Biological Activities and Biochemical Composition of Endemic Achillea fraasii

Yagmur Tunca-Pinarli1, Atakan Benek2, Dilay Turu1, Mustafa Eray Bozyel3*, Kerem Canlı4,5, Ergin Murat Altuner6

1Dokuz Eylül University, Graduate School of Natural and Applied Sciences, Department of Biology, Izmir, Türkiye
2Kastamonu University, Graduate School of Natural and Applied Sciences, Department of Biology, Kastamonu, Türkiye
3Canakkale Onsekiz Mart University, Faculty of Arts and Science, Department of Biology, Canakkale, Türkiye
4Dokuz Eylül University, Faculty of Science, Department of Biology, Izmir, Türkiye
5Dokuz Eylül University, Fauna and Flora Research and Application Center, Izmir, Türkiye
6Kastamonu University, Faculty of Science, Department of Biology, Kastamonu, Türkiye
* Corresponding author: m.eraybozyel@gmail.com

In this study, we investigated the antimicrobial, antioxidant, and antibiofilm activities and the biochemical composition of Achillea fraasii. The antimicrobial activity of A. fraasii ethanol extract (AFEt) was tested against 48 strains, and this is the first study testing the antimicrobial activity of this plant to this extent. The antioxidant activity was determined using the DPPH assay, and the antibiofilm activity of A. fraasii aqueous extract (AFAq) against five strains was assessed. The chemical composition of the plant extract was determined using GC-MS with artemisia ketone (19.41%) as the main component. The findings indicated that AFEt displayed antimicrobial activity against 38 strains, with a particular efficacy observed against various Staphylococcus aureus strains, such as S. aureus ATCC 25923, clinically isolated, multidrug resistant (MDR), and methicillin-resistant (MRSA) strains. In addition, the highest activity was observed against Enterococcus faecium. Moreover, the extract demonstrated activity against Candida strains. The plant extract also showed relatively good antioxidant activity compared to ascorbic acid, with an EC50 value of 55.52 µg/mL. However, AFAq acted as a biofilm activator against Escherichia coli ATCC 25922, increasing the biofilm formation by 2.63-fold. In conclusion, our study demonstrates the potential of A. fraasii as a source of antimicrobial and antioxidant agents.
Keywords: Achillea fraasii; antibacterial activity; antifungal activity; antioxidant activity; antibiofilm activity; GC-MS

How to cite: Tunca-Pinarli Y., Benek A., Turu D., Bozyel M.E., Canlı K., Altuner, E.M. (2023). Biological Activities and Biochemical Composition of Endemic Achillea fraasii. Microorganisms, 11(4): 978.

