Determination of antimicrobial and anti-MRSA activities of Cladonia foliacea extracts

Öz

This study aims to determine the antimicrobial activity of methanol and ethanol extracts of Cladonia foliacea (Huds.) Willd. against pathogenic standard microorganisms and the anti-MRSA activity against clinical MRSA strains. Minimum Inhibitory Concentrations (MIC) were determined by the broth microdilution method. All strains were exposed to concentrations of extracts between 12.5-0.006 mg/ml. Methanol and ethanol extracts were found to have antibacterial activity against standard bacterial strains at doses of 0.01-6.25 mg/ml. The most effective strain for both extracts was the Bacillus cereus strain with an MIC value of 0.01 mg/ml. It was observed that the extracts had a higher effect on gram-positive bacteria than gram-negative bacteria. The MIC values of ethanol and methanol extract against Candida albicans yeast strain were calculated as 0.39 mg/ml and 0.78 mg/ml, respectively. In addition, it was found in the study that both extracts showed very high anti-MRSA activity against all clinical MRSA strains at doses of 0.01-6.25 mg/ml. It can be said that this species can be a natural source of antimicrobial agents and can be used as an alternative in the treatment of MRSA strains.

Anahtar Kelimeler

• Antimicrobial activity
• Anti-MRSA
• Lichen
• Methicillin resistance Staphylococcus aureus

Cladonia foliacea ekstraktlarının antimikrobiyal ve anti-MRSA aktivitelerinin belirlenmesi

Öz

Bu çalışmanın amacı Cladonia foliacea (Huds.) Willd.’in metanol ve etanol ekstraktlarının patojen standart mikroorganizmalara karşı antimikrobiyal aktivitesini ve klinik MRSA suşlarına karşı anti-MRSA aktivitesinin belirlenmesidir. Minimum İnhibisyon Konsantrasyonları (MİK) sıvı mikrodilüsyon metoduyla saptanmıştır. Tüm suşlar ekstraktların 12,5-0,006 mg/ml arasındaki konsantrasyonlarına maruz bırakılmıştır. Metanol ve etanol ekstraktlarının, standart bakteri suşlarına karşı 0.01-6.25 mg/ml dozlarda antibakteriyal aktivite sahip olduğu tespit edilmiştir. Her iki ekstraktın da en etkili olduğu suş 0.01 mg/ml MİK değeriyle Bacillus cereus suşu olmuştur. Ekstraktların gram pozitif bakterilere gram negatif bakterilerden daha yüksek etki gösterdiği görülmüştür. Candida albicans maya suşuna karşı etanol ve metanol ekstraktının MİK değerleri sırasıyla 0.39 mg/ml ve 0.78 mg/ml olarak hesaplanmıştır. Ayrıca çalışmada her iki ekstraktın klinik MRSA suşlarının tamamına karşı 0.01-6.25 mg/ml dozlarında oldukça yüksek anti-MRSA aktivitesi gösterdikleri bulunmuştur. Sonuç olarak bu türün antimikrobiyal ajanların doğal bir kaynağı olabileceği ve MRSA suşlarının tedavisinde alternatif olarak kullanılabileceği söylenebilir.

Anahtar Kelimeler

• Antimikrobiyal aktivite
• Anti-MRSA
• Liken
• Metisilin dirençli Staphylococcus aureus.

Kaynakça

1. Açıkgöz B, Karaltı İ, Ersöz M, Coşkun ZM, Çobanoğlu G, Sesal C (2013). Screening of antimicrobial activity and aytotoxic effects of ewo Cladonia species. Zeitschrift für Naturforschung C 68(5-6): 191-197.
2. Aoussar N, Laasri FE, Bourhia M, Manoljovic N, Mhand RA, Rhallabi N, Ullah R, Shahat AA, Noman OM, Nasr FA (2020). Phytochemical analysis, cytotoxic, antioxidant, and antibacterial activities of lichens. Evidence‐Based Complementary and Alternative Medicine 2020: 8104538.
3. Aslan A, Güllüce M, Sökmen M, Adιgüzel A, Sahin F, Özkan H (2006). Antioxidant and antimicrobial properties of the lichens Cladonia foliacea, Dermatocarpon miniatum, Everinia divaricata, Evernia prunastri, and Neofuscella pulla. Pharmaceutical Biology 44(4): 247-252.
4. Aydın S, Kınalıoğlu K (2018). Comparative antimicrobial activity of crude extracts of Protoparmeliopsis muralis (Schreb) M. Choisy (Lecanoraceae) and Parmotrema perlatum (Hudson) M. Choisy (Parmeliaceae) lichens. Gazi University Journal of Science 31: 687-698.
5. Burgaz AR, Ahti T, Pino-Bodas R (2020). Mediterranean Cladoniaceae. Madrid: Spanish Lichen Society.
6. Candan M, Yilmaz M, Tay T, Erdem M, Türk AO (2007). Antimicrobial activity of extracts of the lichen Parmelia sulcata and its salazinic acid constituent. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 62(7-8): 619-621.
7. Cansaran Duman D (2009). Evaluation of usnic acid in some lichens of Turkey by HPLC analysis and screening of their antimicrobial activity. Türk Hijyen ve Deneysel Biyoloji Dergisi 66(4): 153-160.
8. Cansaran Duman D, Halıcı MG (2012). Antimicrobial activity of usnic acid on Squamarina lentigera lichen species. Türk Hijyen ve Deneysel Biyoloji Dergisi 69(3): 127-134.

