Antimicrobial Potential and Phytochemical Profile of Wild and Cultivated Populations of Thyme (Thymus sp.) Growing in Western Romania
Abstract
:1. Introduction
2. Results and Discussion
2.1. EO Yield and Composition
2.2. Antimicrobial Activity
3. Materials and Methods
3.1. Plant Material
3.2. Obtaining the EOs
3.3. GC–MS Analysis of EOs
3.4. Determination of Antimicrobial Activity
3.4.1. Bacterial Culture
3.4.2. Fungi Culture
3.5. Statistical Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rustaiee, A.; Sefidkon, F.; Tabatabaei, S.M.F.; Omidbaigi, R.; Mirahmadi, S.F.; Shayganfar, A. Chemical Polymorphism of Essential Oils from Five Populations of Thymus daenensis Celak. subsp. daenensis Endemic to Iran. J. Essent. Oil Res. 2011, 23, 6–11. [Google Scholar] [CrossRef]
- Pluhár, Z.; Kocsis, M.; Kuczmog, A.; Csete, S.; Simkó, H.; Sárosi, S.; Molnar, P.; Horváth, G. Essential oil composition and preliminary molecular study of four Hungarian Thymus species. Acta Biol. Hung. 2012, 63, 81–96. [Google Scholar] [CrossRef]
- Morales, R. The history, botany and taxonomy of the genus Thymus. In Thyme: The Genus Thymus, 1st ed.; Stahl-Biskup, E., Saez, F., Eds.; Taylor and Francis: London, UK, 2002; pp. 1–43. [Google Scholar]
- Ložienė, K.; Venskutonis, P. Influence of environmental and genetic factors on the stability of essential oil composition of Thymus pulegioides. Biochem. Syst. Ecol. 2005, 33, 517–525. [Google Scholar] [CrossRef]
- Taghouti, M.; Martins-Gomes, C.; Félix, L.M.; Schäfer, J.; Santos, J.A.; Bunzel, M.; Nunes, F.M.; Silva, A.M. Polyphenol composition and biological activity of Thymus citriodorus and Thymus vulgaris: Comparison with endemic Iberian Thymus species. Food Chem. 2020, 331, 127362. [Google Scholar] [CrossRef]
- Gușuleac, M. Thymus L. In Flora Romaniae; Săvulescu, T.R., Redactore Tomi Nyarady, E.I., Beldie, A., Bioa, A., Grințescu, I., Gușuleac, M., Moraiu, I., Nyarady, A., Nyarady, E.I., Paucă, A., et al., Eds.; Academia Română Publishing House: Bucharest, Romania, 1961; pp. 301–334. [Google Scholar]
- Sârbu, I.; Ștefan, N.; Oprea, A. Plante Vasculare din România. Determinator Ilustrat de Teren; Victor B Victor: Bucharest, Romania, 2013; pp. 666–674. ISBN 9786068149080. [Google Scholar]
- The EuroPlusMedPlantbase. Available online: https://ww2.bgbm.org/EuroPlusMed/query.asp (accessed on 23 June 2021).
- Ramchoun, M.; Khouya, T.; Harnafi, H.; Amrani, S.; Alem, C.; Benlyas, M.; Chadli, F.K.; Nazih, H.; Nguyen, P.; Ouguerram, K. Effect of Aqueous Extract and Polyphenol Fraction Derived from Thymus atlanticus Leaves on Acute Hyperlipidemia in the Syrian Golden Hamsters. Evid.-Based Complement. Altern. Med. 2020, 2020, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Hoven, R.V.D.; Zappe, H.; Zitterl-Eglseer, K.; Jugl, M.; Franz, C. Study of the effect of Bronchipret on the lung function of five Austrian saddle horses suffering recurrent airway obstruction (heaves). Veter. Rec. 2003, 152, 555–557. [Google Scholar] [CrossRef] [PubMed]
- Nascimento, G.G.F.; Locatelli, J.; Freitas, P.C.; Silva, G.L. Antibacterial activity of plant extracts and phytochemicals on antibiotic-resistant bacteria. Braz. J. Microbiol. 2000, 31, 247–256. [Google Scholar] [CrossRef]
- Ciobotaru, V.G.G.; Pavel, I.Z.; Borcan, F.; Moaca, A.; Danciu, C.; Diaconeasa, Z.; Imbrea, I.; Vlad, D.; Dumitrascu, V.; Pop, G. Toxicological Evaluation of Some Essential Oils Obtained from Selected Romania Lamiaceae Species in Complex with Hydroxypropyl—Gamma-cyclodextrin. Rev. Chim. 2019, 70, 3703–3707. [Google Scholar] [CrossRef]
