Antimicrobial and antibiofilm studies on three endemic species of Verbascum L. (Scrophulariaceae) in Türkiye
Year 2024,
Volume: 11 Issue: 3, 543 - 550, 29.08.2024
Pervin Soyer
,
Sevim Küçük
,
Yağmur Tunalı
Abstract
The consumption of traditional medicinal herbs has gained popularity as a viable alternative approach for addressing microbial infections or infectious structures. In this study, Verbascum detersile, Verbascum eskisehirensis, and Verbascum gypsicola endemic species belonging to the Scrophulariaceae family, spreading in Eskişehir and its surroundings, were collected from natural habitats and evaluated in terms of antimicrobial and antibiofilm activities. In biological activity studies, different concentrations of three plant extracts showed various antimicrobial and antibiofilm activities on selected standard microorganism cultures (Staphylococcus aureus ATCC 29213, Staphylococcus epidermidis ATCC 14990, Pseudomonas aeruginosa ATCC 27853, Candida albicans ATCC 90028, and Candida krusei ATCC 6258). It was observed that the selected three endemic Verbascum extracts had a minimum inhibitory and minimum biofilm eradication concentration value of 1250 μg/mL.
Thanks
The present work received financial support from the Anadolu University Scientific Research Projects. The assigned project identifier is 1902S009. We express our sincere gratitude for the generous financial assistance provided. The authors express their gratitude to Merve HAS for their assistance in the preparation of plant materials.
References
- Amirnia, R., Khoshnoud, H., Alahyary, P., Ghiyasi, M., Tajbakhsh, M., & Valizadegan, O. (2011). Antimicrobial activity of Verbascum speciosum against three bacteria strains. Fresenius Environmental Bulletin, 20(3).
- Clinical and Laboratory Standards Institute M27-A2. (2002). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard-Second Edition, CLSI document 2002a; 22(15).
- Clinical and Laboratory Standards Institute M07-A9. (2012). Reference Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard- Ninth Edition, CLSI document M07-A9 2012; 29(2).
- Cruz, C.D., Shah, S., & Tammela, P. (2018). Defining conditions for biofilm inhibition and eradication assays for Gram-positive clinical reference strains. BMC microbiology, 18(1), 1-9. https://doi.org/10.1186/s12866-018-1321-6
- Duman, H., Uzunhisarcıklı, M.E., & Özbek, F. (2020). A new species of Verbascum (Scrophulariacae) from western Türkiye. Botany Letters, 167(4), 409–416. https://doi.org/10.1080/23818107.2020.1796782
- Dülger, B., Kirmizi, S., Arslan, H., & Güleryüz, G. (2002). Antimicrobial Activity of Three Endemic Verbascum Species. Pharmaceutical Biology, 40(8), 587 589. https://doi.org/10.1076/phbi.40.8.587.14657
- EMA. (2021). Verbasci flos - European Medicines Agency. European Medicines Agency. https://www.ema.europa.eu/en/medicines/herbal/verbasci-flos
- Escobar, F.M., Sabini, M.C., Zanon, S.M., Tonn, C.E., & Sabini, L.I. (2012). Antiviral effect and mode of action of methanolic extract of Verbascum thapsus L. on pseudorabies virus (strain RC/79). Natural Product Research, 26(17), 1621 1625. https://doi.org/10.1080/14786419.2011.576394
- Ferraro, M.J. (2000). Performance Standards for Antimicrobial Disk Susceptibility Tests.
- Georgiev, M., Alipieva, K., Orhan, I., Abrashev, R., Denev, P., & Angelova, M. (2011). Antioxidant and cholinesterases inhibitory activities of Verbascum xanthophoeniceum Griseb. and its phenylethanoid glycosides. Food Chemistry, 128(1), 100–105. https://doi.org/10.1016/j.foodchem.2011.02.083
- Ghorbani, A. (2005). Studies on pharmaceutical ethnobotany in the region of Turkmen Sahra, north of Iran. Journal of Ethnopharmacology, 102(1), 58 68. https://doi.org/10.1016/j.jep.2005.05.035
- Gökmen, A. (2021). Phytochemical and Biological Investigations on Verbascum bugulıfolıum L. [Doctoral dissertation]. Yeditepe University.
