Comparison of volatile profiles of Achillea sintenisii, an endemic species from Türkiye, and the evaluation of its essential oil's antibacterial and antibiofilm activities
Year 2025,
Volume: 12 Issue: 3, 645 - 656
Asli Can Agca
,
Nilüfer Vural
,
Sunasibel Rızvanoğlu
,
Müjde Eryılmaz
,
Murat Koç
Abstract
Achillea sintenisii Hub-Mor is an endemic species in Türkiye, characterized by 1–10 capitula and ray flowers, and it thrives on calcareous rocks or gypsum-rich soils. This study aimed to determine the chemical composition and assess the antibacterial and antibiofilm activity of the essential oil of A. sintenisii (AS-EO). The essential oil compounds of the flowering aerial part of A. sintenisii were extracted using both hydrodistillation and solid-phase microextraction (SPME) techniques and identified by gas chromatography-mass spectrometry (GC-MS). Two different adsorbents were employed in the SPME approach. The yield of the essential oil of flowering aerial parts of A. sintenisii was 0,.4% h/h. A total of 74, 112, and 78 compounds were identified from the samples obtained by hydrodistillation (S1) and SPME extraction using the CAR-PDMS (S2) and PDMS-DVB (S3) adsorbents, respectively. The AS-EO exhibited the highest antibacterial activity against Staphylococcus aureus ATCC 25923 and S. aureus ATCC 43300 (MRSA), with a minimum inhibitory concentration (MIC) of <1/512 for each bacterium. This strong antibacterial effect may be attributed to the high content of 1,8-cineole and l-borneol. However, AS-EO did not exhibit any antibiofilm activity. These findings suggest that the essential oil of A. sintenisii has potential as a natural antibacterial agent, warranting further research to uncover its full potential.
References
- Akkaoui, S., Johansson, A., Yagoubi, M., Haubek, D., El Hamidi, A., Rida, R., Claesson, R., & Ennibi, Q. (2020). Chemical composition, antimicrobial activity, in vitro cytotoxicity and leukotoxin neutralization of essential oil from Origanum vulgare against Aggregatibacter actinomycetemcomitans. Pathogens, 9(3), 192. https://doi.org/10.3390/pathogens9030192
- Asfour, H.Z. (2018). Anti-quorum sensing natural compounds. Journal of Microscopy and Ultrastructure, 6, 1-10. https://doi.org/10.4103/JMAU.JMAU_10_18
- Aytaç, Z., Duman, H., & Ekici, M. (2016). Two new Achillea L. (Asteraceae) species from Turkey. Turkish Journal of Botany, 40(4), 373-379. https://doi.org/10.3906/bot-1504-19
- Bader, A., AlQathama, A., Cioni, P.L., Ceccarini, L., Abdelhady, M.I.S., Al-Shareef, W., Ascrizzi, R., & Flamini, G. (2022). Essential oil biodiversity of Achillea ligustica All. obtained from mainland and island populations. Plants, 11, 1054. https://doi.org/10.3390/plants1108105
- Bali, E.B., Türkmen, K.E., Erdönmez, D., & Sağlam, N. (2019). Comparative study of inhibitory potential of dietary phytochemicals against quorum sensing activity of and biofilm formation by Chromobacterium violaceum 12472, and swimming and swarming behaviour of Pseudomonas aeruginosa PAO1. Food Technology and Biotechnology, 57(2), 212-221. https://doi.org/10.17113/ftb.57.02.19.5823
- Başer, K.H.C. (2016). Essential oils of Achillea species of Turkey. Natural Volatiles & Essential Oils, 3, 1-14.
- Becker, L., Bergfeld, W.F., Belsito, D.V., Hill, R.A., Klaassen, C.D., Liebler, D.C., Marks, J.G., Jr, Shank, R.C., Slaga, T.J., Snyder, P.W., & Andersen, F.A. (2016). Safety assessment of Achillea millefolium as used in cosmetics. International Journal of Toxicology, 35 (Supplement 3), 5S-15S. https://doi.org/10.1177/1091581816677717
- Cai, Z-M., Peng, J-Q., Chen, Y., Tao, L., Zhang, Y-Y., Fu, L-T., Long, Q-D., & Shen, X-C. (2020). 1,8-Cineole: a review of source, biological activities, and application. Journal of Asian Natural Products Research, 23(10), 938-954. https://doi.org/10.1080/10286020.2020.1839432
- Clinical and Laboratory Standards Institute. (2009). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard (8th ed.) (CLSI standard M07-A8). Clinical and Laboratory Standards Institute.
