0800300702. [Google Scholar] [CrossRef] [Green Version]
  26. Imtara, H.; Al-Waili, N.; Aboulghazi, A.; Abdellaoui, A.; Al-Waili, T.; Lyoussi, B. Chemical Composition and Antioxidant Content of Thymus Vulgaris Honey and Origanum Vulgare Essential Oil; Their Effect on Carbon Tetrachloride-Induced Toxicity. Vet. World 2021, 14, 292–301. [Google Scholar] [CrossRef]
  27. Khalil, M.I.M.; Ibrahim, M.M.; El-Gaaly, G.A.; Sultan, A.S. Trigonella Foenum (Fenugreek) Induced Apoptosis in Hepatocellular Carcinoma Cell Line, HepG2, Mediated by Upregulation of P53 and Proliferating Cell Nuclear Antigen. BioMed Res. Int. 2015, 2015, 914645. [Google Scholar] [CrossRef] [Green Version]
  28. Sparkman, O.D. Identification of Essential Oil Components by Gas Chromatography/Quadrupole Mass Spectroscopy Robert P. Adams. J. Am. Soc. Mass Spectrom. 2005, 16, 1902–1903. [Google Scholar] [CrossRef] [Green Version]
  29. Wiley/NBS. Registry of Mass Spectral Data. Available online: https://analyticalscience.wiley.com/do/10.1002/sepspec.9780471628866 (accessed on 25 November 2022).
  30. Treangen, T.J.; Maybank, R.A.; Enke, S.; Friss, M.B.; Diviak, L.F.; Karaolis, D.K.R.; Koren, S.; Ondov, B.; Phillippy, A.M.; Bergman, N.H.; et al. Complete Genome Sequence of the Quality Control Strain Staphylococcus Aureus Subsp. Aureus ATCC 25923. Genome Announc. 2014, 2, e01110-14. [Google Scholar] [CrossRef] [Green Version]
  31. Minogue, T.D.; Daligault, H.A.; Davenport, K.W.; Bishop-Lilly, K.A.; Broomall, S.M.; Bruce, D.C.; Chain, P.S.; Chertkov, O.; Coyne, S.R.; Freitas, T.; et al. Complete Genome Assembly of Escherichia Coli ATCC 25922, a Serotype O6 Reference Strain. Genome Announc. 2014, 2, e00969-14. [Google Scholar] [CrossRef] [Green Version]
  32. Imtara, H.; Elamine, Y.; Lyoussi, B. Honey Antibacterial Effect Boosting Using Origanum Vulgare L. Essential Oil. Evid.-Based Complement. Altern. Med. 2018, 2018, e7842583. [Google Scholar] [CrossRef] [Green Version]
  33. Daraghmeh, J.; Imtara, H. In Vitro Evaluation of Palestinian Propolis as a Natural Product with Antioxidant Properties and Antimicrobial Activity against Multidrug-Resistant Clinical Isolates. J. Food Qual. 2020, 2020, e8861395. [Google Scholar] [CrossRef]
  34. Sadeq, O.; Mechchate, H.; Es-safi, I.; Bouhrim, M.; Jawhari, F.Z.; Ouassou, H.; Kharchoufa, L.; AlZain, M.N.; Alzamel, N.M.; Al kamaly, M.O.; et al. Phytochemical Screening, Antioxidant and Antibacterial Activities of Pollen Extracts from Micromeria Fruticosa, Achillea Fragrantissima, and Phoenix Dactylifera. Plants 2021, 10, 676. [Google Scholar] [CrossRef] [PubMed]
  35. Aref, H.L.; Karima, B.H.S.; Fekih, A.; Chemli, R.; Mars, M.; Aouni, M.; Chaumon, J.P.; Said, K. Variability in Antimicrobial Activity of Latex from Two Varieties of Ficus Carica. AJMR 2011, 5, 1361–1367. [Google Scholar] [CrossRef]
  36. El Fadili, M.; Er-rajy, M.; Imtara, H.; Kara, M.; Zarougui, S.; Altwaijry, N.; Al Kamaly, O.; Al Sfouk, A.; Elhallaoui, M. 3D-QSAR, ADME-Tox In Silico Prediction and Molecular Docking Studies for Modeling the Analgesic Activity against Neuropathic Pain of Novel NR2B-Selective NMDA Receptor Antagonists. Processes 2022, 10, 1462. [Google Scholar] [CrossRef]