9. Carrasco F, Hernández W, Castro N, Guerrero M, Tamariz-Angeles C, Olivera-Gonzales P, Echevarría-Rodríguez D, Raposo C, Silva LA, Rodilla JM (2024). Identification and determination of usnic acid and fatty acid from various lichen species in arequipa, Peru, as well as antibacterial and antioxidant capacity. Heliyon 10(21): e39703.
10. Chand P, Singh M, Rai M (2009). Antibacterial activity of some Indian lichens. Journal of Ecophysiology & Occupational Health 9(1-2): 23-29.
11. Coskun ZM, Ersoz M, Acikgoz B, Karalti I, Cobanoglu G, Sesal C (2015). Anti-Proliferative and apoptotic effects of methanolic extracts from different Cladonia species on human breast cancer cells. Folia Biologia 61(3): 97-103.
12. Çobanoğlu G, Sesal C, Gökmen B, Çakar S (2010). Evaluation of the antimicrobial properties of some lichens. South Western Journal of Horticulture 1(2): 153-158.
13. Çobanoğlu G, Sesal C, Açıkgöz B, Karaltı I (2016). Evaluation of antimicrobial activity of the lichens Physcia aipolia, Xanthoria parietina, Usnea florida, Usnea subfloridana and Melanohalea exasperata. Modern Phytomorphology 10: 19-24.
14. Das AK, Sarkar S, Devi P (2024). Overview of lichen In: Das AK, Sharma A, Kathuria D, Ansari MJ, Bhardwaj G (eds.).Chemistry, Biology and Pharmacology of Lichen. New Jersey: John Wiley & Sons Ltd., pp. 1-12.
15. Dülger B, Dülger G, Gedik B, Oran S (2023). Evaluation on antimicrobial activity of the lichen Pleurosticta acetabulum. Düzce University Journal of Science & Technology 11: 199-203.
16. Elo H, Matikainen J, Pelttari E (2007). Potent activity of the lichen antibiotic (+)-usnic acid against clinical isolates of vancomycin-resistant enterococci and methicillin-resistant Staphylococcus aureus. Naturwissenschaften94: 465-468.
17. Ersoz M, Coskun Z, Acikgoz B, Karalti I, Cobanoglu G, Cesal C (2017). In vitro evaluation of cytotoxic, anti-proliferative, anti-oxidant, apoptotic, and anti-microbial activities of Cladonia pocillum. Cellular and Molecular Biology 63: 69-75.
18. Gupta V, Verma S, Gupta S, Singh A, Pal A, Srivastava S, Srivastava P, Singh S, Darokar M (2012). Membrane-damaging potential of natural L-(−)-usnic acid in Staphylococcus aureus. European Journal of Clinical Microbiology & Infectious Diseases 31: 3375-3383.
19. Gunes, E., Durak, Y. (2013). Investigation of Methicillin Resistance of Staphylococcus aureus Strains Isolated from Various Sources by Different Methods. Journal of Pure and Applied Microbiology, 7(4), 2815-2823. John V, Türk A (2017). Türkiye likenleri listesi. İstanbul: Nezahat Gökyiğit Botanik Bahçesi Yayını.
20. Karagoz N, Zeybek Z, Aslan A (2009). Antibacterial activity of some lichen extracts. Journal of Medicinal Plants Research 3(12): 1034-1039.
21. Kocakaya Z, Kocakaya M, Şeker Karatoprak G (2021). Comparative analyses of antioxidant, cytotoxic, and anti-inflammatory activities of different Cladonia species and determination of fumarprotocetraric acid Amounts. KSU Journal of Agriculture and Nature 24: 1196-1207.
22. Kosanić M, Ranković B, Stanojković T, Rančić A, Manojlović N (2014). Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. LWT - Food Science and Technology 59(1): 518-525. Kosanić M, Ristić S, Stanojkovic T, Manojlovic N, Ranković B (2018). Extracts of five Cladonia lichens as sources of biologically active compounds. Farmacia 66: 644-651.
23. Maciąg-Dorszyńska M, Węgrzyn G, Guzow-Krzemińska B (2014). Antibacterial activity of lichen secondary metabolite usnic acid is primarily caused by inhibition of RNA and DNA synthesis. FEMS Microbiology Letters 353(1): 57-62.
