Evaluation of DNA Protective and Antimicrobial Properties of some Cladonia Species
Year 2022,
, 550 - 555, 27.12.2022
Ahmet Ceylan
,
Gökçe Şeker Karatoprak
,
Zekiye Kocakaya
,
Mustafa Kocakaya
Abstract
The present study evaluated the DNA protective properties and antimicrobial activities of the methanol extracts of nine Cladonia species, namely C. pocillum, C. subulata, C. pyxidata, C. coniocraea, C. foliacea, C. firma, C. furcata, C. fimbriata and C. rangiformis collected in Turkey. DNA protection properties efficiency of Cladonia extracts was evaluated using pBR322 plasmid DNA. In vitro antimicrobial activities of methanol extracts against two Gram-negative bacteria (Escherichia coli and Proteus mirabilis), three Gram-positive bacteria (Staphylococcus aureus, Micrococcus luteus and Bacillus subtilis) and two fungal strains (Candida glabrata and Candida albicans) were examined using the disc diffusion method and through the determination of minimal inhibitory concentrations (MIC). DNA protective studies, all Cladonia extracts protected pBR322 plasmid DNA against damage caused by the hydrogen peroxide (H2O2) with ultraviolet (UV). The results demonstrated that the inhibition zones in the disc diffusion method ranged from 6.5 to 19.0 mm. MIC results were ranged from 3.12 to 6.25 mg/mL. Cladonia extracts show a better antimicrobial effect against bacterial strains than fungal strains. The highest antimicrobial effect among lichen species was demonstrated by Cladonia pocillum. Our results demonstrated that tested Cladonia extracts had strong antibacterial and DNA protective effects. This is the first comprehensive study to evaluate the DNA protective properties activity of Cladonia extracts.
Thanks
We would like to thank the research councils of Erciyes University and Bozok University for the financial support.
References
- [1] Honegger R., Functional aspects of the lichen symbiosis, Annu. Rev. Plant Physiol., 42(1) (1991) 553-578.
- [2] Bates S. T., Cropsey G. W., Caporaso J. G., Knight R., Fierer N., Bacterial communities associated with the lichen symbiosis, Appl Environ Microbiol., 77 (2011) 1309–1314.
- [3] Selbmann L., Zucconi L., Ruisi S., Grube M., Cardinale M., Onofri S., Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance, Polar Biol., 33(1) (2010) 71–83.
- [4] Molnár K., Farkas E., Current results on biological activities of lichen secondary metabolites: a review, Z Naturforsch C., 65(3–4) (2010) 157–173.
- [5] Mitscher L. A., Drake S., Gollapudi S. R., Okwute S. K., A modern look at folkloric use of anti-infective agents, J. Nat. Prod., 50 (6) (1987) 1025–1040.
- [6] Hostettman K., Wolfender J. L .,The search for biologically active secondary metabolites, Pestic. Sci., 51 (1997) 471–482.
- [7] Bate P. N. N., Orock A. E., Nyongbela K. D., Babiaka S. B., Kukwah A., Ngemenya M. N., In vitro activity against multi-drug resistant bacteria and cytotoxicity of lichens collected from Mount Cameroon, J. King Saud Univ. Sci., 32 (1) (2020) 614–619.
- [8] Nishanth K. S., Sreerag R. S., Deepa I., Mohandas C., Nambisan B., Protocetraric acid: an excellent broad-spectrum compound from the lichen Usnea albopunctata against medically important microbes, Nat. Prod. Res., 29(6) (2015) 574–577.
- [9] Timbreza L. P., De los Reyes J. L., Flores C. H., Perez R. J. L. A., Stockel M. A., Santiago K. A., Antibacterial activities of the lichen Ramalina and Usnea collected from Mt. Banoi, Batangas and Dahilayan, Bukidnon, against multi-drug resistant (MDR) bacteria, Aust J Mycol, 26 (2017) 27–42.
- [10] Kilavuz E., Turac E., Ilk S., Sahmetliogl, E. Electropolymerizations of two novel EDOT‐BODIPY zinc oxide nanocomposites and evaluation of their in vitro antibacterial activities, Polym. Adv. Technol., 32(3) (2021) 1086-1100.