  37. El Fadili, M.; Er-Rajy, M.; Kara, M.; Assouguem, A.; Belhassan, A.; Alotaibi, A.; Mrabti, N.N.; Fidan, H.; Ullah, R.; Ercisli, S.; et al. QSAR, ADMET In Silico Pharmacokinetics, Molecular Docking and Molecular Dynamics Studies of Novel Bicyclo (Aryl Methyl) Benzamides as Potent GlyT1 Inhibitors for the Treatment of Schizophrenia. Pharmaceuticals 2022, 15, 670. [Google Scholar] [CrossRef] [PubMed]
  38. Busatta, C.; Mossi, A.J.; Rodrigues, M.R.A.; Cansian, R.L.; Oliveira, J.V. De Evaluation of Origanum Vulgare Essential Oil as Antimicrobial Agent in Sausage. Braz. J. Microbiol. 2007, 38, 610–616. [Google Scholar] [CrossRef] [Green Version]
  39. Hayani, M.; Bencheikh, N.; Ailli, A.; Bouhrim, M.; Elbouzidi, A.; Ouassou, H.; Kharchoufa, L.; Baraich, A.; Atbir, A.; Ayyad, F.Z.; et al. Quality Control, Phytochemical Profile, and Antibacterial Effect of Origanum Compactum Benth. Essential Oil from Morocco. IJPB 2022, 13, 546–560. [Google Scholar] [CrossRef]
  40. Mastro, G.D.; Tarraf, W.; Verdini, L.; Brunetti, G.; Ruta, C. Essential Oil Diversity of Origanum Vulgare L. Populations from Southern Italy. Food Chem. 2017, 235, 1–6. [Google Scholar] [CrossRef]
  41. Teixeira, B.; Marques, A.; Ramos, C.; Serrano, C.; Matos, O.; Neng, N.R.; Nogueira, J.M.F.; Saraiva, J.A.; Nunes, M.L. Chemical Composition and Bioactivity of Different Oregano (Origanum Vulgare) Extracts and Essential Oil. J. Sci. Food Agric. 2013, 93, 2707–2714. [Google Scholar] [CrossRef] [PubMed]
  42. Stešević, D.; Jaćimović, Ž.; Šatović, Z.; Šapčanin, A.; Jančan, G.; Kosović, M.; Damjanović-Vratnica, B. Chemical Characterization of Wild Growing Origanum Vulgare Populations in Montenegro. Nat. Prod. Commun. 2018, 13, 1934578X1801301031. [Google Scholar] [CrossRef] [Green Version]
  43. Perry, N.B.; Anderson, R.E.; Brennan, N.J.; Douglas, M.H.; Heaney, A.J.; McGimpsey, J.A.; Smallfield, B.M. Essential Oils from Dalmatian Sage (Salvia Officinalis L.): Variations among Individuals, Plant Parts, Seasons, and Sites. J. Agric. Food Chem. 1999, 47, 2048–2054. [Google Scholar] [CrossRef]
  44. Desam, N.R.; Al-Rajab, A.J.; Sharma, M.; Mylabathula, M.M.; Gowkanapalli, R.R.; Albratty, M. Chemical Constituents, in Vitro Antibacterial and Antifungal Activity of Mentha×Piperita L. (Peppermint) Essential Oils. J. King Saud. Univ.-Sci. 2019, 31, 528–533. [Google Scholar] [CrossRef]
  45. Lombrea, A.; Antal, D.; Ardelean, F.; Avram, S.; Pavel, I.Z.; Vlaia, L.; Mut, A.-M.; Diaconeasa, Z.; Dehelean, C.A.; Soica, C.; et al. A Recent Insight Regarding the Phytochemistry and Bioactivity of Origanum Vulgare L. Essential Oil. Int. J. Mol. Sci. 2020, 21, 9653. [Google Scholar] [CrossRef]
  46. Ballester-Costa, C.; Sendra, E.; Fernández-López, J.; Pérez-Álvarez, J.A.; Viuda-Martos, M. Assessment of Antioxidant and Antibacterial Properties on Meat Homogenates of Essential Oils Obtained from Four Thymus Species Achieved from Organic Growth. Foods 2017, 6, 59. [Google Scholar] [CrossRef] [Green Version]
