Abstract
The purpose of the present study was to determine for the first time the volatile constituents, the antioxidant and antimicrobial activities of the essential oil (EO) of the endemic Moroccan Linaria ventricosa, alone or in combination with four known antibiotics. The major constituents were 2-methoxy-4-vinylphenol (17.4%), α-terpinene (13.64%) and 3,5-dimethylphenyl isocyanate (12.21%). The EO had moderate antioxidant potency, as measured by DPPH free radical scavenging (1.233 ± 0.031 mg/mL), ferric reducing antioxidant power assay (0.373 ± 0.019 mg/mL) and β-carotene/linoleic acid (0.922 ± 0.026 mg/mL). EO showed microbicidal activity against all microorganisms tested. The highest effectiveness was recorded against Candida albicans (IZ = 24 mm, MIC = 4.87 mg/mL and MMC = 9.75 mg/mL) and Candida glabrata (IZ = 22 mm, MIC = MMC = 4.87 mg/mL). Gram negative bacteria were the most resistant (MIC = MMC = 39 mg/mL). The combination of EO at sub-inhibitory concentrations with antibiotics showed a significant decrease in their individual MICs from 2 to 128 fold, being the best for ciprofloxacin and fluconazole against E. coli and C. albicans and C. glabrata, respectively.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data and material availability
Data can be available upon request.
References
Boukef K (1986) Les Plates Dans la Médecine Traditionnelle Tunisienne. Agence De Coopération Culturelle Et Technique 1:350
Cheriet T, Mancini I, Seghiri R et al (2015) Chemical constituents and biological activities of the genus Linaria (Scrophulariaceae). Nat Prod Res 29:1589–1613. https://doi.org/10.1080/14786419.2014.999243
Cos P, Vlietinck AJ, Vanden BD, Maes L (2006) Anti-infective potential of natural products: how to develop a stronger in vitro ‘proof-of-concept.’ J Ethnopharmacol 106:290–302. https://doi.org/10.1016/j.jep.2006.04.003
Cox G, Wright GD (2013) Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. Int J Med Microbiol 303:287–292. https://doi.org/10.1016/j.ijmm.2013.02.009
Didry N, Dubreuil L, Pinkas M (1993) Microbiological properties of protoanemonin isolated from Ranunculus bulbosus. Phyther Res 7:21–24. https://doi.org/10.1002/ptr.2650070107
Donsì F, Ferrari G (2016) Essential oil nanoemulsions as antimicrobial agents in food. J Biotechnol 233:106–120. https://doi.org/10.1016/j.jbiotec.2016.07.005
Elhidar N, Nafis A, Kasrati A et al (2019) Chemical composition, antimicrobial activities and synergistic effects of essential oil from Senecio anteuphorbium, a Moroccan endemic plant. Ind Crops Prod 130:310–315. https://doi.org/10.1016/j.indcrop.2018.12.097
Fernández-Mazuecos M, Blanco-Pastor JL, Vargas P (2013) A phylogeny of Toadflaxes (Linaria Mill.) based on nuclear internal transcribed spacer sequences: systematic and evolutionary consequences. Int J Plant Sci 174:234–249. https://doi.org/10.1086/668790
Fukai S, Tanimoto S, Maeda A et al (2009) Pharmacological activity of compounds extracted from persimmon peel (Diospyros kaki Thunb.). J Oleo Sci 58:213–219
Gülçin İ, Huyut Z, Elmastaş M, Aboul-Enein HY (2010) Radical scavenging and antioxidant activity of tannic acid. Arab J Chem 3:43–53. https://doi.org/10.1016/J.ARABJC.2009.12.008
Helal IM, El-Bessoumy A, Al-Bataineh E et al (2019) Antimicrobial efficiency of essential oils from traditional medicinal plants of Asir region, Saudi Arabia, over drug resistant isolates. Biomed Res Int 2019:1–9. https://doi.org/10.1155/2019/8928306
Helander IM, Alakomi H-L, Latva-Kala K et al (1998) Characterization of the action of selected essential oil components on Gram-negative bacteria. J Agric Food Chem 46:3590–3595. https://doi.org/10.1021/jf980154m
Hua H, Cheng M, Li X, Pei Y (2002) A new pyrroloquinazoline alkaloid from Linaria vulgaris. Chem Pharm Bull (tokyo) 50:1393–1394
Janssen A, Scheffer J, Svendsen A (1987) Antimicrobial activity of essential oils: a 1976–1986 literature review. Aspects of the test methods. Planta Med 53:395–398. https://doi.org/10.1055/s-2006-962755
Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:813–829. https://doi.org/10.2174/0929867033457719
Khalil N, Ashour M, Fikry S et al (2018) Chemical composition and antimicrobial activity of the essential oils of selected Apiaceous fruits. Futur J Pharm Sci 4:88–92. https://doi.org/10.1016/j.fjps.2017.10.004
Kitagawa I, Tani T, Akita K, Yosioka I (1973) On the constituents of Linaria japonica MIQ. I. The structure of linarioside, a new chlorinated iridoid glucoside and identification of two related glucosides. Chem Pharm Bull 21:1978–1987. https://doi.org/10.1248/cpb.21.1978
Langeveld WT, Veldhuizen EJA, Burt SA (2014) Synergy between essential oil components and antibiotics: a review. Crit Rev Microbiol 40:76–94. https://doi.org/10.3109/1040841X.2013.763219