- [11] Shukla V., Joshi G. P., Rawat M. S. M., Lichens as a potential natural source of bioactive compounds: a review, Phytochem Rev., 9(2) (2010) 303–314.
- [12] Perry N. B., Benn M. H., Brennan N. J., Burgess E. J., Ellis G., Galloway D. J., Tangney R. S., Antimicrobial, antiviral and cytotoxic activity of New Zealand lichens,The Lichenologist, 31(6) (1999) 627–636.
- [13] Mitrović T., Stamenković S., Cvetković V., Tošić S., Stanković M., Radojević I., Marković S. Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Int. J. Mol. Sci., 12(8) (2011) 5428–5448.
- [14] Manojlović N., Ranković B., Kosanić M., Vasiljević P., Stanojković T., Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites, Phytomedicine, 19(13) (2012) 1166–1172.
- [15] Lumbsch H. T., Huhndorf S. M., Part One. Outline of Ascomycota-2009. Part Two. Notes on Ascomycete Systematics, Fieldiana: life and earth sciences 1 (2010) 4751–5113.
- [16] Miadlikowska J., Kauff F., Hofstetter V., Fraker E., Grube M., HafellnerJ., Lutzoni F., New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA-and two protein-coding genes, Mycologia, 98(6) (2006) 1088-1103.
- [17] Huovinen K., Ahti T., Biosequential patterns for the formation of depsides, depsidones and dibenzofurans in the genus Cladonia (lichen-forming ascomycetes), In Annales Botanici Fennici (1982) 225–234.
- [18] Kosanić M., Ranković B., Stanojković T., Rančić A., Manojlović N.,Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. LWT - Food Sci. Technol., 59(1) (2014) 518–525.
- [19] Kosanić M., Ristić S., Stanojković T., Manojlović N., Ranković B., Extracts of five Cladonia lichens as sources of biologically active compounds, Farmacia, 66 (2018) 644–651.
- [20] Mitrovic T. L., Stamenkovic S. M., Cvetkovic V. J., Radulovic N. S., Mladenovic M. Z., Stankovic M. S., Markovic S. D., Contribution to the knowledge of the chemical composition and biological activity of the lichens Cladonia foliacea hud s.(wild.) and Hypogymnia physodes (l.), Oxid. Commun., 38(4A) (2015) 2016–2032.
- [21] Yano Melo A. M., Vicente C., Xavier Filho L., Allelopathic efect of the Cladonia verticillaris lichen extracts and fumarprotocetraric acid on the early growth of germinated seedlings in Allium cepa L. Trop Bryol, 17 (1999) 133–139.
- [22] Yılmaz M., Türk A. Ö., Tay T., Kıvanç M., The antimicrobial activity of extracts of the lichen Cladonia foliacea and its (–)-usnic acid, atranorin, and fumarprotocetraric acid constituents, Z. Naturforsch., C, 59(3-4) (2004) 249-254.
- [23] Ranković B., Mišić M., The antimicrobial activity of the lichen substances of the lichens Cladonia furcata, Ochrolechia androgyna, Parmelia caperata and Parmelia conspresa, Biotechnol. Biotechnol. Equip., 22(4) (2008) 1013–1016.
- [24] Alves de Barros G. M., de Sousa Maia M. B., de Souza Franco E., Galvão A. M., da Silva T. G., Gomes R. M., da Silva N. H., Expectorant and antioxidant activities of purified fumarprotocetraric acid from Cladonia verticillaris lichen in mice, Pulm Pharmacol Ther, 27(2) (2013) 139–143.
- [25] Sinha S., Biswas D., Mukherjee A., Antigenotoxic and antioxidant activities of palmarosa and citronella essential oils, J Ethnopharmacol, 137(3) (2011) 1521–1527.
- [26] Ahti T., Stenroos S., Moberg R., Nordic lichen flora, (Vol 5, Cladoniaceae). Museum of Evolution, Uppsala University, Uppsala, (2013)
- [27] Ahti T., Hammer S., Cladonia. In: Nash III T.H., Ryan B.D., Gries C., Bungartz F (ed, Lichen flora of the greater sonoran desert region, Arizona State University, Tempe, (2002).