References
  • Abebe, G.M. The role of bacterial biofilm in antibiotic resistance and food contamination. Int. J. Microbiol. 2020, 2020, 1705814.
  • World Health Organization. Antimicrobial Resistance: Global Report on Surveillance; WHO Press: Geneva, Switzerland, 2014; Available online: http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf (accessed on 15 August 2019).
  • Batoni, G.; Maisetta, G.; Esin, S. Antimicrobial peptides and their interaction with biofilms of medically relevant bacteria. Biochim. Biophys. Acta Biomembr. 2016, 1858, 1044–1060.
  • Tewari, A.; Jain, B.; Dhamannapatil, P.S.; Saxena, M.K. Biofilm resistance to antimicrobial agents and novel approaches to combat biofilm mediated resistance in bacteria. EC Microbiol. 2018, 14, 71–77.
  • Koo, H.; Allan, R.N.; Howlin, R.P.; Stoodley, P.; Hall-Stoodley, L. Targeting microbial biofilms: Current and prospective therapeutic strategies. Nat. Rev. Microbiol. 2017, 15, 740–755.
  • Brackman, G.; Coenye, T. Quorum sensing inhibitors as anti-biofilm agents. Curr. Pharm. Des. 2015, 21, 5–11.
  • Tan, Z.; Deng, J.; Ye, Q.; Zhang, Z. The antibacterial activity of natural-derived flavonoids. Curr. Top. Med. Chem. 2022, 22, 1009–1019.
  • Ünal Turhan, E.; Erginkaya, Z.; Korukluoğlu, M.; Konuray, G. Beneficial Biofilm Applications in Food and Agricultural Industry. In Health and Safety Aspects of Food Processing Technologies; Springer: Cham, Switzerland, 2019; pp. 445–469.
  • Maurya, A.; Raj, A. Recent Advances in the Application of Biofilm in Bioremediation of Industrial Wastewater and Organic Pollutants. In Microorganisms for Sustainable Environment and Health; Elsevier: Amsterdam, The Netherlands, 2020; pp. 81–118.
  • Martelli, G.; Giacomini, D. Antibacterial and antioxidant activities for natural and synthetic dual-active compounds. Eur. J. Med. Chem. 2018, 158, 91–105.
  • Elliot, J.G. Application of antioxidant vitamins in foods and beverages. Food Technol. 1999, 53, 46–48.
  • El-Shiekh, R.A.; Al-Mahdy, D.A.; Hifnawy, M.S.; Abdel-Sattar, E.A. In-vitro screening of selected traditional medicinal plants for their anti-obesity and antioxidant activities. S. Afr. J. Bot. 2019, 123, 43–50.
  • Pandey, A.K.; Kumar, S. Perspective on plant products as antimicrobial agents: A review. Pharmacologia 2013, 4, 469–480.
  • Vaou, N.; Stavropoulou, E.; Voidarou, C.; Tsigalou, C.; Bezirtzoglou, E. Towards advances in medicinal plant antimicrobial activity: A review study on challenges and future perspectives. Microorganisms 2021, 9, 2041.
  • Arabacı, T. The Revision of Achillea L. (Asteraceae) Genus Grown in Turkey. Ph.D. Thesis, Inönü University, Malatya, Turkey, 2006.
  • Oladosu, I.A.; Usman, L.A.; Olawore, N.O.; Atata, R.F. Antibacterial activity of rhizomes essential oils of two types of Cyperus articulatus growing in Nigeria. Adv. Biol. Res. 2011, 5, 179–183.
  • Magiatis, P.; Skaltsounis, A.L.; Chinou, I.; Haroutounian, S.A. Chemical composition and in-vitro antimicrobial activity of the essential oils of three Greek Achillea species. Z. Naturforsch. C Bio. Sci. 2002, 57, 287–290.
  • Zafar, M.M.I.; Hassan, F.; Naqvi, S.B.S.; Muhammad, S.; Hasan, F.; Jabeen, S.; Israr, F. Evaluation of antibacterial activity of camphor, benzoin, cubebs, fenugreek, apricot and cinnamon leaf against standard cultures and clinical isolates of an array of organisms. J. Pharmacol. 2019, 36, 69–75.
  • Mensor, L.L.; Menezes, F.S.; Leitão, G.G.; Reis, A.S.; Santos, T.C.D.; Coube, C.S.; Leitão, S.G. Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytother. Res. 2001, 15, 127–130.
  • Karaca, B.; Cihan, A.Ç.; Akata, I.; Altuner, E.M. Anti-biofilm and antimicrobial activities of five edible and medicinal macrofungi samples on some biofilm producing multi drug resistant Enterococcus strains. Turk. J. Agri. Food Sci. Technol. 2020, 8, 69–80.
  • Bharat, C.R.; Krishna, G.D. GC-MS analysis of young leaves of Allophylus cobbe (L.) raeusch. and Allophylus serratus (Roxb.) Kurz. Indian J. Pharm. Educ. Res. 2017, 51, 472–479.
  • Rashid, S.; Rather, M.A.; Shah, W.A.; Bhat, B.A. Chemical composition, antimicrobial, cytotoxic and antioxidant activities of the essential oil of Artemisia indica Willd. Food Chem. 2013, 138, 693–700.
