Abstract
Since lichens have been recognised as a potential natural source of bioactive substances, the aim of this study was to investigate the antimicrobial, lysozyme and antifungal effects of methanol, acetone and quencher extracts from four lichens: Diploschistes ocellatus, Flavoparmelia caperata, Squamarina cartilaginea and Xanthoria parietina. The results showed that the tested extracts had antimicrobial activity against Gram-positive and Gram-negative bacteria and anti-candida, and inhibit the spore germination of tested fungi. The different extracts varied in their effect as determined by the diameter of the inhibition zone, the highest values being observed with the methanol and acetone extracts (29.5 and 27.5 mm, respectively) for S. cartilaginea against Enterococcus faecalis. For powdered material (quencher), F. caperata showed the highest inhibition diameter (25.5 mm) against Staphylococcus aureus. The Minimum Inhibitory Concentration (MIC) values varied from 125 to 2000 μg mL−1. Methanol extracts of S. cartilaginea were more active against Enterobacter cloacae (MIC 125 µg mL−1) and Staphylococcus aureus (MIC 125 µg mL−1), and also affected lysozyme activity against Staphylococcus aureus, as well as the morphology of fungal hyphae. This study demonstrated that the investigated species are a potential source of bioactive compounds which are potentially important antimicrobial agents.
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References
Almola ZS, Al-Ni’ma BA, Ramadan NA (2016) Antibacterial effect of some Iraqi lichen extracts. IJST 5(9):448–456
Aydin S, Kinalioğlu K (2013) The investigation of antibacterial activities of ethanol and methanol extracts of Flavoparmelia caperata (L.) Hale (Parmeliaceae) and Roccella phycopsis Ach. (Roccellaceae) lichens collected from eastern Black Sea Region, Turkey. J App Pharm Sci 3(2):143–147
Basile A, Rigano D, Loppi S, Di Santi A, Nebbioso A, Sorbo S, Bontempo P (2015) Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. Int J Mol Sci 16(12):7861–7875. https://doi.org/10.3390/ijms16047861
Behera BC, Verma N, Sonone A, Makhija U (2007) Antioxidant and antibacterial properties of some cultured lichens. Bioresource Technol 99:776–784. https://doi.org/10.1016/j.biortech.2007.01.031
Buçukoglu TZ, Albayrak S, Halici MG (2012) Antimicrobial and antioxidant activities of extracts and lichen acids obtained from some Umbilicaria species from Central Anatolia, Turkey. J Food Process Preserv 37:1103–1110. https://doi.org/10.1111/j.1745-4549.2012.00811.x
Burkholder PR, Evans AW, Mcveigh I, Thornton HK (1944) Antibiotic activity of lichens. Proc Natl Acad Sci USA 30(9):250–255. https://doi.org/10.1073/pnas.30.9.250
Dias DA, Urban S (2009) Phytochemical investigation of the Australian lichens Ramalina glaucescens and Xanthoria parietina. Nat Prod Commun 4(7):959–964. https://doi.org/10.1177/1934578x0900400717
Dieu A, Mambu L, Champavier Y, Chaleix V, Sol V, Gloaguen V, Millot M (2019) Antibacterial activity of the lichens Usnea florida and Flavoparmelia caperata (Parmeliaceae). Natl Prod Res. https://doi.org/10.1080/14786419.2018.1561678
Essghaier B, Dhieb C, Rebib H, Ayari S, Rezgui A, Boudabous A, Sadfi-Zouaoui N (2014) Antimicrobial behavior of intracellular proteins from two moderately halophilic bacteria: strain J31 of Terribacillus halophilus and strain M3–23 of Virgibacillus marismortui. J Plant Pathol Microb 5(1):214. https://doi.org/10.4172/2157-7471.1000214
Felczykowska A, Pastuszak-Skrzypczak A, Pawlik A, Bogucka K, Herman-Antosiewicz A, Guzow-Krzemińska B (2017) Antibacterial and anticancer activities of acetone extracts from in vitro cultured lichen-forming fungi. BMC Complement Altern Med 17(1):300. https://doi.org/10.1186/s12906-017-1819-8
Ganesan A, Thangapandian M, Ponnusamy P, Sundararaj JP, Nayaka S (2015) Antioxidant and antibacterial activity of parmeliod lichens from Shevaroy hills of Eastern Ghats. India Int J PharmTech Res 8(9):13–23
Gökmen V, Serpen A, Fogliano V (2009) Direct measurement of the total antioxidant capacity of foods: the ‘QUENCHER’ approach. J Food Sci Technol 20:278–288. https://doi.org/10.1016/j.talanta.2013.02.061
Gomez-Serranillos MP, Fernández-Moriano C, González-Burgos E, Divakar PK, Crespo A (2014) Parmeliaceae family: phytochemistry, pharmacological potential and phylogenetic features. Royal Soc Chem Adv 4:59017–59047. https://doi.org/10.1039/C4RA09104C
Graciela M, Vignolo M, Kairuz N, Aida AP, Ruiz H, Oliver G (1995) Influence of growth conditions on the production of lactocin 705, a bacteriocin produced by Lactobacillus casei CRL 705. J Appl Microbiol 78:5–10. https://doi.org/10.1111/j.1365-2672.1995.tb01665.x