24. Matić J, Petrović N, Kosanić M (2024). Antimicrobial and antioxidant activity of the lichens Cladonia rangiferina and Lobaria pulmonaria. 3rd International Conference, Conference on Advances in Science and Technology Coast 2024, Herceg Novi, Montenegro, proceeding book, pp. 419-425.
25. Mitrović T, Stamenković S, Cvetković V, Tošić S, Stanković M, Radojević I, Stefanović O, Comić L, Dačić D, Curčić M, Marković, S (2011). Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Internatiola Journal of Molecular Sciences 12(8): 5428-5448.
26. Mitrović T, Stamenkovi S., Cvetković V, Radulović N, Mladenović M, Stankovic M, Topuzovic M, Radojevic I. Stefanovic O, Vasić S, Čomić L, Seklic D, Obradović A (2015). Contribution to the knowledge of the chemical composition and biological activity of the lichens Cladonia foliacea Huds. (Wild.) and Hypogymnia physodes (L.). Oxidation Communications 38(4A): 2016-2032.
27. Altuner EM, Çeter T, Demirkapı D, Özkay K., Hayal U, Eser G (2011). Investigation on antimicrobial effects of some lichen species collected from Kastamonu region. Communications Faculty of Sciences University of Ankara Series C Biology 23(1-2): 21-31.
28. Ogbole OO, Adebisi P, Segun PA (2019). Medicinal mushrooms with methicillin resistant Staphylococcus aureus (MRSA) inhibitory activity. Journal of Pharmacy & Bioresources 16(1): 41-46.
29. Ranković B, Kosanić M, Stanojković T, Vasiljević P, Manojlović N (2012). Biological activities of Toninia candida and Usnea barbata together with their norstictic acid and usnic acid constituents. International Journal of Molecular Sciences 13(11): 14707-14722.
30. Ranković BR, Kosanić M, Stanojković T (2011). Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis. BMC Complementary and Alternative Medicine 11: 1-8.
31. Ristić S, Ranković B, Kosanić M, Stanojković T, Stamenković S, Vasiljević P, Manojlović I, Manojlović N (2016). Phytochemical study and antioxidant, antimicrobial and anticancer activities of Melanelia subaurifera and Melanelia fuliginosa lichens. Journal of Food Science and Technology 53: 2804-2816.
32. Rositzki MJ, Raksat A, Simmons CJ, Smith C, Wongwiwatthananuki S (2024). Antimicrobial properties of compounds from the Hawaiian lichen Cladonia Skottsbergii. SSRN (in print).
33. Studzińska-Sroka E, Hołderna-Kędzia E, Galanty A, Bylka W, Kacprzak K, Ćwiklińska K (2015). In vitro antimicrobial activity of extracts and compounds isolated from Cladonia uncialis. Natural Product Research 29(24): 2302-2307.
34. Türk AO, Yilmaz M, Kivanç M, and Türk H (2003). The antimicrobial activity of extracts of the lichen Cetraria aculeata and its protolichesterinic acid constituent. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 58(11-12): 850-854.
35. Us D, Kara A, Ünal E, Akıncıoğlu H, Aslan A (2023). Investigation of antimicrobial and antioxidant activities of some lichens. Cumhuriyet Science Journal 44: 418-429.
36. Wayne P (2011). Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute.
37. Yılmaz M, Türk AO, Tay T, Kivanç M (2004). The antimicrobial activity of extracts of the lichen Cladonia foliacea and its (-)-usnic acid, atranorin, and fumarprotocetraric acid constituents. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 59(3-4): 249-254.
38. Yücel O, Odabaşoǧlu F, Güllüce M, Çalik ZZ, Çakir A, Aslan A, Yazici K, Halici M (2007). Antioxidant and antimicrobial properties of a lichen species, Cladonia rangiformis growing in Turkey. Turkish Journal of Pharmaceutical Sciences 4(2): 101-109.
39. Zengin G, Uysal A, Gunes E, Aktumsek A (2014). Survey of phytochemical composition and biological effects of three extracts from a wild plant (Cotoneaster nummularia Fisch. et Mey.): A potential source for functional food ingredients and drug formulations. PLoS One 9(11): e113527.