- Alexa, E.; Sumalan, R.M.; Danciu, C.; Obistioiu, D.; Negrea, M.; Poiana, M.-A.; Rus, C.; Radulov, I.; Pop, G.; Dehelean, C. Synergistic Antifungal, Allelopatic and Anti-Proliferative Potential of Salvia officinalis L., and Thymus vulgaris L. Essential Oils. Molecules 2018, 23, 185. [Google Scholar] [CrossRef] [Green Version]
- Granger, R.; Passet, J. Thymus vulgaris spontane de France: Races chimiques et chemotaxonomie. Phytochemistry 1973, 12, 1683–1691. [Google Scholar] [CrossRef]
- Semeniuc, C.A.; Socaciu, M.-I.; Socaci, S.A.; Mureșan, V.; Nagy, M.; Rotar, A.M. Chemometric Comparison and Classification of Some Essential Oils Extracted from Plants Belonging to Apiaceae and Lamiaceae Families Based on Their Chemical Composition and Biological Activities. Molecules 2018, 23, 2261. [Google Scholar] [CrossRef] [Green Version]
- Pinto, E.; Gonçalves, M.J.; Hrimpeng, K.; Pinto, J.; Vaz, S.; Vale-Silva, L.A.; Cavaleiro, C.; Salgueiro, L. Antifungal activity of the essential oil of Thymus villosus subsp. lusitanicus against Candida, Cryptococcus, Aspergillus and dermatophyte species. Ind. Crop. Prod. 2013, 51, 93–99. [Google Scholar] [CrossRef]
- Lawrence, B.M.; Tucker, A.O. The genus Thymus as a source of commercial products. In Thyme: The Genus Thymus, 1st ed.; Stahl-Biskup, E., Saez, F., Eds.; Taylor and Francis: London, UK, 2002; p. 330. [Google Scholar]
- Hadian, J.; Bigdeloo, M.; Nazeri, V.; Khadivi-Khub, A. Assessment of genetic and chemical variability in Thymus caramanicus. Mol. Biol. Rep. 2014, 41, 3201–3210. [Google Scholar] [CrossRef] [PubMed]
- Tohidi, B.; Rahimmalek, M.; Arzani, A.; Sabzalian, M.R. Thymol, carvacrol, and antioxidant accumulation in Thymus species in response to different light spectra emitted by light-emitting diodes. Food Chem. 2020, 307, 125521. [Google Scholar] [CrossRef]
- Ghasemi, P.; Barani, M.; Hamedi, B.; Ataei, K.; Karimi, A. Environment effect on diversity in quality and quantity of essential oil of different wild populations of Kerman thyme. Genetika 2013, 45, 441–450. [Google Scholar] [CrossRef]
- Vladimir-Knežević, S.; Blažeković, B.; Kindl, M.; Vladić, J.; Lower-Nedza, A.D.; Brantner, A.H. Acetylcholinesterase Inhibitory, Antioxidant and Phytochemical Properties of Selected Medicinal Plants of the Lamiaceae Family. Molecules 2014, 19, 767–782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cocan, I.; Alexa, E.; Danciu, C.; Radulov, I.; Galuscan, A.; Obistioiu, D.; Morvay, A.A.; Sumalan, R.M.; Poiana, M.-A.; Pop, G.; et al. Phytochemical screening and biological activity of Lamiaceae family plant extracts. Exp. Ther. Med. 2017, 15, 1863–1870. [Google Scholar] [CrossRef] [Green Version]
- Nieto, G. Biological Activities of Three Essential Oils of the Lamiaceae Family. Medicines 2017, 4, 63. [Google Scholar] [CrossRef] [Green Version]
- Karpiński, T.M. Essential Oils of Lamiaceae Family Plants as Antifungals. Biomolecules 2020, 10, 103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iseppi, R.; Tardugno, R.; Brighenti, V.; Benvenuti, S.; Sabia, C.; Pellati, F.; Messi, P. Phytochemical Composition and In Vitro Antimicrobial Activity of Essential Oils from the Lamiaceae Family against Streptococcus agalactiae and Candida albicans Biofilms. Antibiotics 2020, 9, 592. [Google Scholar] [CrossRef]
- Ložienė, K.; Vaičiulytė, V.; Maždžierienė, R. Influence of meteorological conditions on essential oil composition in geraniol-bearing Thymus pulegioides and Thymus hybrid. Acta Physiol. Plant. 2021, 43, 1–9. [Google Scholar] [CrossRef]