  47. Gajic, I.; Kabic, J.; Kekic, D.; Jovicevic, M.; Milenkovic, M.; Mitic Culafic, D.; Trudic, A.; Ranin, L.; Opavski, N. Antimicrobial Susceptibility Testing: A Comprehensive Review of Currently Used Methods. Antibiotics 2022, 11, 427. [Google Scholar] [CrossRef]
  48. Breijyeh, Z.; Jubeh, B.; Karaman, R. Resistance of Gram-Negative Bacteria to Current Antibacterial Agents and Approaches to Resolve It. Molecules 2020, 25, 1340. [Google Scholar] [CrossRef] [Green Version]
  49. Sikkema, J.; de Bont, J.A.; Poolman, B. Interactions of Cyclic Hydrocarbons with Biological Membranes. J. Biol. Chem. 1994, 269, 8022–8028. [Google Scholar] [CrossRef]
  50. Carson, C.F.; Mee, B.J.; Riley, T.V. Mechanism of Action of Melaleuca Alternifolia (Tea Tree) Oil on Staphylococcus Aureus Determined by Time-Kill, Lysis, Leakage, and Salt Tolerance Assays and Electron Microscopy. Antimicrob. Agents Chemother. 2002, 46, 1914–1920. [Google Scholar] [CrossRef] [Green Version]
  51. Dorman, H.J.; Deans, S.G. Antimicrobial Agents from Plants: Antibacterial Activity of Plant Volatile Oils. J. Appl. Microbiol. 2000, 88, 308–316. [Google Scholar] [CrossRef]
  52. Cordeiro, L.; Figueiredo, P.; Souza, H.; Sousa, A.; Andrade-Júnior, F.; Medeiros, D.; Nóbrega, J.; Silva, D.; Martins, E.; Barbosa-Filho, J.; et al. Terpinen-4-Ol as an Antibacterial and Antibiofilm Agent against Staphylococcus Aureus. Int. J. Mol. Sci. 2020, 21, 4531. [Google Scholar] [CrossRef] [PubMed]
  53. Lambert, R.J.; Skandamis, P.N.; Coote, P.J.; Nychas, G.J. A Study of the Minimum Inhibitory Concentration and Mode of Action of Oregano Essential Oil, Thymol and Carvacrol. J. Appl. Microbiol. 2001, 91, 453–462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Rúa, J.; del Valle, P.; de Arriaga, D.; Fernández-Álvarez, L.; García-Armesto, M.R. Combination of Carvacrol and Thymol: Antimicrobial Activity Against Staphylococcus Aureus and Antioxidant Activity. Foodborne Pathog. Dis. 2019, 16, 622–629. [Google Scholar] [CrossRef] [PubMed]
  55. Saghrouchni, H.; El Barnossi, A.; Salamatullah, A.M.; Bourhia, M.; Alzahrani, A.; Alkaltham, M.S.; Alyahya, H.K.; Tahiri, N.E.H.; Imtara, H.; Var, I. Carvacrol: A Promising Environmentally Friendly Agent to Fight Seeds Damping-Off Diseases Induced by Fungal Species. Agronomy 2021, 11, 985. [Google Scholar] [CrossRef]
  56. He, J.; Qiao, W.; An, Q.; Yang, T.; Luo, Y. Dihydrofolate Reductase Inhibitors for Use as Antimicrobial Agents. Eur. J. Med. Chem. 2020, 195, 112268. [Google Scholar] [CrossRef] [PubMed]
  57. Eakin, A.E.; Green, O.; Hales, N.; Walkup, G.K.; Bist, S.; Singh, A.; Mullen, G.; Bryant, J.; Embrey, K.; Gao, N.; et al. Pyrrolamide DNA Gyrase Inhibitors: Fragment-Based Nuclear Magnetic Resonance Screening to Identify Antibacterial Agents. Antimicrob. Agents Chemother. 2012, 56, 1240–1246. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. J, S.; Pc, L.; Hl, Z. Tyrosyl-TRNA Synthetase Inhibitors: A Patent Review. Expert Opin. Ther. Pat. 2017, 27. [Google Scholar] [CrossRef]
Processes 11 00650 g001 550
Figure 1. GC-MS chromatogram of Origanum vulgare.