Man A, Santacroce L, Jacob R et al (2019) Antimicrobial activity of six essential oils against a group of human pathogens: a comparative study. Pathogens 8:15. https://doi.org/10.3390/pathogens8010015
Mastelić J, Blažević I, Kosalec I (2010) Chemical composition and antimicrobial activity of volatiles from Degenia velebitica, a European Stenoendemic plant of the Brassicaceae family. Chem Biodivers 7:2755–2765. https://doi.org/10.1002/cbdv.201000053
Miraliakbari H, Shahidi F (2008) Antioxidant activity of minor components of tree nut oils. Food Chem 111:421–427. https://doi.org/10.1016/J.FOODCHEM.2008.04.008
Miranda CD, Godoy FA, Lee MR (2018) Current status of the use of antibiotics and the antimicrobial resistance in the Chilean salmon farms. Front Microbiol 9:1284. https://doi.org/10.3389/fmicb.2018.01284
Nafis A, Kasrati A, Jamali CA et al (2019) Antioxidant activity and evidence for synergism of Cannabis sativa (L.) essential oil with antimicrobial standards. Ind Crops Prod 137:396–400. https://doi.org/10.1016/j.indcrop.2019.05.032
Nieto G (2017) Biological activities of three essential oils of the Lamiaceae family. Medicines 4:63. https://doi.org/10.3390/medicines4030063
Okoh OO, Sadimenko AP, Afolayan AJ (2010) Comparative evaluation of the antibacterial activities of the essential oils of Rosmarinus officinalis L. obtained by hydrodistillation and solvent free microwave extraction methods. Food Chem 120:308–312. https://doi.org/10.1016/j.foodchem.2009.09.084
Otsuka H (1993) Phenylethanoids from Linaria japonica. Phytochemistry 32:979–981. https://doi.org/10.1016/0031-9422(93)85239-N
Pandey AK, Singh P, Tripathi NN (2014) Chemistry and bioactivities of essential oils of some Ocimum species: an overview. Asian Pac J Trop Biomed 4:682–694. https://doi.org/10.12980/APJTB.4.2014C77
Rosato A, Vitali C, Piarulli M et al (2009) In vitro synergic efficacy of the combination of Nystatin with the essential oils of Origanum vulgare and Pelargonium graveolens against some Candida species. Phytomedicine 16:972–975. https://doi.org/10.1016/J.PHYMED.2009.02.011
Şahin F, Güllüce M, Daferera D et al (2004) Biological activities of the essential oils and methanol extract of Origanum vulgare ssp. vulgare in the eastern Anatolia region of Turkey. Food Control 15:549–557. https://doi.org/10.1016/J.FOODCONT.2003.08.009
San Feliciano A, Gordaliza M, Miguel Del Corral JM, De La Puente ML (1993) Neo-clerodane diterpenoids from roots of Linaria saxatilis var. Glutinosa Phytochemistry 33:631–633. https://doi.org/10.1016/0031-9422(93)85462-Z
Sarikurkcu C, Ozer MS, Calli N, Popović-Djordjević J (2018) Essential oil composition and antioxidant activity of endemic Marrubium parviflorum subsp. oligodon. Ind Crops Prod 119:209–213. https://doi.org/10.1016/j.indcrop.2018.04.023
Silva VA, Sousa JP, Guerra FQS et al (2015) Antibacterial activity of the monoterpene linalool: alone and in association with antibiotics against bacteria of clinical importance. Int J Pharmacogn Phytochem Res 7:1022–1026
Tekaya-Karoui A, Hammami S, Mrad NN et al (2010) Chemical composition of floral essential oil from Linaria heterophylla Desf. growing in Tunisia. J Essent Oil Bear Plants 13:165–169. https://doi.org/10.1080/0972060X.2010.10643806
Tepe B, Sokmen M, Akpulat HA et al (2005) Antioxidative activity of the essential oils of Thymus sipyleus subsp. sipyleus var. sipyleus and Thymus sipyleus subsp. sipyleus var. rosulans. J Food Eng 66:447–454. https://doi.org/10.1016/j.jfoodeng.2004.04.015
Vazirian M, Hamidian K, Noorollah M et al (2019) Enhancement of antibiotic activity and reversal of resistance in clinically isolated methicillin-resistant Staphylococcus aureus by Trachyspermum ammi essential oil. Res J Pharmacogn 6:1–10. https://doi.org/10.22127/RJP.2018.80365
Zengin G, Sarikurkcu C, Aktumsek A, Ceylan R (2014) Sideritis galatica Bornm.: a source of multifunctional agents for the management of oxidative damage, Alzheimer’s and diabetes mellitus. J Funct Foods 11:538–547. https://doi.org/10.1016/J.JFF.2014.08.011s
Acknowledgements
They thank also the professor Ahmed OUHAMMOU, responsible for the Regional herbarium MARK of Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakech, Morocco.
Funding
The authors acknowledge the FCT Projects UIDB/04423/2020 and UIDP/04423/2020.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No potential conflict of interest was reported by the authors.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nafis, A., Saad, F.E., Khalloufi, F.E. et al. New insight into antimicrobial activities of Linaria ventricosa essential oil and its synergetic effect with conventional antibiotics. Arch Microbiol 203, 4361–4366 (2021). https://doi.org/10.1007/s00203-021-02391-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-021-02391-7