- Imelouane, B.; Amhamdi, H.; Wathelet, J.P.; Ankit, M.; Khedid, K.; El Bachiri, A. Chemical composition and antimicrobial activity of essential oil of thyme (Thymus vulgaris) from Eastern Morocco. Int. J. Agric. Biol. 2009, 11, 205–208. [Google Scholar]
- Golkar, P.; Mosavat, N.; Jalali, S.A.H. Essential oils, chemical constituents, antioxidant, antibacterial and in vitro cytotoxic activity of different Thymus species and Zataria multiflora collected from Iran. S. Afr. J. Bot. 2020, 130, 250–258. [Google Scholar] [CrossRef]
- Pavel, M.; Ristić, M.; Stević, T. Essential oils of Thymus pulegioides and Thymus glabrescens from Romania: Chemical composition and antimicrobial activity. J. Serb. Chem. Soc. 2010, 75, 27–34. [Google Scholar] [CrossRef]
- Mamadalieva, N.Z.; Akramov, D.K.; Ovidi, E.; Tiezzi, A.; Nahar, L.; Azimova, S.S.; Sarker, S.D. Aromatic Medicinal Plants of the Lamiaceae Family from Uzbekistan: Ethnopharmacology, Essential Oils Composition, and Biological Activities. Medicines 2017, 4, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boros, B.; Jakabová, S.; Dornyei, A.; Horváth, G.; Pluhár, Z.; Kilar, F.; Felinger, A. Determination of polyphenolic compounds by liquid chromatography–mass spectrometry in Thymus species. J. Chromatogr. A 2010, 1217, 7972–7980. [Google Scholar] [CrossRef]
- Borugă, O.; Jianu, C.; Mişcă, C.; Goleţ, I.; Gruia, A.T.; Horhat, F.G. Thymus vulgaris essential oil: Chemical composition nd antimicrobial activity. J. Med. Life 2014, 7, 56–60. [Google Scholar]
- Isopencu, G.; Ferdes, M. Aspects regarding the influence of concentration of compoments with antifungal activity from some essential oils. Rev. Chim. 2012, 63, 205–211. [Google Scholar]
- Grigore, A.; Mihul, A.; Paraschiv, I.; Nita, S.; Christof, R.; Iuksel, R.; Ichim, M. Chemical analysis and antimicrobial activity of indigenous medicinal species volatile oils. Rom. Biotechnol. Lett. 2012, 17, 7620–7627. [Google Scholar]
- Varga, E.; Bardocz, A.; Belak, A.; Maraz, A.; Boros, B.; Felinger, A.; Boszormenyi, A.; Horvath, G. Antimicrobial activity and chemical composition of thyme essential oils and the polyphenolic content of different Thymus extract. Farmacia 2015, 63, 357–361. [Google Scholar]
- Lorenzo, J.M.; Munekata, P.E.S.; Dominguez, R.; Pateiro, M.; Saraiva, J.A.; Franco, D. Main Groups of Microorganisms of Relevance for Food Safety and Stability. Innov. Technol. Food Preserv. 2018, 2018, 53–107. [Google Scholar] [CrossRef]
- Park, S.-N.; Lim, Y.K.; Freire, M.; Cho, E.; Jin, D.; Kook, J.-K. Antimicrobial effect of linalool and α-terpineol against periodontopathic and cariogenic bacteria. Anaerobe 2012, 18, 369–372. [Google Scholar] [CrossRef] [PubMed]
- Rehab, M.A.E.-B.; Zeinab, S.H. Eugenol and linalool: Comparison of their antibacterial and antifungal activities. Afr. J. Microbiol. Res. 2016, 10, 1860–1872. [Google Scholar] [CrossRef] [Green Version]
- Ložienė, K.; Venskutonis, P.R.; Šipailienė, A.; Labokas, J. Radical scavenging and antibacterial properties of the extracts from different Thymus pulegioides L. chemotypes. Food Chem. 2007, 103, 546–559. [Google Scholar] [CrossRef]
- Mockute, D.; Bernotiene, G. Five Chemotypes of the Essential Oils of Thymus pulegioides L. Growing Wild in Lithuania. J. Essent. Oil Bear. Plants 2003, 6, 139–147. [Google Scholar] [CrossRef]
- De Martino, L.; Bruno, M.; Formisano, C.; De Feo, V.; Napolitano, F.; Rosselli, S.; Senatore, F. Chemical Composition and Antimicrobial Activity of the Essential Oils from Two Species of Thymus Growing Wild in Southern Italy. Molecules 2009, 14, 4614–4624. [Google Scholar] [CrossRef] [Green Version]