- Göse, M., & Doğru, N.H. (2019). Antibiofilm activity of Verbascum pinnatifidum Vahl. ethanolic extract. Biologica Nyssana, 10(2). https://doi.org/10.5281/zenodo.3600197
- Göse, M., & Hacıoğlu, N. (2021). Bioactive compounds, antimicrobial and antibiofilm activity of two Verbascum species. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 24(3), 479-487. https://doi.org/10.18016/ksutarimdoga.v24i60916.750034
- Grant, S.S., & Hung, D.T. (2013). Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence, 4(4), 273–283. https://doi.org/10.4161/viru.23987
- Grigorov, M., Pavlović, D., Mladenović, A.S., Tasić, K.M., & Ilić, D. (2023). In vitro antimicrobial activity of different Verbascum niveum extracts. Acta facultatis medicae Naissensis, 40(2), 193-198. https://doi.org/10.5937/afmnai40-40582
- Hunt, C. (2009). Mabberley’s Plant‐Book: A Portable Dictionary of Plants, their Classifications and Uses (3rd edition)2009175David. J. Mabberley. Mabberley’s Plant‐Book: A Portable Dictionary of Plants, their Classifications and Uses (3rd edition). Cambridge: Cambridge University Press 2008. xviii+1021 pp., ISBN: 978 0 521 82071 4 £50, $90. Reference Reviews, 23(4), 35–36. https://doi.org/10.1108/09504120910958511
- Karavelioğulları, A.F., Ocak, A., Ekici, M., & Cabi, E. (2009). Verbascum eskisehirensis sp. nov. (Scrophulariaceae) from central Anatolia, Türkiye. Nordic Journal of Botany, 27(3), 222–227. https://doi.org/10.1111/j.1756-1051.2008.00250.x
- Karavelioğulları, F.A. Verbascum L. In: Güner, A. Aslan, S. Ekim, T. Vural, M., & Babaç, M. T. (eds.). (2012). Türkiye Bitkileri Listesi (Damarlı Bitkiler). Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği Yayını, İstanbul, pp. 850-870.
- Kargıoğlu, M., Cenkci, S., Serteser, A., Evliyaoğlu, N., Konuk, M., Kök, M.A., & Bağcı, Y. (2008). An Ethnobotanical Survey of Inner-West Anatolia, Türkiye. Human Ecology, 36(5), 763–777. https://doi.org/10.1007/s10745-008-9198-x
- Khafagi, I.K. (2002). Screening in vitro cultures of some Sinai medicinal plants for their antibiotic activity. Egyptian Journal of Microbiology (Egypt).
- Knobloch, J.K.M., Bartscht, K., Sabottke, A., Rohde, H., Feucht, H.H., & Mack, D. (2001). Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. Journal of Bacteriology, 183(8), 2624 2633. https://doi.org/10.1128/jb.183.8.2624-2633.2001
- Küçük, S., Özdemir, F., İşcan, G., & İncesu, Z. (2016). Determination of Cytotoxic and Anticandidal Activities of Three Verbascum L. Species from Türkiye: V. cheiranthifolium Boiss. var. asperulum (Boiss.) Murb. Monorg., V. pycnostachyum Boiss. & Heldr and V. orgyale Boiss. & Heldr. Turkish Journal of Pharmaceutical Sciences, 13(3), 318–322. https://doi.org/10.4274/tjps.2016.06
- Mohamadi, N., Sharififar, F., Koohpayeh, A., & Daneshpajouh, M. (2015). Traditional and Ethnobotanical uses of medicinal plants by ancient populations in Khabr and Rouchon of Iran. Journal of Applied Pharmaceutical Science, 101 107. https://doi.org/10.7324/japs.2015.501117
- Mükemre, M., Behçet, L., & Çakılcıoğlu, U. (2015, May). Ethnobotanical study on medicinal plants in villages of Çatak (Van-Türkiye). Journal of Ethnopharmacology, 166, 361–374. https://doi.org/10.1016/j.jep.2015.03.040
- Ocak, E., İnci, Ş., Öztürk, D., Şafak, S. A., Özdeniz, E., Kırbağ, S., ... & Kurt, L. (2021). Antimicrobial activities of some narrow endemic gypsopyhte. İstanbul Journal of Pharmacy, 51(1), 118-122. https://doi.org/10.26650/IstanbulJPharm.2020.0084
- Öztürk, D., Sezer, O., Koyuncu, O., & Ocak, A. (2018). Flora of gypsiferous and marl soils in Eskisehir (Türkiye). Biological Diversity and Conservation, 11(2), 137-15.