- Conforti, F., Loizzo, M.R., Statti, G.A., & Menichini, F. (2005). Comparative radical scavenging and antidiabetic activities of methanolic extract and fractions from Achillea ligustica ALL. Biological & Pharmaceutical Bulletin, 28, 1791–1794. https://doi.org/10.1248/bpb.28.1791
- Dorman, H.J.D., & Deans, S.G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88, 308–316. https://doi.org/10.1046/j.1365-2672.2000.00969.x
- European Medicine Agency- EMA. (2020, December 3). Millefolii herba. https://www.ema.europa.eu/en/medicines/herbal/millefolii-herba
- Eryılmaz, M., Kart, D., & Gürpınar, S.S. (2019). Vajinal floradan izole edilen Lactobacillus sp. metabolitlerinin antibiyofilm aktivitelerinin araştırılması [Investigation of antibiofilm activities of Lactobacillus sp. metabolites isolated from vaginal flora]. Turk Mikrobiyoloji Cemiyeti Dergisi, 49(3), 169-174. https://doi.org/10.5222/TMCD.2019.169
- Güner, A., Aslan, S., Ekim, T., Vural, M., & Babaç, M.T., (Eds.) (2012). Türkiye Bitkileri Listesi (Damarlı Bitkiler) [List of Türkiye plants-vascular plants]. Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği.
- Jardak, M., Mnif, S., Ayed, R.B., Rezgui, F., & Aifa, S. (2021). Chemical composition, antibiofilm activities of Tunisian spices essential oils and combinatorial effect against Staphylococcus epidermidis biofilm. LWT - Food Science and Technology, 140, 110691. https://doi.org/10.1016/j.lwt.2020.110691
- Karaca, B., Cihan, A.Ç., Akata, I., & Altuner, E.M. (2020). Anti-biofilm and antimicrobial activities of five edible and medicinal macrofungi samples on some biofilm producing multi-drug resistant Enterococcus strains. Turkish Journal of Agriculture - Food Science and Technology, 8, 69-80.
- Kataoka, H., Lord, H.L., & Pawliszyn, J. (2000). Applications of solid-phase microextraction in food analysis. Journal of Chromatography A, 880(1-2), 35-62. https://doi.org/10.1016/s0021-9673(00)00309-5
- Kordali, S., Cakir, A., Akcin, T.A., Mete, E., Akcin, A., Aydın, T., & Kiliç, H. (2009). Antifungal and herbicidal properties of essential oils and n-hexane extracts of Achillea gypsicola Hub-Mor. and Achillea biebersteinii Afan. (Asteraceae). Industrial Crops and Products, 29, 562-570. https://doi.org/10.1016/j.indcrop.2008.11.002
- Leite-Sampaio, N.F., Gondim, C.N.F.L., Souza, C.E.S., & Coutinho, H.D.M. (2022). Antibiotic potentiating action of α-pinene and borneol against EPEC and ETEC serotypes. Microbial Pathogenesis, 162, 105371. https://doi.org/10.1016/j.micpath.2021.105371
- Maffei, M., Germano, F., Doglia, G., & Chialva, F. (1993). Essential oils, chromosome numbers and karyotypes from Italian Achillea species. Part II. Journal of Essential Oil Research, 5, 61–70. https://doi.org/10.1080/10412905.1993.9698171
- Maggi, F., Bramucci, M., Cecchini, C., Coman, M.M., Cresci, A., Cristalli, G., Lupidi, G., Papa, F., Quassinti, L., Sagratini, G., & Vittori, S. (2009). Composition and biological activity of essential oil of Achillea ligustica All. (Asteraceae) naturalized in central Italy: Ideal candidate for anti-cariogenic formulations. Fitoterapia, 80, 313–319. https://doi.org/10.1016/j.fitote.2009.04.004