- Duman, A.D.; Telci, I.; Dayisoylu, K.S.; Digrak, M.; Demirtas, I.; Alma, M.H. Evaluation of Bioactivity of Linalool-rich Essential Oils from Ocimum basilucum and Coriandrum sativum Varieties. Nat. Prod. Commun. 2010, 5, 969–974. [Google Scholar] [CrossRef] [Green Version]
- Afonso, A.F.; Pereira, O.R.; Válega, M.; Silva, A.M.S.; Cardoso, S.M. Metabolites and Biological Activities of Thymus zygis, Thymus pulegioides, and Thymus fragrantissimus Grown under Organic Cultivation. Molecules 2018, 23, 1514. [Google Scholar] [CrossRef] [Green Version]
- Vaičiulytė, V.; Ložienė, K.; Švedienė, J.; Raudonienė, V.; Paškevičius, A. α-Terpinyl Acetate: Occurrence in Essential Oils Bearing Thymus pulegioides, Phytotoxicity, and Antimicrobial Effects. Molecules 2021, 26, 1065. [Google Scholar] [CrossRef]
- Niculae, M.; Hanganu, D.; Oniga, I.; Benedec, D.; Ielciu, I.; Giupana, R.; Sandru, C.D.; Ciocârlan, N.; Spinu, M. Phytochemical Profile and Antimicrobial Potential of Extracts Obtained from Thymus marschallianus Willd. Molecules 2019, 24, 3101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mancini, E.; Senatore, F.; Del Monte, D.; De Martino, L.; Grulova, D.; Scognamiglio, M.; Snoussi, M.; De Feo, V. Studies on Chemical Composition, Antimicrobial and Antioxidant Activities of Five Thymus vulgaris L. Essential Oils. Molecules 2015, 20, 12016–12028. [Google Scholar] [CrossRef] [Green Version]
- Verma, R.S.; Padalia, R.C.; Saikia, D.; Chauhan, A.; Krishna, V.; Sundaresan, V. Chemical Composition and Antimicrobial Activity of the Essential Oils Isolated from the Herbage and Aqueous Distillates of two Thymus Species. J. Essent. Oil Bear. Plants 2016, 19, 936–943. [Google Scholar] [CrossRef]
- Al-Shuneigat, J.; Al-Sarayreh, S.; Al-Saraireh, Y.; Al-Qudah, M.; Al-Tarawneh, I.; Al Bataineh, E. Effects of wild Thymus vulgaris essential oil on clinical isolates biofilm-forming bacteria. IOSR J. Dent. Med Sci. 2014, 13, 62–66. [Google Scholar] [CrossRef]
- Soković, M.D.; Vukojevic, J.; Marin, P.D.; Brkić, D.D.; Vajs, V.; Van Griensven, L.J.L.D. Chemical Composition of Essential Oilsof Thymus and Mentha Speciesand Their Antifungal Activities. Molecules 2009, 14, 238–249. [Google Scholar] [CrossRef]
- De Carvalho, R.J.; de Souza, G.T.; Honório, V.G.; de Sousa, J.P.; da Conceição, M.L.; Maganani, M.; de Souza, E.L. Comparative inhibitory effects of Thymus vulgaris L. essential oil against Staphylococcus aureus, Listeria monocytogenes and mesophilic starter co-culture in cheese-mimicking models. Food Microbiol. 2015, 52, 59–65. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, A.; Van Vuuren, S.; Viljoen, A. Unravelling the Complex Antimicrobial Interactions of Essential Oils—The Case of Thymus vulgaris (Thyme). Molecules 2014, 19, 2896–2910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galovičová, L.; Borotová, P.; Valková, V.; Vukovic, N.; Vukic, M.; Terentjeva, M.; Štefániková, J.; Ďúranová, H.; Kowalczewski, P.; Kačániová, M. Thymus serpyllum Essential Oil and Its Biological Activity as a Modern Food Preserver. Plants 2021, 10, 1416. [Google Scholar] [CrossRef]
- Guimarães, A.C.; Meireles, L.M.; Lemos, M.F.; Guimarães, M.C.C.; Endringer, D.C.; Fronza, M.; Scherer, R. Antibacterial Activity of Terpenes and Terpenoids Present in Essential Oils. Molecules 2019, 24, 2471. [Google Scholar] [CrossRef] [Green Version]