Gulluce M, Aslan A, Sokmen M, Sahin F, Adiguzel A, Agar G, Sokmen A (2006) Screening the antioxidant and antimicrobial properties of the lichens Parmelia saxatilis, Platismatia glauca, Ramalina pollinaria, Ramalina polymorpha and Umbilicaria nylanderiana. Phytomedicine 13:515–521. https://doi.org/10.1016/j.phymed.2005.09.008
Gupta VK, Darokar MP, Saikia D, Pal A, Fatima A, Khanuja SPS (2007) Antimycobacterial activity of lichens. Pharm Biol 45(3):200–204. https://doi.org/10.1080/13880200701213088
Hassan STS, Šudomová M, Berchová-Bímová K, Šmejkal K, Echeverría J (2019) Psoromic acid, a lichen-derived molecule, inhibits the replication of HSV-1 and HSV-2, and inactivates HSV-1 DNA polymerase: shedding light on antiherpetic properties. Molecules 24(16):2912. https://doi.org/10.3390/molecules24162912
Huneck S, Yoshimura I (1996) Identification of lichen substances. Springer-Verlag, Berlin
Jorgensen JH, Turnidge JD (2007) Antibacterial susceptibility tests: dilution and disk diffusion methods. In: Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA (eds) Manual of clinical microbiology, 9th edn. American Society for Microbiology, Washington, pp 1152–1172
Kosanić M, Ranković B, Stanojković T (2012) Antioxidant, antimicrobial, and anticancer activities of three Parmelia species. J Sci Food Agric 9:1909–1916. https://doi.org/10.1002/jsfa.5559
Mendili M, Bannour M, Araújo MEM, Aschi-Smiti S, Seaward MRD, Khadhri A (2019) Secondary metabolites and antioxidant capacity of the Tunisian lichen Diploschistes ocellatus (Ascomycota). Int J Med Mushrooms 21(8):817–823. https://doi.org/10.1615/IntJMedMushrooms.2019031423
Mitrović T, Stamenković S, Cvetković V, Tošić S, Stanković M, Radojević I, Stefanović O, Čomić L, Đačić D, Ćurčić M, Marković S (2011) Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Int J Mol Sci 12(8):5428–5448. https://doi.org/10.3390/ijms12085428
Nugraha AS, Untari LF, Laub A, Porzel A, Franke K, Wessjohann LA (2020) Anthelmintic and antimicrobial activities of three new depsides and ten known depsides and phenols from Indonesian lichen: Parmelia cetrata Ach. Nat Prod Res. https://doi.org/10.1080/14786419.2020.1761361
Podterob AP (2008) Chemical composition of lichens and their medical applications. Pharm Chem J 42:582–588
Ranković B (2015) Lichen secondary metabolites. Bioactive properties and pharmaceutical potential. Springer International, Switzerland
Ranković B, Misić M, Sukdolak S (2007) Antimicrobial activity of extracts of the lichens Cladonia furcata, Parmelia caperata, Parmelia pertusa, Hypogymnia physodes and Umbilicaria polyphylla. Br J Biomed Sci 64:143–148
Ranković B, Misić M, Sukdolak S (2008) The antimicrobial activity of substances derived from the lichens Physcia aipolia, Umbilicaria polyphylla, Parmelia caperata and Hypogymnia physodes. World J Microbiol Biotechnol 24:1239–1242. https://doi.org/10.1007/s11274-007-9580-7
Ryazanova LP, Stepnaya OA, Suzina NE, Kulaev IS (2005) Antifungal action of the lytic enzyme complex from Lysobacter sp. XL.1. Process Biochem 40:557–564. https://doi.org/10.1016/j.procbio.2004.01.031
Sarangi N, Athukorala P, Fernando D, RashidKievit KYTD (2010) The role of volatile and non-volatile antibiotics produced by Pseudomonas chlororaphis strain PA23 in its root colonization and control of Sclerotinia sclerotiorum. Biocontrol Sci Technol 20:875–890. https://doi.org/10.1080/09583157.2010.484484
Soundararajan S, Shanmugam P, Nagarajan N, Palanisamy D, Ponnusamy P (2019) In vitro study on screening antimicrobial and anti-oxidant potential of Ramalina fastigiata. J Drug Deliv Ther 9(1):216–219. https://doi.org/10.22270/jddt.v9i1.2217
Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Res 25:188–200. https://doi.org/10.1039/b606983p
Tas I, Yildirim AB, Ozkan E, Ozyigitoglu GC, Yavuz MZ, Turker AU (2019) Biological evaluation and phytochemical profiling of some lichen species. Acta Aliment 48(4):457–465. https://doi.org/10.1556/066.2019.48.4.7
Thadhani VM, Choudhary MI, Ali S, Omar I, Siddique H, Karunaratne V (2011) Antioxidant activity of some lichen metabolites. Nat Prod Res 25:1827–1837. https://doi.org/10.1080/14786419.2010.529546
Zheng KX, Jiang Y, Jiang JX, Huang R, He J, Wu SH (2019) A new phthalazinone derivative and a new isoflavonoid glycoside from lichen-associated Amycolatopsis sp. Fitoterapia 135:85–89. https://doi.org/10.1016/j.fitote.2019.04.011
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Mendili, M., Essghaier, B., Seaward, M.R.D. et al. In vitro evaluation of lysozyme activity and antimicrobial effect of extracts from four Tunisian lichens: Diploschistes ocellatus, Flavoparmelia caperata, Squamarina cartilaginea and Xanthoria parietina. Arch Microbiol 203, 1461–1469 (2021). https://doi.org/10.1007/s00203-020-02129-x
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DOI: https://doi.org/10.1007/s00203-020-02129-x