- Öztürk, G., Ağalar, H., Yildiz, G., Göger, F., & Kırımer, N. (2019). Biological activities and luteolin derivatives of Verbascum eskisehirensis Karavel., Ocak & Ekici. Journal of Research in Pharmacy, 23(3). https://doi.org/10.12991/jrp.2019.160
- Saltan, F.Z., Sokmen, M., Akin, M., Saracoglu, H.T., Gokturk, R.S., Ahmad, M., ... & Shah, M.R. (2011). Antimicrobial and antioxidant activities of phenolic compound extracted from new Verbascum species growing in Türkiye. Journal of the Chemical Society of Pakistan, 33(5),764 771. https://inis.iaea.org/search/search.aspx?orig_q=RN:43027999
- Sánchez, E., Rivas Morales, C., Castillo, S., Leos-Rivas, C., García-Becerra, L., & Ortiz Martínez, D. M. (2016). Antibacterial and Antibiofilm Activity of Methanolic Plant Extracts against Nosocomial Microorganisms. Evidence-Based Complementary and Alternative Medicine, 2016, 1–8. https://doi.org/10.1155/2016/1572697
- Senatore, F., Rigano, D., Formisano, C., Grassia, A., Basile, A., & Sorbo, S. (2007). Phytogrowth-inhibitory and antibacterial activity of Verbascum sinuatum. Fitoterapia, 78(3), 244–247. https://doi.org/10.1016/j.fitote.2006.11.010
- Süntar, I., Tatlı, I.I., Küpeli Akkol, E., Keleş, H., Kahraman, I., & Akdemir, Z. (2010). An ethnopharmacological study on Verbascum species: From conventional wound healing use to scientific verification. Journal of Ethnopharmacology, 132(2), 408 413. https://doi.org/10.1016/j.jep.2010.08.004
- Vural, M., & Aydoğdu, M. (1993). A new species from central Anatolia Verbascum gypsicola (Scrophulariaceae). The Karaca Arboretum Magazine, 2(2), 75-78.
Antimicrobial and antibiofilm studies on three endemic species of Verbascum L. (Scrophulariaceae) in Türkiye
Year 2024,
Volume: 11 Issue: 3, 543 - 550, 29.08.2024
Pervin Soyer
,
Sevim Küçük
,
Yağmur Tunalı
Abstract
The consumption of traditional medicinal herbs has gained popularity as a viable alternative approach for addressing microbial infections or infectious structures. In this study, Verbascum detersile, Verbascum eskisehirensis, and Verbascum gypsicola endemic species belonging to the Scrophulariaceae family, spreading in Eskişehir and its surroundings, were collected from natural habitats and evaluated in terms of antimicrobial and antibiofilm activities. In biological activity studies, different concentrations of three plant extracts showed various antimicrobial and antibiofilm activities on selected standard microorganism cultures (Staphylococcus aureus ATCC 29213, Staphylococcus epidermidis ATCC 14990, Pseudomonas aeruginosa ATCC 27853, Candida albicans ATCC 90028, and Candida krusei ATCC 6258). It was observed that the selected three endemic Verbascum extracts had a minimum inhibitory and minimum biofilm eradication concentration value of 1250 μg/mL.
References
- Amirnia, R., Khoshnoud, H., Alahyary, P., Ghiyasi, M., Tajbakhsh, M., & Valizadegan, O. (2011). Antimicrobial activity of Verbascum speciosum against three bacteria strains. Fresenius Environmental Bulletin, 20(3).
- Clinical and Laboratory Standards Institute M27-A2. (2002). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard-Second Edition, CLSI document 2002a; 22(15).
- Clinical and Laboratory Standards Institute M07-A9. (2012). Reference Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard- Ninth Edition, CLSI document M07-A9 2012; 29(2).