- Marchese, A.; Arciola, C.R.; Barbieri, R.; Silva, A.S.; Nabavi, S.M.; Sokeng, A.J.T.; Izadi, M.; Jafari, N.J.; Suntar, I.; Daglia, M.; et al. Update on Monoterpenes as Antimicrobial Agents: A Particular Focus on p-Cymene. Materials 2017, 10, 947. [Google Scholar] [CrossRef]
- Togashi, N.; Inoue, Y.; Hamashima, H.; Takano, A. Effects of Two Terpene Alcohols on the Antibacterial Activity and the Mode of Action of Farnesol against Staphylococcus aureus. Molecules 2008, 13, 3069–3076. [Google Scholar] [CrossRef] [Green Version]
- Lorenzi, V.; Muselli, A.; Bernardini, A.F.; Berti, L.; Pagès, J.-M.; Amaral, L.; Bolla, J.-M. Geraniol Restores Antibiotic Activities against Multidrug-Resistant Isolates from Gram-Negative Species. Antimicrob. Agents Chemother. 2009, 53, 2209–2211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hrytsyna, M.R.; Kryvtsova, M.V.; Salamon, I.; Skybitska, M.I. Promising ex situ essential oil from Thymus camphoratus (Lamiaceae). Regul. Mech. Biosyst. 2020, 11, 315–322. [Google Scholar] [CrossRef]
- Kryvtsova, M.V.; Salamon, I.; Koscova, J.; Bucko, D.; Spivak, M. Antimicrobial, antibiofilm and biochemichal properties of Thymus vulgaris essential oil against clinical isolates of opportunistic infections. Biosyst. Divers. 2019, 27, 270–275. [Google Scholar] [CrossRef] [Green Version]
- Adams, R.P. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, 4th ed.; Allured Publishing Corporation: Carol Stream, IL, USA, 2007; ISBN 978-1-932633-21-4. [Google Scholar]
- Obistioiu, D.; Cocan, I.; Tîrziu, E.; Herman, V.; Negrea, M.; Cucerzan, A.; Neacsu, A.-G.; Cozma, A.; Nichita, I.; Hulea, A.; et al. Phytochemical Profile and Microbiological Activity of Some Plants Belonging to the Fabaceae Family. Antibiotics 2021, 10, 662. [Google Scholar] [CrossRef]
- Alexa, V.T.; Galuscan, A.; Popescu, I.; Tirziu, E.; Obistioiu, D.; Floare, A.D.; Perdiou, A.; Jumanca, D. Synergistic/Antagonistic Potential of Natural Preparations Based on Essential Oils Against Streptococcus mutans from the Oral Cavity. Molecules 2019, 24, 4043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Costa, L.C.B.; Pinto, J.E.B.P.; Bertolucci, S.K.V.; Costa, J.C.D.B.; Alves, P.B.; Niculau, E.D.S. In vitroantifungal activity of Ocimum selloi essential oil and methylchavicol against phytopathogenic fungi. Rev. Cienc. Agron. 2015, 46, 428–435. [Google Scholar] [CrossRef] [Green Version]
Population | EO Abbreviation | Location | EO Yield (%) | EO Color | |
---|---|---|---|---|---|
T. odoratissimus Mill. | | TgS | Silagiu | 0.620 ± 0.012 | Brown |
T. pulegioides L. | | TpP | Prigor | 0.460 ± 0.033 | Brown–yellow |
T. pulegioides L. | | TpC | Carasova | 0.440 ± 0.021 | Yellow |
T. pulegioides L. | | TpB | Bazias | 0.490 ± 0.017 | Pale-yellow |
T. vulgaris L. | | TvL | Lovrin | 0.810 ± 0.042 | Brown–yellow |
Nr Crt | Ri a | Ri b | Compound | Classes | TgS | TpP | TpC | TpB | TvL |
---|---|---|---|---|---|---|---|---|---|
1 | 930 | 930 | α-Thujene | MH | 1.42 | 1.12 | 1 | 0.5 | 0.63 |
2 | 939 | 939 | α-Pinene * | MH | 0.67 | 0.59 | 0.5 | 0.25 | 0.5 |
3 | 954 | 954 | Camphene | MH | 0.38 | 0.36 | 0.42 | 0.21 | |
4 | 975 | 975 | Sabinene * | MH | 0.06 | 0.1 | 0.09 | 0.04 | |
5 | 979 | 983 | β-Pinene * | MH | 1.63 | 1.03 | 1.01 | 0.48 | 0.52 |
6 | 990 | 987 | β-Myrcene * | MH | 0.08 | ||||
7 | 1002 | 993 | α-Phellandrene * | MH | 0.31 | 0.21 | 0.16 | ||
8 | 1011 | 1002 | 3-Carene * | MH | 0.07 | 0.06 | 0.04 | ||
9 | 1012 | 1010 | 4-Carene | MH | 1.86 | 1.6 | 1.3 | 0.57 | |
10 | 1020 | 1019 | D-Limonene * | MH | 0.23 | ||||
11 | 1023 | 1020 | m-Cymene | MH | 8.45 | 6.3 | |||
12 | 1024 | 1021 | p-Cymene | MH | 8.55 | 15.12 | 0.43 | 10.94 | |