- Mazandarani, M., Mirdeilami, S.Z., & Pessarakli, M. (2013). Essential oil composition and antibacterial activity of Achillea millefolium L. from different regions in Northeast of Iran. Journal of Medicinal Plants Research, 7(16), 1063-1069. https://doi.org/10.5897/JMPR12.961
- Mohammadhosseini, M., Sarker, S.D., & Akbarzadeh, A. (2017). Chemical composition of the essential oils and extracts of Achillea species and their biological activities: A review. Journal of Ethnopharmacology, 199, 257-315. https://doi.org/10.1016/j.jep.2017.02.010
- Raut, J.S., & Karuppayil, S.M. (2014). A status review on the medicinal properties of essential oils. Industrial Crops and Products, 62, 250-64. https://doi.org/10.1016/j.indcrop.2014.05.055
- Sökmen, A., Vardar-Ünlü, G., Polissiou, M., Daferera, D., Sökmen, M., & Dönmez, E. (2003). Antimicrobial activity of essential oil and methanol extracts of Achillea sintenisii Hub. Mor. (Asteraceae). Phytotherapy Research, 17, 1005–1010. https://doi.org/10.1002/ptr.1274
- Strzępek-Gomółka, M., Gaweł-Bęben, K., & Kukula-Koch, W. (2021). Achillea species as sources of active phytochemicals for dermatological and cosmetic applications. Oxidative Medicine and Cellular Longevity, 2021, ID 6643827. https://doi.org/10.1155/2021/6643827
- Toplan, G.G., Taskın, T., İşcan, G., Göger, F., Kürkçüoğlu, M., Civaş, A., Ecevit-Genç, G., Mat, A., & Başer, K.H.C. (2022). Comparative studies on essential oil and phenolic content with in vitro antioxidant, anticholinesterase, antimicrobial activities of Achillea biebersteinii Afan. and A. millefolium subsp. millefolium Afan. L. growing in Eastern Turkey. Molecules, 27, 1956. https://doi.org/10.3390/molecules27061956
- Tunca-Pınarlı, Y., Benek, A., Turu, D., Bozyel, M.E., Canli, K., & Altuner, E.M. (2023). Biological activities and biochemical composition of endemic Achillea fraasii. Microorganisms, 11, 978. https://doi.org/10.3390/microorganisms11040978
- Turkmenoglu, F.P., Agar, O.T., Akaydin, G., Hayran, M., & Demirci, B. (2015). Characterization of volatile compounds of eleven Achillea species from Turkey and biological activities of essential oil and methanol extract of A. hamzaoglui Arabacı & Budak. Molecules, 20, 11432-11458. https://doi.org/10.3390/molecules200611432
- Tuzlacı, E. (2016). Türkiye bitkileri geleneksel ilaç rehberi [Traditional medicine guide to plants of Turkey]. İstanbul Medikal Yayıncılık.
- Vas, G., & Vekey, K. (2004). Solid-phase microextraction: a powerful sample preparation tool prior to mass spectrometric analysis. Journal of Mass Spectrometry, 39, 233–254. https://doi.org/10.1002/jms.606
- Wang, Y., Zhang, Y., Song, X., Fang, C., Xing, R., Liu, L., Zhao, X., Zou, Y., Li, L., Jia, R., Ye, G., Shi, F., Zhou, X., Zhang, Y., Wan, H., Wei, Q., & Yin, Z. (2022). 1,8-Cineole inhibits biofilm formation and bacterial pathogenicity by suppressing luxS gene expression in Escherichia coli. Frontiers in Pharmacology, 13, 988245. https://doi.org/10.3389/fphar.2022.988245
- World Health Organization. (2015). Antibiotic resistance: Multi-country public awareness survey. https://iris.who.int/bitstream/handle/10665/194460/9789241509817_eng.pdf
- Yeşilada, E. (2023). Halk hekimlerinin hazinesi, bilimsel referanslar ışığında Anadolu halk ilaçları envanteri [Treasure of folk medicine, Anatolian folk medicines inventory in the light of scientific references]. Hayygrup Yayıncılık.