- Cruz, C.D., Shah, S., & Tammela, P. (2018). Defining conditions for biofilm inhibition and eradication assays for Gram-positive clinical reference strains. BMC microbiology, 18(1), 1-9. https://doi.org/10.1186/s12866-018-1321-6
- Duman, H., Uzunhisarcıklı, M.E., & Özbek, F. (2020). A new species of Verbascum (Scrophulariacae) from western Türkiye. Botany Letters, 167(4), 409–416. https://doi.org/10.1080/23818107.2020.1796782
- Dülger, B., Kirmizi, S., Arslan, H., & Güleryüz, G. (2002). Antimicrobial Activity of Three Endemic Verbascum Species. Pharmaceutical Biology, 40(8), 587 589. https://doi.org/10.1076/phbi.40.8.587.14657
- EMA. (2021). Verbasci flos - European Medicines Agency. European Medicines Agency. https://www.ema.europa.eu/en/medicines/herbal/verbasci-flos
- Escobar, F.M., Sabini, M.C., Zanon, S.M., Tonn, C.E., & Sabini, L.I. (2012). Antiviral effect and mode of action of methanolic extract of Verbascum thapsus L. on pseudorabies virus (strain RC/79). Natural Product Research, 26(17), 1621 1625. https://doi.org/10.1080/14786419.2011.576394
- Ferraro, M.J. (2000). Performance Standards for Antimicrobial Disk Susceptibility Tests.
- Georgiev, M., Alipieva, K., Orhan, I., Abrashev, R., Denev, P., & Angelova, M. (2011). Antioxidant and cholinesterases inhibitory activities of Verbascum xanthophoeniceum Griseb. and its phenylethanoid glycosides. Food Chemistry, 128(1), 100–105. https://doi.org/10.1016/j.foodchem.2011.02.083
- Ghorbani, A. (2005). Studies on pharmaceutical ethnobotany in the region of Turkmen Sahra, north of Iran. Journal of Ethnopharmacology, 102(1), 58 68. https://doi.org/10.1016/j.jep.2005.05.035
- Gökmen, A. (2021). Phytochemical and Biological Investigations on Verbascum bugulıfolıum L. [Doctoral dissertation]. Yeditepe University.
- Göse, M., & Doğru, N.H. (2019). Antibiofilm activity of Verbascum pinnatifidum Vahl. ethanolic extract. Biologica Nyssana, 10(2). https://doi.org/10.5281/zenodo.3600197
- Göse, M., & Hacıoğlu, N. (2021). Bioactive compounds, antimicrobial and antibiofilm activity of two Verbascum species. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 24(3), 479-487. https://doi.org/10.18016/ksutarimdoga.v24i60916.750034
- Grant, S.S., & Hung, D.T. (2013). Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence, 4(4), 273–283. https://doi.org/10.4161/viru.23987
- Grigorov, M., Pavlović, D., Mladenović, A.S., Tasić, K.M., & Ilić, D. (2023). In vitro antimicrobial activity of different Verbascum niveum extracts. Acta facultatis medicae Naissensis, 40(2), 193-198. https://doi.org/10.5937/afmnai40-40582
- Hunt, C. (2009). Mabberley’s Plant‐Book: A Portable Dictionary of Plants, their Classifications and Uses (3rd edition)2009175David. J. Mabberley. Mabberley’s Plant‐Book: A Portable Dictionary of Plants, their Classifications and Uses (3rd edition). Cambridge: Cambridge University Press 2008. xviii+1021 pp., ISBN: 978 0 521 82071 4 £50, $90. Reference Reviews, 23(4), 35–36. https://doi.org/10.1108/09504120910958511
- Karavelioğulları, A.F., Ocak, A., Ekici, M., & Cabi, E. (2009). Verbascum eskisehirensis sp. nov. (Scrophulariaceae) from central Anatolia, Türkiye. Nordic Journal of Botany, 27(3), 222–227. https://doi.org/10.1111/j.1756-1051.2008.00250.x
- Karavelioğulları, F.A. Verbascum L. In: Güner, A. Aslan, S. Ekim, T. Vural, M., & Babaç, M. T. (eds.). (2012). Türkiye Bitkileri Listesi (Damarlı Bitkiler). Nezahat Gökyiğit Botanik Bahçesi ve Flora Araştırmaları Derneği Yayını, İstanbul, pp. 850-870.