Figure 1. GC-MS chromatogram of Origanum vulgare.
Processes 11 00650 g001
Processes 11 00650 g002 550
Figure 2. The chemical structures of compounds identified in Origanum vulgare essential oil.
Figure 2. The chemical structures of compounds identified in Origanum vulgare essential oil.
Processes 11 00650 g002
Processes 11 00650 g003 550
Figure 3. The results of intermolecular interaction between 1JIJ.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.375 Å (C).
Figure 3. The results of intermolecular interaction between 1JIJ.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.375 Å (C).
Processes 11 00650 g003
Processes 11 00650 g004 550
Figure 4. The results of intermolecular interaction between 1KZN.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.987 Å (C).
Figure 4. The results of intermolecular interaction between 1KZN.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.987 Å (C).
Processes 11 00650 g004
Processes 11 00650 g005 550
Figure 5. The results of intermolecular interaction between 1JIJ.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.948 Å (C).
Figure 5. The results of intermolecular interaction between 1JIJ.pdb protein and co-crystallized ligand, which are produced computationally (A) and experimentally (B), and the result of superposition pose with RMSD of 1.948 Å (C).
Processes 11 00650 g005
Processes 11 00650 g006 550
Figure 6. The interaction between tyrosyl-tRNA synthetase (TyrRS) and tested compounds. (A): Beta-terpineol; (B): 3-epimoretenol.
Figure 6. The interaction between tyrosyl-tRNA synthetase (TyrRS) and tested compounds. (A): Beta-terpineol; (B): 3-epimoretenol.
Processes 11 00650 g006
Processes 11 00650 g007 550
Figure 7. The interaction between DNA gyrase and tested compounds. (A): Beta-terpineol; (B): Terpinen-4-ol (C): 3-epimoretenol.
Figure 7. The interaction between DNA gyrase and tested compounds. (A): Beta-terpineol; (B): Terpinen-4-ol (C): 3-epimoretenol.
Processes 11 00650 g007
Processes 11 00650 g008 550
Figure 8. The interaction between dihydrofolate reductase (DHFR) and tested compounds. (A): Beta-terpineol; (B): Terpinen-4-ol (C): 3-epimoretenol.
Figure 8. The interaction between dihydrofolate reductase (DHFR) and tested compounds. (A): Beta-terpineol; (B): Terpinen-4-ol (C): 3-epimoretenol.
Processes 11 00650 g008
Table
Table 1. Description of the studied receptors.
Table 1. Description of the studied receptors.
ReceptorsIDClass
TyrRS1jijLigase
DNA gyrase1KZNIsomerase
DHFR3fyvOxidoreductase
TyrRS: tyrosyl-tRNA synthetase, DHFR: dihydrofolate reductase.
Table
Table 2. The chemical composition of Origanum vulgare essential oil using GC-MS analysis.