- [28] Ranković B. R., Kosanić M. M., Stanojković T. P., Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis, BMC Complement Altern. Med., 11(1) (2011) 1–8.
- [29] Kocakaya Z., Kocakaya M., Şeker Karatoprak G., Comparative analyses of antioxidant, cytotoxic, and anti-inflammatory activities of different Cladonia species and determination of fumarprotocetraric acid amounts. KSÜ Tarım ve Doğa Dergisi Tarım, 24(6) (2021) 1196–1207.
- [30] Brakni R., Ali Ahmed M., Burger P., Schwing A., Michel G., Pomares C., Michel T., UHPLC‐HRMS/MS Based Profiling of Algerian Lichens and Their Antimicrobial Activities. Chem Biodivers., 15(4) (2018) 1-17.
- [31] Plaza C. M., de Salazar C. P., Vizcaya M., Rodríguez-Castillo C. G., Ramírez G. E. M., Plaza R. E., Potential antifungal activity of Cladonia aff. rappii A. Evans. J. Pharm. Pharmacogn. Res. 5(5) (2017) 301–309.
- [32] Studzińska-Sroka E., Tomczak H., Malińska N., Wrońska M., Kleszcz R., Galanty A., Paluszczak J., Cladonia uncialis as a valuable raw material of biosynthetic compounds against clinical strains of bacteria and fungi. Acta Biochim. Pol., 66(4) (2019) 597–603.
- [33] Açıkgöz B., Karaltı İ., Ersöz M., Coşkun Z. M., Çobanoğlu G., Sesal C., Screening of antimicrobial activity and cytotoxic effects of two Cladonia species. Z Naturforsch C, 68(5–6) (2013) 191–197.
- [34] Russo A., Piovano M., Lombardo L., Garbarino J., Cardile V. Lichen metabolites prevent UV light and nitric oxide-mediated plasmid DNA damage and induce apoptosis in human melanoma cells. Life Sci., 83(13–14) (2008) 468–474.
- [35] Abbas M., Ali A., Arshad M., Atta A., Mehmood Z., Tahir I. M., Iqbal M., Mutagenicity, cytotoxic and antioxidant activities of Ricinus communis different parts, Chem. Cent. J. 12(3) (2018) 1–9.
- [36] Korkmaz A. I., Akgul H., Sevindik M., Selamoglu Z., Study on determination of bioactive potentials of certain lichens, Acta Aliment, 47(1) (2018) 80–87.
- [37] Pillai T. G., Salvi V. P., Maurya D. K., Nair C. K. K., Janardhanan K. K., Prevention of radiation-induced damages by aqueous extract of Ganoderma lucidum occurring in southern parts of India, Curr. Sci., (2006) 341–344.
Year 2022,
, 550 - 555, 27.12.2022
Ahmet Ceylan
,
Gökçe Şeker Karatoprak
,
Zekiye Kocakaya
,
Mustafa Kocakaya
References
- [1] Honegger R., Functional aspects of the lichen symbiosis, Annu. Rev. Plant Physiol., 42(1) (1991) 553-578.
- [2] Bates S. T., Cropsey G. W., Caporaso J. G., Knight R., Fierer N., Bacterial communities associated with the lichen symbiosis, Appl Environ Microbiol., 77 (2011) 1309–1314.
- [3] Selbmann L., Zucconi L., Ruisi S., Grube M., Cardinale M., Onofri S., Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance, Polar Biol., 33(1) (2010) 71–83.
- [4] Molnár K., Farkas E., Current results on biological activities of lichen secondary metabolites: a review, Z Naturforsch C., 65(3–4) (2010) 157–173.
- [5] Mitscher L. A., Drake S., Gollapudi S. R., Okwute S. K., A modern look at folkloric use of anti-infective agents, J. Nat. Prod., 50 (6) (1987) 1025–1040.
- [6] Hostettman K., Wolfender J. L .,The search for biologically active secondary metabolites, Pestic. Sci., 51 (1997) 471–482.