- Kargıoğlu, M., Cenkci, S., Serteser, A., Evliyaoğlu, N., Konuk, M., Kök, M.A., & Bağcı, Y. (2008). An Ethnobotanical Survey of Inner-West Anatolia, Türkiye. Human Ecology, 36(5), 763–777. https://doi.org/10.1007/s10745-008-9198-x
- Khafagi, I.K. (2002). Screening in vitro cultures of some Sinai medicinal plants for their antibiotic activity. Egyptian Journal of Microbiology (Egypt).
- Knobloch, J.K.M., Bartscht, K., Sabottke, A., Rohde, H., Feucht, H.H., & Mack, D. (2001). Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. Journal of Bacteriology, 183(8), 2624 2633. https://doi.org/10.1128/jb.183.8.2624-2633.2001
- Küçük, S., Özdemir, F., İşcan, G., & İncesu, Z. (2016). Determination of Cytotoxic and Anticandidal Activities of Three Verbascum L. Species from Türkiye: V. cheiranthifolium Boiss. var. asperulum (Boiss.) Murb. Monorg., V. pycnostachyum Boiss. & Heldr and V. orgyale Boiss. & Heldr. Turkish Journal of Pharmaceutical Sciences, 13(3), 318–322. https://doi.org/10.4274/tjps.2016.06
- Mohamadi, N., Sharififar, F., Koohpayeh, A., & Daneshpajouh, M. (2015). Traditional and Ethnobotanical uses of medicinal plants by ancient populations in Khabr and Rouchon of Iran. Journal of Applied Pharmaceutical Science, 101 107. https://doi.org/10.7324/japs.2015.501117
- Mükemre, M., Behçet, L., & Çakılcıoğlu, U. (2015, May). Ethnobotanical study on medicinal plants in villages of Çatak (Van-Türkiye). Journal of Ethnopharmacology, 166, 361–374. https://doi.org/10.1016/j.jep.2015.03.040
- Ocak, E., İnci, Ş., Öztürk, D., Şafak, S. A., Özdeniz, E., Kırbağ, S., ... & Kurt, L. (2021). Antimicrobial activities of some narrow endemic gypsopyhte. İstanbul Journal of Pharmacy, 51(1), 118-122. https://doi.org/10.26650/IstanbulJPharm.2020.0084
- Öztürk, D., Sezer, O., Koyuncu, O., & Ocak, A. (2018). Flora of gypsiferous and marl soils in Eskisehir (Türkiye). Biological Diversity and Conservation, 11(2), 137-15.
- Öztürk, G., Ağalar, H., Yildiz, G., Göger, F., & Kırımer, N. (2019). Biological activities and luteolin derivatives of Verbascum eskisehirensis Karavel., Ocak & Ekici. Journal of Research in Pharmacy, 23(3). https://doi.org/10.12991/jrp.2019.160
- Saltan, F.Z., Sokmen, M., Akin, M., Saracoglu, H.T., Gokturk, R.S., Ahmad, M., ... & Shah, M.R. (2011). Antimicrobial and antioxidant activities of phenolic compound extracted from new Verbascum species growing in Türkiye. Journal of the Chemical Society of Pakistan, 33(5),764 771. https://inis.iaea.org/search/search.aspx?orig_q=RN:43027999
- Sánchez, E., Rivas Morales, C., Castillo, S., Leos-Rivas, C., García-Becerra, L., & Ortiz Martínez, D. M. (2016). Antibacterial and Antibiofilm Activity of Methanolic Plant Extracts against Nosocomial Microorganisms. Evidence-Based Complementary and Alternative Medicine, 2016, 1–8. https://doi.org/10.1155/2016/1572697
- Senatore, F., Rigano, D., Formisano, C., Grassia, A., Basile, A., & Sorbo, S. (2007). Phytogrowth-inhibitory and antibacterial activity of Verbascum sinuatum. Fitoterapia, 78(3), 244–247. https://doi.org/10.1016/j.fitote.2006.11.010
- Süntar, I., Tatlı, I.I., Küpeli Akkol, E., Keleş, H., Kahraman, I., & Akdemir, Z. (2010). An ethnopharmacological study on Verbascum species: From conventional wound healing use to scientific verification. Journal of Ethnopharmacology, 132(2), 408 413. https://doi.org/10.1016/j.jep.2010.08.004
- Vural, M., & Aydoğdu, M. (1993). A new species from central Anatolia Verbascum gypsicola (Scrophulariaceae). The Karaca Arboretum Magazine, 2(2), 75-78.