  • Setzer, W.N.; Vogler, B.; Schmidt, J.M.; Leahy, J.G.; Rives, R. Antimicrobial activity of Artemisia douglasiana leaf essential oil. Fitoterapia 2004, 75, 192–200.
  • Mulyaningsih, S.; Sporer, F.; Zimmermann, S.; Reichling, J.; Wink, M. Synergistic properties of the terpenoids aromadendrene and 1, 8-cineole from the essential oil of Eucalyptus globulus against antibiotic-susceptible and antibiotic-resistant pathogens. Phytomedicine 2010, 17, 1061–1066.
  • Türkez, H.; Çelik, K.; Toğar, B. Effects of copaene, a tricyclic sesquiterpene, on human lymphocytes cells in vitro. Cytotechnology 2014, 66, 597–603.
  • Landoulsi, A.; Hennebelle, T.; Bero, J.; Rivière, C.; Sahpaz, S.; Quetin-Leclercq, J.; Neut, J.; Benhamida, J.; Roumy, V. Antimicrobial and Light-Enhanced Antimicrobial Activities, Cytotoxicity and Chemical Variability of All Tunisian Eryngium Species. Chem. Biodivers. 2020, 17, e1900543.
  • Al-Rajhi, A.M.H.; Qanash, H.; Almuhayawi, M.S.; Al Jaouni, S.K.; Bakri, M.M.; Ganash, M.; Salama, H.M.; Selim, S.; Abdelghany, T.M. Molecular interaction studies and phytochemical characterization of Mentha pulegium L. constituents with multiple biological utilities as antioxidant, antimicrobial, anticancer and anti-hemolytic agents. Molecules 2022, 27, 4824.
  • Aparna, V.; Dileep, K.V.; Mandal, P.K.; Karthe, P.; Sadasivan, C.; Haridas, M. Anti-inflammatory property of n-hexadecanoic acid: Structural evidence and kinetic assessment. Chem. Biol. Drug Des. 2012, 80, 434–439.
  • Abubakar, M.N.; Majinda, R.R.T. GC-MS Analysis and preliminary antimicrobial activity of Albizia adianthifolia (Schumach) and Pterocarpus angolensis (DC). Medicines 2016, 3, 3.
  • Bruno, F.; Castelli, G.; Migliazzo, A.; Piazza, M.; Galante, A.; Verde, V.L.; Calderone, S.; Nucatolo, G.; Vitale, F. Cytotoxic screening and in vitro evaluation of pentadecane against Leishmania infantum promastigotes and amastigotes. J. Parasitol. 2015, 101, 701–705.
  • Vanitha, V.; Vijayakumar, S.; Nilavukkarasi, M.; Punitha, V.N.; Vidhya, E.; Praseetha, P.K. Heneicosane-A novel microbicidal bioactive alkane identified from Plumbago zeylanica L. Ind. Crops. Prod. 2020, 154, 112748.
  • Algammal, A.M.; Hetta, H.F.; Elkelish, A.; Alkhalifah, D.H.H.; Hozzein, W.N.; Batiha, G.E.S.; El Nahas, N.; Mabrok, M.A. Methicillin-Resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect. Drug Resist. 2020, 13, 3255–3265.
  • Tigabu, A.; Getaneh, A. Staphylococcus aureus, ESKAPE bacteria challenging current health care and community settings: A literature review. Clin. Lab. 2021, 67, 1539–1549.
  • Nami, S.; Mohammadi, R.; Vakili, M.; Khezripour, K.; Mirzaei, H.; Morovati, H. Fungal vaccines, mechanism of actions and immunology: A comprehensive review. Biomed. Pharmacother. 2019, 109, 333–344.
  • Pristov, K.E.; Ghannoum, M.A. Resistance of Candida to azoles and echinocandins worldwide. Clin. Microbiol. Infect. 2019, 25, 792–798.
  • Barış, D.; Kızıl, M.; Aytekin, Ç.; Kızıl, G.; Yavuz, M.; Çeken, B.; Ertekin, A.S. In vitro antimicrobial and antioxidant activity of ethanol extract of three Hypericum and three Achillea species from Turkey. Int. J. Food Prop. 2011, 14, 339–355.
  • Çolak, S.; Dağlı, F.; Çömlekcioğlu, N.; Kocabaş, Y.Z.; Aygan, A. Antimicrobial Activity and Some Phytochemical Properties of Extracts Obtained from Different Organs of Achillea aleppica subsp. aleppica. Gıda 2020, 45, 929–941.
  • World Health Organization. Report on the Burden of Endemic Health Care-Associated Infection Worldwide; World Health Organization: Geneva, Switzerland, 2011.
  • O’Toole, R.F.; Leong, K.W.; Cumming, V.; van Hal, S.J. Vancomycin-Resistant Enterococcus faecium and the Emergence of New Sequence Types Associated with Hospital Infection. Res. Microbiol. 2023, 174, 104046.
  • Anraku, M.; Gebicki, J.M.; Iohara, D.; Tomida, H.; Uekama, K.; Maruyama, T.; Hirayama, F.; Otagiri, M. Antioxidant activities of chitosans and its derivatives in in vitro and in vivo studies. Carbohydr. Polym. 2018, 199, 141–149.
  • Munteanu, I.G.; Apetrei, C. Analytical methods used in determining antioxidant activity: A review. Int. J. Mol. Sci. 2021, 22, 3380.
  • Samoilova, Z.; Muzyka, N.; Lepekhina, E.; Oktyabrsky, O.; Smirnova, G. Medicinal plant extracts can variously modify biofilm formation in Escherichia coli. Antonie Van Leeuwenhoek 2014, 105, 709–722.
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