13 | 1037 | 1027 | cis-β-Ocimene * | MH | 0.22 | 0.99 | |||
14 | 1050 | 1038 | trans-β-Ocimene * | MH | 0.06 | ||||
15 | 1059 | 1069 | γ-Terpinene | MH | 8.96 | 5.14 | 7.47 | 1.68 | 8.5 |
16 | 1070 | 1085 | cis-Sabinene hydrate | MH | 1.69 | 0.55 | 0.49 | 0.2 | 1.27 |
17 | 1088 | 1107 | α-Terpinolene | MH | 0.1 | 0.16 | 1.04 | ||
18 | 1299 | 1295 | Carvacrol * | MO | 7.94 | 5.71 | 25.43 | 15.92 | 2.58 |
19 | 1235 | 1238 | Thymyl methyl ether | MO | 6.34 | 5.88 | 2.05 | 1.6 | 5.27 |
20 | 1244 | 1250 | Carvacrol methyl ether | MO | 6.67 | 5.73 | 5.54 | 3.81 | 5.24 |
21 | 1290 | 1290 | Thymol | MO | 30.82 | 33.81 | 13.93 | 17.14 | 40.85 |
22 | 1096 | 1121 | Linalool | MO | 2.84 | 0.77 | 2.27 | ||
23 | 1146 | 1140 | Camphor | MO | 0.08 | ||||
24 | 1169 | 1168 | endo-Borneol | MO | 0.62 | 0.55 | 0.86 | 0.47 | 0.7 |
25 | 1160 | 1170 | Isoborneol | MO | 0.55 | ||||
26 | 1177 | 1171 | Terpinen-4-ol | MO | 0.68 | 0.79 | 0.38 | ||
27 | 1188 | 1190 | α-Terpineol | MO | 6.29 | ||||
28 | 1252 | 1259 | cis-Geraniol | MO | 1.88 | 13.12 | 28.35 | ||
29 | 1257 | 1263 | Linalyl acetate | MO | 0.72 | ||||
30 | 1285 | 1287 | Borneol acetate | MO | 0.56 | ||||
31 | 1381 | 1390 | cis-Geranyl acetate | MO | 0.72 | 3.33 | 5.7 | ||
32 | 1271 | 1280 | Lavandulol acetate | MO | 1.22 | ||||
33 | 1422 | 1423 | Lavandulyl isobutyrate | MO | 0.13 | ||||
34 | 1591 | 1603 | (R)-Lavandulyl (R)-2-methylbutanoate | MO | 0.12 | ||||
35 | Dihydro-1,8-cineole | MO | 0.49 | 0.41 | 0.25 | ||||
36 | 980 | 984 | 3-Octanol | others | 0.12 | 0.66 | |||
37 | 963 | 963 | 3-Octanone | others | 2.6 | ||||
38 | 1-Methyl-4-(methylethyl)-(E)-2-cyclohexenol | others | 1.95 | ||||||
39 | 4,8,8-Trimethyl-2-methylene-4-vinylbicyclo[5.2.0] nonane | others | 2.39 | ||||||
40 | Unidentified | others | 0.3 | ||||||
41 | Methyl-3-methylenetricyclo[4.4.0.02,7] decane | others | 0.43 | ||||||
42 | Unidentified | others | 0.22 | ||||||
43 | Unidentified | others | 0.33 | 0.37 | |||||
44 | 977 | 977 | 1-Octen-3-ol | others | 0.52 | 0.4 | 0.23 | 0.23 | 0.84 |
45 | 1110 | 1123 | 3-Octanol acetate | others | 0.21 | ||||
46 | cis-4,11,11-Trimethyl-8-methylenebicyclo(7.2.0)undeca-4-ene (cis-caryophyllene) | SH | 6.51 | 3.45 | 3.68 | ||||
47 | Isoledene | SH | 1.46 | 0.23 | 0.29 | ||||
48 | α-Muurolene | SH | 0.6 | 0.1 | |||||
49 | β-Bisabolene | SH | 7.54 | ||||||
50 | γ-Cadinene | SH | 0.17 | ||||||
51 | 1408 | 1410 | Isocaryophyllene | SH | 5.22 | 6.83 | |||
52 | 1419 | 1420 | Caryophyllene * | SH | 4.19 | 5.98 | |||
53 | 1376 | 1380 | α-Copaene | SH | 0.9 | 0.4 | |||
54 | 1454 | 1456 | Humulene | SH | 0.24 | 0.37 | 0.53 | ||
55 | 1479 | 1483 | gamma-Muurolene | SH | 0.83 | 0.14 | 0.05 | ||
56 | 1481 | 1485 | Germacrene D | SH | 1.88 | 0.18 | 1.05 | 1.25 | 2.24 |
57 | 1441 | 1442 | Aromadendrene | SH | 4.14 | ||||
58 | 1432 | 1435 | β-copaene | SH | 0.61 | ||||
59 | 1583 | 1584 | Caryophyllene oxide | SO | 0.34 | ||||
60 | 1640 | 1638 | Cadinol | SO | 0.07 | ||||
TOTAL | 100 | 99.39 | 100 | 99.6 | 99.7 | ||||
Total of Major Compounds | TgS | TpP | TpC | TpB | TvL | ||||
Area (%) | |||||||||
Monoterpene hydrocarbonates (MH) | 25.92 | 27.03 | 21.5 | 10.46 | 23.4 | ||||
Monoterpene oxygenate (MO) | 56.4 | 62.33 | 67.13 | 75.89 | 55.36 | ||||
Total Monoterpene | 82.32 | 89.36 | 88.63 | 86.35 | 78.76 | ||||
Sesquiterpene hydrocarbonates (SH) | 12.18 | 9.29 | 10.47 | 12.58 | 16.54 | ||||
Sesquiterpene oxygenate (SO) | 0 | 0 | 0.34 | 0.07 | 0 | ||||
Total Sesquiterpene | 12.18 | 9.29 | 10.81 | 12.65 | 16.54 | ||||
Others | 5.5 | 0.74 | 0.56 | 0.6 | 4.4 | ||||