Comparison of volatile profiles of Achillea sintenisii, an endemic species from Türkiye, and the evaluation of its essential oil's antibacterial and antibiofilm activities
Year 2025,
Volume: 12 Issue: 3, 645 - 656
Asli Can Agca
,
Nilüfer Vural
,
Sunasibel Rızvanoğlu
,
Müjde Eryılmaz
,
Murat Koç
Abstract
Achillea sintenisii Hub-Mor is an endemic species in Türkiye, characterized by 1–10 capitula and ray flowers, and it thrives on calcareous rocks or gypsum-rich soils. This study aimed to determine the chemical composition and assess the antibacterial and antibiofilm activity of the essential oil of A. sintenisii (AS-EO). The essential oil compounds of the flowering aerial part of A. sintenisii were extracted using both hydrodistillation and solid-phase microextraction (SPME) techniques and identified by gas chromatography-mass spectrometry (GC-MS). Two different adsorbents were employed in the SPME approach. The yield of the essential oil of flowering aerial parts of A. sintenisii was 0,.4% h/h. A total of 74, 112, and 78 compounds were identified from the samples obtained by hydrodistillation (S1) and SPME extraction using the CAR-PDMS (S2) and PDMS-DVB (S3) adsorbents, respectively. The AS-EO exhibited the highest antibacterial activity against Staphylococcus aureus ATCC 25923 and S. aureus ATCC 43300 (MRSA), with a minimum inhibitory concentration (MIC) of <1/512 for each bacterium. This strong antibacterial effect may be attributed to the high content of 1,8-cineole and l-borneol. However, AS-EO did not exhibit any antibiofilm activity. These findings suggest that the essential oil of A. sintenisii has potential as a natural antibacterial agent, warranting further research to uncover its full potential.
References
- Akkaoui, S., Johansson, A., Yagoubi, M., Haubek, D., El Hamidi, A., Rida, R., Claesson, R., & Ennibi, Q. (2020). Chemical composition, antimicrobial activity, in vitro cytotoxicity and leukotoxin neutralization of essential oil from Origanum vulgare against Aggregatibacter actinomycetemcomitans. Pathogens, 9(3), 192. https://doi.org/10.3390/pathogens9030192
- Asfour, H.Z. (2018). Anti-quorum sensing natural compounds. Journal of Microscopy and Ultrastructure, 6, 1-10. https://doi.org/10.4103/JMAU.JMAU_10_18
- Aytaç, Z., Duman, H., & Ekici, M. (2016). Two new Achillea L. (Asteraceae) species from Turkey. Turkish Journal of Botany, 40(4), 373-379. https://doi.org/10.3906/bot-1504-19
- Bader, A., AlQathama, A., Cioni, P.L., Ceccarini, L., Abdelhady, M.I.S., Al-Shareef, W., Ascrizzi, R., & Flamini, G. (2022). Essential oil biodiversity of Achillea ligustica All. obtained from mainland and island populations. Plants, 11, 1054. https://doi.org/10.3390/plants1108105
- Bali, E.B., Türkmen, K.E., Erdönmez, D., & Sağlam, N. (2019). Comparative study of inhibitory potential of dietary phytochemicals against quorum sensing activity of and biofilm formation by Chromobacterium violaceum 12472, and swimming and swarming behaviour of Pseudomonas aeruginosa PAO1. Food Technology and Biotechnology, 57(2), 212-221. https://doi.org/10.17113/ftb.57.02.19.5823
- Başer, K.H.C. (2016). Essential oils of Achillea species of Turkey. Natural Volatiles & Essential Oils, 3, 1-14.
- Becker, L., Bergfeld, W.F., Belsito, D.V., Hill, R.A., Klaassen, C.D., Liebler, D.C., Marks, J.G., Jr, Shank, R.C., Slaga, T.J., Snyder, P.W., & Andersen, F.A. (2016). Safety assessment of Achillea millefolium as used in cosmetics. International Journal of Toxicology, 35 (Supplement 3), 5S-15S. https://doi.org/10.1177/1091581816677717
- Cai, Z-M., Peng, J-Q., Chen, Y., Tao, L., Zhang, Y-Y., Fu, L-T., Long, Q-D., & Shen, X-C. (2020). 1,8-Cineole: a review of source, biological activities, and application. Journal of Asian Natural Products Research, 23(10), 938-954. https://doi.org/10.1080/10286020.2020.1839432
- Clinical and Laboratory Standards Institute. (2009). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard (8th ed.) (CLSI standard M07-A8). Clinical and Laboratory Standards Institute.