- [7] Bate P. N. N., Orock A. E., Nyongbela K. D., Babiaka S. B., Kukwah A., Ngemenya M. N., In vitro activity against multi-drug resistant bacteria and cytotoxicity of lichens collected from Mount Cameroon, J. King Saud Univ. Sci., 32 (1) (2020) 614–619.
- [8] Nishanth K. S., Sreerag R. S., Deepa I., Mohandas C., Nambisan B., Protocetraric acid: an excellent broad-spectrum compound from the lichen Usnea albopunctata against medically important microbes, Nat. Prod. Res., 29(6) (2015) 574–577.
- [9] Timbreza L. P., De los Reyes J. L., Flores C. H., Perez R. J. L. A., Stockel M. A., Santiago K. A., Antibacterial activities of the lichen Ramalina and Usnea collected from Mt. Banoi, Batangas and Dahilayan, Bukidnon, against multi-drug resistant (MDR) bacteria, Aust J Mycol, 26 (2017) 27–42.
- [10] Kilavuz E., Turac E., Ilk S., Sahmetliogl, E. Electropolymerizations of two novel EDOT‐BODIPY zinc oxide nanocomposites and evaluation of their in vitro antibacterial activities, Polym. Adv. Technol., 32(3) (2021) 1086-1100.
- [11] Shukla V., Joshi G. P., Rawat M. S. M., Lichens as a potential natural source of bioactive compounds: a review, Phytochem Rev., 9(2) (2010) 303–314.
- [12] Perry N. B., Benn M. H., Brennan N. J., Burgess E. J., Ellis G., Galloway D. J., Tangney R. S., Antimicrobial, antiviral and cytotoxic activity of New Zealand lichens,The Lichenologist, 31(6) (1999) 627–636.
- [13] Mitrović T., Stamenković S., Cvetković V., Tošić S., Stanković M., Radojević I., Marković S. Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Int. J. Mol. Sci., 12(8) (2011) 5428–5448.
- [14] Manojlović N., Ranković B., Kosanić M., Vasiljević P., Stanojković T., Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites, Phytomedicine, 19(13) (2012) 1166–1172.
- [15] Lumbsch H. T., Huhndorf S. M., Part One. Outline of Ascomycota-2009. Part Two. Notes on Ascomycete Systematics, Fieldiana: life and earth sciences 1 (2010) 4751–5113.
- [16] Miadlikowska J., Kauff F., Hofstetter V., Fraker E., Grube M., HafellnerJ., Lutzoni F., New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA-and two protein-coding genes, Mycologia, 98(6) (2006) 1088-1103.
- [17] Huovinen K., Ahti T., Biosequential patterns for the formation of depsides, depsidones and dibenzofurans in the genus Cladonia (lichen-forming ascomycetes), In Annales Botanici Fennici (1982) 225–234.
- [18] Kosanić M., Ranković B., Stanojković T., Rančić A., Manojlović N.,Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. LWT - Food Sci. Technol., 59(1) (2014) 518–525.
- [19] Kosanić M., Ristić S., Stanojković T., Manojlović N., Ranković B., Extracts of five Cladonia lichens as sources of biologically active compounds, Farmacia, 66 (2018) 644–651.
- [20] Mitrovic T. L., Stamenkovic S. M., Cvetkovic V. J., Radulovic N. S., Mladenovic M. Z., Stankovic M. S., Markovic S. D., Contribution to the knowledge of the chemical composition and biological activity of the lichens Cladonia foliacea hud s.(wild.) and Hypogymnia physodes (l.), Oxid. Commun., 38(4A) (2015) 2016–2032.
- [21] Yano Melo A. M., Vicente C., Xavier Filho L., Allelopathic efect of the Cladonia verticillaris lichen extracts and fumarprotocetraric acid on the early growth of germinated seedlings in Allium cepa L. Trop Bryol, 17 (1999) 133–139.
- [22] Yılmaz M., Türk A. Ö., Tay T., Kıvanç M., The antimicrobial activity of extracts of the lichen Cladonia foliacea and its (–)-usnic acid, atranorin, and fumarprotocetraric acid constituents, Z. Naturforsch., C, 59(3-4) (2004) 249-254.