TOTAL | 100 | 99.39 | 100 | 99.6 | 99.7 |
% | S. pyogenes | S. aureus | S. flexneri | P. aeruginosa | E. coli | S. typhimurium | H. influenza | C. parapsilopsis | C. albicans |
---|---|---|---|---|---|---|---|---|---|
TgS16 | 0.167 ± 0.006 a | 0.197 ± 0.008 a | 0.199 ± 0.006 a | 0.572 ± 0.004 a | 0.166 ± 0.001 a | 0.171 ± 0.002 a | 0.130 ± 0.001 a | 0.201 ± 0.001 a | 0.218 ± 0.005 a |
TgS8 | 0.188 ± 0.004 b | 0.222 ± 0.001 b | 0.221 ± 0.003 b | 0.589 ± 0.002 b | 0.190 ± 0.007 b | 0.185 ± 0.002 b | 0.152 ± 0.002 b | 0.224 ± 0.005 b | 0.220 ± 0.003 a |
TgS4 | 0.192 ± 0.003 b | 0.244 ± 0.004 c | 0.221 ± 0.002 b | 0.594 ± 0.003 c | 0.209 ± 0.004 c | 0.193 ± 0.003 c | 0.202 ± 0.003 c | 0.241 ± 0.002 c | 0.222 ± 0.004 a |
TgS2 | 0.215 ± 0.002 c | 0.279 ± 0.002 d | 0.285 ± 0.001 c | 0.636 ± 0.012 d | 0.238 ± 0.006 d | 0.237 ± 0.013 d | 0.272 ± 0.003 d | 0.294 ± 0.005 d | 0.264 ± 0.005 b |
TpP16 | 0.163 ± 0.005 a | 0.218 ± 0.002 e | 0.210 ± 0.002 d | 0.634 ± 0.009 d | 0.191 ± 0.001 b | 0.200 ± 0.001 e | 0.202 ± 0.001 c | 0.217 ± 0.001 b | 0.240 ± 0.003 c |
TpP8 | 0.219 ± 0.004 c | 0.259 ± 0.002 f | 0.215 ± 0.002 e | 0.744 ± 0.013 e | 0.280 ± 0.001 e | 0.248 ± 0.003 d | 0.264 ± 0.002 e | 0.255 ± 0.005 e | 0.260 ± 0.003 d |
TpP4 | 0.289 ± 0.003 d | 0.361 ± 0.001 g | 0.348 ± 0.012 f | 1.144 ± 0.047 f | 0.328 ± 0.001 e | 0.315 ± 0.004 f | 0.296 ± 0.044 f,h | 0.334 ± 0.002 f | 0.277 ± 0.002 e |
TpP2 | 0.321 ± 0.001 e | 0.385 ± 0.007 h | 0.391 ± 0.009 g | 1.169 ± 0.020 f,g | 0.456 ± 0.008 e | 0.385 ± 0.008 g | 0.428 ± 0.004 g | 0.437 ± 0.004 g | 0.358 ± 0.001 f |
TpC16 | 0.159 ± 0.003 a | 0.158 ± 0.001 e | 0.161 ± 0.001 h | 1.132 ± 0.055 f | 0.167 ± 0.005 a | 0.164 ± 0.001 h | 0.201 ± 0.003 c | 0.165 ± 0.003 h | 0.155 ± 0.003 g |
TpC8 | 0.194 ± 0.001 b | 0.191 ± 0.004 a | 0.189 ± 0.001 i | 1.255 ± 0.022 h,g | 0.193 ± 0.002 b | 0.193 ± 0.002 c | 0.235 ± 0.003 i | 0.180 ± 0.001 i | 0.162 ± 0.002 h,j |
TpC4 | 0.204 ± 0.002 f | 0.218 ± 0.001 e | 0.192 ± 0.002 i | 1.375 ± 0.066 i | 0.202 ± 0.004 b | 0.202 ± 0.001 e | 0.240 ± 0.002 i | 0.205 ± 0.003 j | 0.218 ± 0.004 i |
TpC2 | 0.204 ± 0.002 f | 0.244 ± 0.003 c | 0.223 ± 0.002 j | 1.364 ± 0.032 i | 0.226 ± 0.009 d,f | 0.227 ± 0.011 d | 0.269 ± 0.012 e,h | 0.255 ± 0.010 e | 0.234 ± 0.002 k |
TpB16 | 0.149 ± 0.002 h | 0.654 ± 0.020 i | 0.142 ± 0.001 k | 0.970 ± 0.024 j | 0.124 ± 0.003 g | 0.133 ± 0.002 i | 0.180 ± 0.002 j | 0.149 ± 0.001 k | 0.137 ± 0.002 l |
TpB8 | 0.161 ± 0.002 a | 0.699 ± 0.019 j | 0.145 ± 0.005 k | 1.200 ± 0.025 g | 0.146 ± 0.001 h | 0.140 ± 0.001 j | 0.223 ± 0.002 k | 0.141 ± 0.002 k | 0.136 ± 0.003 l |
TpB4 | 0.162 ± 0.001 a | 0.754 ± 0.008 k | 0.166 ± 0.001 l | 1.365 ± 0.090 i | 0.178 ± 0.004 b | 0.150 ± 0.002 k | 0.446 ± 0.008 k | 0.177 ± 0.003 l | 0.136 ± 0.005 l |
TpB2 | 0.167 ± 0.003 a,g | 0.778 ± 0.002 l | 0.171 ± 0.021 l | 1.507 ± 0.019 k | 0.187 ± 0.003 b | 0.172 ± 0.003 l | 0.380 ± 0.003 l | 0.635 ± 0.027 m | 0.156 ± 0.009 g,j |
TvL16 | 0.166 ± 0.002 a,g | 0.179 ± 0.001 m | 0.181 ± 0.002 m | 1.393 ± 0.050 i | 0.184 ± 0.007 b | 0.183 ± 0.000 b | 0.202 ± 0.002 c | 0.185 ± 0.004 n | 0.157 ± 0.004 g,j |
TvL8 | 0.227 ± 0.002 c | 0.210 ± 0.001 n | 0.206 ± 0.002 a | 1.219 ± 0.038 g | 0.220 ± 0.006 c,f | 0.211 ± 0.001 m | 0.195 ± 0.000 m | 0.209 ± 0.003 o | 0.167 ± 0.002 h |
TvL4 | 0.235 ± 0.002 f | 0.463 ± 0.014 o | 0.213 ± 0.005 e | 0.903 ± 0.018 l | 0.242 ± 0.002 d,i | 0.214 ± 0.003 m | 0.203 ± 0.002 c | 0.250 ± 0.001 e | 0.237 ± 0.002 m |
TvL2 | 0.234 ± 0.004 f | 0.462 ± 0.003 o | 0.260 ± 0.009 n | 0.828 ± 0.002 m | 0.267 ± 0.022 i | 0.221 ± 0.005 d | 0.255 ± 0.001 j,h | 0.282 ± 0.003 p | 0.268 ± 0.002 n |