- Conforti, F., Loizzo, M.R., Statti, G.A., & Menichini, F. (2005). Comparative radical scavenging and antidiabetic activities of methanolic extract and fractions from Achillea ligustica ALL. Biological & Pharmaceutical Bulletin, 28, 1791–1794. https://doi.org/10.1248/bpb.28.1791
- Dorman, H.J.D., & Deans, S.G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88, 308–316. https://doi.org/10.1046/j.1365-2672.2000.00969.x
- European Medicine Agency- EMA. (2020, December 3). Millefolii herba. https://www.ema.europa.eu/en/medicines/herbal/millefolii-herba
- Eryılmaz, M., Kart, D., & Gürpınar, S.S. (2019). Vajinal floradan izole edilen Lactobacillus sp. metabolitlerinin antibiyofilm aktivitelerinin araştırılması [Investigation of antibiofilm activities of Lactobacillus sp. metabolites isolated from vaginal flora]. Turk Mikrobiyoloji Cemiyeti Dergisi, 49(3), 169-174. https://doi.org/10.5222/TMCD.2019.169
- Güner, A., Aslan, S., Ekim, T., Vural, M., & Babaç, M.T., (Eds.) (2012). Türkiye Bitkileri Listesi (Damarlı Bitkiler) [List of Türkiye plants-vascular plants]. Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği.
- Jardak, M., Mnif, S., Ayed, R.B., Rezgui, F., & Aifa, S. (2021). Chemical composition, antibiofilm activities of Tunisian spices essential oils and combinatorial effect against Staphylococcus epidermidis biofilm. LWT - Food Science and Technology, 140, 110691. https://doi.org/10.1016/j.lwt.2020.110691
- Karaca, B., Cihan, A.Ç., Akata, I., & Altuner, E.M. (2020). Anti-biofilm and antimicrobial activities of five edible and medicinal macrofungi samples on some biofilm producing multi-drug resistant Enterococcus strains. Turkish Journal of Agriculture - Food Science and Technology, 8, 69-80.
- Kataoka, H., Lord, H.L., & Pawliszyn, J. (2000). Applications of solid-phase microextraction in food analysis. Journal of Chromatography A, 880(1-2), 35-62. https://doi.org/10.1016/s0021-9673(00)00309-5
- Kordali, S., Cakir, A., Akcin, T.A., Mete, E., Akcin, A., Aydın, T., & Kiliç, H. (2009). Antifungal and herbicidal properties of essential oils and n-hexane extracts of Achillea gypsicola Hub-Mor. and Achillea biebersteinii Afan. (Asteraceae). Industrial Crops and Products, 29, 562-570. https://doi.org/10.1016/j.indcrop.2008.11.002
- Leite-Sampaio, N.F., Gondim, C.N.F.L., Souza, C.E.S., & Coutinho, H.D.M. (2022). Antibiotic potentiating action of α-pinene and borneol against EPEC and ETEC serotypes. Microbial Pathogenesis, 162, 105371. https://doi.org/10.1016/j.micpath.2021.105371
- Maffei, M., Germano, F., Doglia, G., & Chialva, F. (1993). Essential oils, chromosome numbers and karyotypes from Italian Achillea species. Part II. Journal of Essential Oil Research, 5, 61–70. https://doi.org/10.1080/10412905.1993.9698171
- Maggi, F., Bramucci, M., Cecchini, C., Coman, M.M., Cresci, A., Cristalli, G., Lupidi, G., Papa, F., Quassinti, L., Sagratini, G., & Vittori, S. (2009). Composition and biological activity of essential oil of Achillea ligustica All. (Asteraceae) naturalized in central Italy: Ideal candidate for anti-cariogenic formulations. Fitoterapia, 80, 313–319. https://doi.org/10.1016/j.fitote.2009.04.004