- [23] Ranković B., Mišić M., The antimicrobial activity of the lichen substances of the lichens Cladonia furcata, Ochrolechia androgyna, Parmelia caperata and Parmelia conspresa, Biotechnol. Biotechnol. Equip., 22(4) (2008) 1013–1016.
- [24] Alves de Barros G. M., de Sousa Maia M. B., de Souza Franco E., Galvão A. M., da Silva T. G., Gomes R. M., da Silva N. H., Expectorant and antioxidant activities of purified fumarprotocetraric acid from Cladonia verticillaris lichen in mice, Pulm Pharmacol Ther, 27(2) (2013) 139–143.
- [25] Sinha S., Biswas D., Mukherjee A., Antigenotoxic and antioxidant activities of palmarosa and citronella essential oils, J Ethnopharmacol, 137(3) (2011) 1521–1527.
- [26] Ahti T., Stenroos S., Moberg R., Nordic lichen flora, (Vol 5, Cladoniaceae). Museum of Evolution, Uppsala University, Uppsala, (2013)
- [27] Ahti T., Hammer S., Cladonia. In: Nash III T.H., Ryan B.D., Gries C., Bungartz F (ed, Lichen flora of the greater sonoran desert region, Arizona State University, Tempe, (2002).
- [28] Ranković B. R., Kosanić M. M., Stanojković T. P., Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis, BMC Complement Altern. Med., 11(1) (2011) 1–8.
- [29] Kocakaya Z., Kocakaya M., Şeker Karatoprak G., Comparative analyses of antioxidant, cytotoxic, and anti-inflammatory activities of different Cladonia species and determination of fumarprotocetraric acid amounts. KSÜ Tarım ve Doğa Dergisi Tarım, 24(6) (2021) 1196–1207.
- [30] Brakni R., Ali Ahmed M., Burger P., Schwing A., Michel G., Pomares C., Michel T., UHPLC‐HRMS/MS Based Profiling of Algerian Lichens and Their Antimicrobial Activities. Chem Biodivers., 15(4) (2018) 1-17.
- [31] Plaza C. M., de Salazar C. P., Vizcaya M., Rodríguez-Castillo C. G., Ramírez G. E. M., Plaza R. E., Potential antifungal activity of Cladonia aff. rappii A. Evans. J. Pharm. Pharmacogn. Res. 5(5) (2017) 301–309.
- [32] Studzińska-Sroka E., Tomczak H., Malińska N., Wrońska M., Kleszcz R., Galanty A., Paluszczak J., Cladonia uncialis as a valuable raw material of biosynthetic compounds against clinical strains of bacteria and fungi. Acta Biochim. Pol., 66(4) (2019) 597–603.
- [33] Açıkgöz B., Karaltı İ., Ersöz M., Coşkun Z. M., Çobanoğlu G., Sesal C., Screening of antimicrobial activity and cytotoxic effects of two Cladonia species. Z Naturforsch C, 68(5–6) (2013) 191–197.
- [34] Russo A., Piovano M., Lombardo L., Garbarino J., Cardile V. Lichen metabolites prevent UV light and nitric oxide-mediated plasmid DNA damage and induce apoptosis in human melanoma cells. Life Sci., 83(13–14) (2008) 468–474.
- [35] Abbas M., Ali A., Arshad M., Atta A., Mehmood Z., Tahir I. M., Iqbal M., Mutagenicity, cytotoxic and antioxidant activities of Ricinus communis different parts, Chem. Cent. J. 12(3) (2018) 1–9.
- [36] Korkmaz A. I., Akgul H., Sevindik M., Selamoglu Z., Study on determination of bioactive potentials of certain lichens, Acta Aliment, 47(1) (2018) 80–87.
- [37] Pillai T. G., Salvi V. P., Maurya D. K., Nair C. K. K., Janardhanan K. K., Prevention of radiation-induced damages by aqueous extract of Ganoderma lucidum occurring in southern parts of India, Curr. Sci., (2006) 341–344.