M | 0.475 ± 0.005 i | 0.438 ± 0.031 o | 0.798 ± 0.050 o | 1.284 ± 0.005 g | 0.462 ± 0.021 e | 0.574 ± 0.021 m | 0.337 ± 0.002 n | 0.863 ± 0.005 q | 0.377 ± 0.004 o |
S. pyogenes (ATCC 19615) | S. aureus (ATCC 25923) | S. flexneri (ATCC 120022) | P. aeruginosa (ATCC 27853) | E. coli (ATCC 25922) | S. typhimurium (ATCC 140028) | H. influenzae type B (ATCC 100211) | C. parapsilopsis (ATCC 220019) | C. albicans (ATCC 100231) | |
---|---|---|---|---|---|---|---|---|---|
TgS | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 |
TgS | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 |
TgS | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 |
TgS | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
TpP | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 |
TpP | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 |
TpP | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 |
TpP | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
TpC | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 |
TpC | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 |
TpC | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 |
TpC | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
TpB | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 |
TpB | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 |
TpB | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 |
TpB | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
TvL | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 | 16 |
TvL | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 | 8 |
TvL | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 |
TvL | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Code | Analyzed Species | Location | Voucher Specimen Number | County | GPS Coordinates (Decimal Degree) | ||
---|---|---|---|---|---|---|---|
Altitude (m) | Latitude | Longitude | |||||
TgS | Thymus odoratissimus Mill. | Silagiu | VSNH.BUASTM: 1931 | Timis | 192 | 45.60703 | 21.60335 |
TgP | Thymus pulegioides L. | Prigor | VSNH.BUASTM: 1934 | Caras-Severin | 347 | 44.932547 | 22.115320 |
TgC | Thymus pulegioides L. | Carasova | VSNH.BUASTM: 1932 | Caras-Severin | 568 | 45.152790 | 21.878892 |
TgB | Thymus pulegioides L. | Bazias | VSNH.BUASTM: 1933 | Caras-Severin | 120 | 44.823742 | 21.387344 |
TvL | Thymus vulgaris L. | Lovrin | VSNH.BUASTM: 1927 | Timis | 91 | 45.975270 | 20.789621 |
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Beicu, R.; Alexa, E.; Obiștioiu, D.; Cocan, I.; Imbrea, F.; Pop, G.; Circioban, D.; Moisa, C.; Lupitu, A.; Copolovici, L.; et al. Antimicrobial Potential and Phytochemical Profile of Wild and Cultivated Populations of Thyme (Thymus sp.) Growing in Western Romania. Plants 2021, 10, 1833. https://doi.org/10.3390/plants10091833
Beicu R, Alexa E, Obiștioiu D, Cocan I, Imbrea F, Pop G, Circioban D, Moisa C, Lupitu A, Copolovici L, et al. Antimicrobial Potential and Phytochemical Profile of Wild and Cultivated Populations of Thyme (Thymus sp.) Growing in Western Romania. Plants. 2021; 10(9):1833. https://doi.org/10.3390/plants10091833
Chicago/Turabian StyleBeicu, Rodica, Ersilia Alexa, Diana Obiștioiu, Ileana Cocan, Florin Imbrea, Georgeta Pop, Denisa Circioban, Cristian Moisa, Andreea Lupitu, Lucian Copolovici, and et al. 2021. "Antimicrobial Potential and Phytochemical Profile of Wild and Cultivated Populations of Thyme (Thymus sp.) Growing in Western Romania" Plants 10, no. 9: 1833. https://doi.org/10.3390/plants10091833