- Mazandarani, M., Mirdeilami, S.Z., & Pessarakli, M. (2013). Essential oil composition and antibacterial activity of Achillea millefolium L. from different regions in Northeast of Iran. Journal of Medicinal Plants Research, 7(16), 1063-1069. https://doi.org/10.5897/JMPR12.961
- Mohammadhosseini, M., Sarker, S.D., & Akbarzadeh, A. (2017). Chemical composition of the essential oils and extracts of Achillea species and their biological activities: A review. Journal of Ethnopharmacology, 199, 257-315. https://doi.org/10.1016/j.jep.2017.02.010
- Raut, J.S., & Karuppayil, S.M. (2014). A status review on the medicinal properties of essential oils. Industrial Crops and Products, 62, 250-64. https://doi.org/10.1016/j.indcrop.2014.05.055
- Sökmen, A., Vardar-Ünlü, G., Polissiou, M., Daferera, D., Sökmen, M., & Dönmez, E. (2003). Antimicrobial activity of essential oil and methanol extracts of Achillea sintenisii Hub. Mor. (Asteraceae). Phytotherapy Research, 17, 1005–1010. https://doi.org/10.1002/ptr.1274
- Strzępek-Gomółka, M., Gaweł-Bęben, K., & Kukula-Koch, W. (2021). Achillea species as sources of active phytochemicals for dermatological and cosmetic applications. Oxidative Medicine and Cellular Longevity, 2021, ID 6643827. https://doi.org/10.1155/2021/6643827
- Toplan, G.G., Taskın, T., İşcan, G., Göger, F., Kürkçüoğlu, M., Civaş, A., Ecevit-Genç, G., Mat, A., & Başer, K.H.C. (2022). Comparative studies on essential oil and phenolic content with in vitro antioxidant, anticholinesterase, antimicrobial activities of Achillea biebersteinii Afan. and A. millefolium subsp. millefolium Afan. L. growing in Eastern Turkey. Molecules, 27, 1956. https://doi.org/10.3390/molecules27061956
- Tunca-Pınarlı, Y., Benek, A., Turu, D., Bozyel, M.E., Canli, K., & Altuner, E.M. (2023). Biological activities and biochemical composition of endemic Achillea fraasii. Microorganisms, 11, 978. https://doi.org/10.3390/microorganisms11040978
- Turkmenoglu, F.P., Agar, O.T., Akaydin, G., Hayran, M., & Demirci, B. (2015). Characterization of volatile compounds of eleven Achillea species from Turkey and biological activities of essential oil and methanol extract of A. hamzaoglui Arabacı & Budak. Molecules, 20, 11432-11458. https://doi.org/10.3390/molecules200611432
- Tuzlacı, E. (2016). Türkiye bitkileri geleneksel ilaç rehberi [Traditional medicine guide to plants of Turkey]. İstanbul Medikal Yayıncılık.
- Vas, G., & Vekey, K. (2004). Solid-phase microextraction: a powerful sample preparation tool prior to mass spectrometric analysis. Journal of Mass Spectrometry, 39, 233–254. https://doi.org/10.1002/jms.606
- Wang, Y., Zhang, Y., Song, X., Fang, C., Xing, R., Liu, L., Zhao, X., Zou, Y., Li, L., Jia, R., Ye, G., Shi, F., Zhou, X., Zhang, Y., Wan, H., Wei, Q., & Yin, Z. (2022). 1,8-Cineole inhibits biofilm formation and bacterial pathogenicity by suppressing luxS gene expression in Escherichia coli. Frontiers in Pharmacology, 13, 988245. https://doi.org/10.3389/fphar.2022.988245
- World Health Organization. (2015). Antibiotic resistance: Multi-country public awareness survey. https://iris.who.int/bitstream/handle/10665/194460/9789241509817_eng.pdf
- Yeşilada, E. (2023). Halk hekimlerinin hazinesi, bilimsel referanslar ışığında Anadolu halk ilaçları envanteri [Treasure of folk medicine, Anatolian folk medicines inventory in the light of scientific references]. Hayygrup Yayıncılık.