Table 2. The chemical composition of Origanum vulgare essential oil using GC-MS analysis.
#Compound NameChemical FormulaMolecular Weight (g/mol)RT (min)Area %
1Beta-TerpineneC10H16136.236.732.94
2Beta-MyrceneC10H16136.236.990.53
32-CareneC10H16136.237.422.29
4O-CymeneC10H14134.227.552.21
5Gamma-TerpineneC10H16136.238.086.36
6TerpinoleneC10H16136.238.551.31
7Beta-TerpineolC10H18O154.258.7516.97
82-Cyclohexen-1-ol,
1-methyl-4-(1-methylethyl)-,
trans-		C10H18O154.259.11.71
9Cyclohexanol,
2-methyl-5-(1-methylethenyl)-,
(1α,2α,5β)-		C10H18O154.259.380.85
10Terpinen-4-olC10H18O154.259.9943.32
11Alpha-TerpineolC10H18O154.2510.163.86
12Linalyl anthranilateC17H23NO2273.3710.980.48
13CaryophylleneC15H24204.3513.361.65
141,5-Heptadiene,
2,5-dimethyl-3-methylene-		C10H16136.2314.330.53
159,17-Octadecadienal, (Z)-C18H32O264.421.030.48
163-EpimoretenolC30H50O426.725.0711.84
17(8S,14) Cedran-diol,C15H26O238.427.931.43
18Cycloeucalenyl acetateC32H52O2468.828.331.22
RT: Retention time.
Table
Table 3. Inhibition zone generated by Origanum vulgare essential oil on bacteria studied and list of antibiotics that bacteria have resisted.
Table 3. Inhibition zone generated by Origanum vulgare essential oil on bacteria studied and list of antibiotics that bacteria have resisted.
Escherichia coliStaphylococcus aureus
Origanum vulgare essential oil6 mm8 mm
DMSO--
Antibiotic resistantCXM, AML, CTX, SXT, CIPPG, FA
-: not active, mm: millimeter, DMSO: Dimethyl sulfoxide, PG: Penicillin G, FA: Fusidic acid, CXM: Cefuroxime, AML: Amoxicillin, CTX: Cefotaxime, SXT: Trimethoprim/sulfamethoxazole, CIP: Ciprofloxacin.
Table
Table 4. Affinity results of the selected receptors and molecules.
Table 4. Affinity results of the selected receptors and molecules.
Affinities (Kcal/mol)
TyrRSDNA GyraseDHFR
Beta-terpineol−4.4−6.1−5.7
Terpinen-4-olNo interaction−6.6−6.1
3-epimoretenol−8.3−7.4−9.2
Clorobiocin−8.2−9.1_
SCHEMBL2181345__−6.3
TyrRS: Tyrosyl-tRNA synthetase; DHFR: dihydrofolate reductase; _: no affinity.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Al kamaly, O.; Alanazi, A.S.; Conte, R.; Imtara, H. Phytochemical Composition and Insight into Antibacterial Potential of Origanum vulgare Essential Oil from Saudi Arabia Using In Vitro and In Silico Approaches. Processes 2023, 11, 650. https://doi.org/10.3390/pr11030650

AMA Style

Al kamaly O, Alanazi AS, Conte R, Imtara H. Phytochemical Composition and Insight into Antibacterial Potential of Origanum vulgare Essential Oil from Saudi Arabia Using In Vitro and In Silico Approaches. Processes. 2023; 11(3):650. https://doi.org/10.3390/pr11030650

Chicago/Turabian Style

Al kamaly, Omkulthom, Ashwag S. Alanazi, Raffaele Conte, and Hamada Imtara. 2023. "Phytochemical Composition and Insight into Antibacterial Potential of Origanum vulgare Essential Oil from Saudi Arabia Using In Vitro and In Silico Approaches" Processes 11, no. 3: 650. https://doi.org/10.3390/pr11030650

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop