Advertisement

Lichen Secondary Metabolites as Potential Antibiotic Agents

  • Marijana Kosanić
  • Branislav Ranković
Chapter

Abstract

It is well known that pathogenic microbes pose serious threats to human health and are increasing in prevalence in institutional health care settings due to the growing resistance that infectious agents have developed against antibiotics. Therefore, new alternatives for combating the spread of infection through antibiotic-resistant microbes are necessary for keeping pace with the evolution of ‘super’ pathogens. Natural products are proposed as a therapeutic alternative to conventional antimicrobial treatment. Among them, lichen-derived products and their antibiotic properties are of special interest to scientists as up to 50% of all lichens have been reported to possess antibiotic activities. A great number of reports concerning the antimicrobial screening of lichens have appeared in the literature. According to published data, the lichens and their secondary metabolites exhibited the activity against a great number of microorganisms. Therefore, this study represents lichens as very interesting source of bioactive compounds which provide unlimited opportunities for new antimicrobial agents.

References

  1. Abdullah ST, Hamid H, Ali M et al (2007) Two new terpenes from the lichen Parmelia perlata. Ind J Chem 46B:173–176Google Scholar
  2. Abo-Khatwa AN, al-Robai AA, al-Jawhari DA (1996) Lichen acids as uncouplers of oxidative phosphorylation of mouse-liver mitochondria. Nat Toxins 4:96–102PubMedCrossRefPubMedCentralGoogle Scholar
  3. Abraham EP, Chain E (1940) An enzyme from bacteria able to destroy penicillin. Nature 146:837CrossRefGoogle Scholar
  4. Ankith GN, Rajesh MR, Karthik KN et al (2017) Antibacterial and antifungal activity of three Ramalina species. J Drug Deliv Ther 7:27–32Google Scholar
  5. Bačkor M, Hudák J, Repčák M et al (1998) The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of lichen photobiont Trebouxia irregularis. Lichenologist 30:577–582CrossRefGoogle Scholar
  6. Balaji P, Hariharan GN (2007) In vitro antimicrobial activity of Parmotrema prasorediosum thallus extracts. Res J Bot 2:54–59CrossRefGoogle Scholar
  7. Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6:71–79PubMedCrossRefGoogle Scholar
  8. Basile A, Rigano D, Loppi S et al (2015) Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. Int J Mol Sci 16:7861–7875PubMedPubMedCentralCrossRefGoogle Scholar
  9. Behera BC, Verma N, Sonone A et al (2005) Antimicrobial activity of various solvent extracts of lichen Usnea ghattensis. Agarkar Research Institute, PuneGoogle Scholar
  10. Bondarenko V, Korczynski M, Techathaveewat W (2017) The antimicrobial properties of extracts isolated from lichen Parmelia vagans [supplemental material]. FASEB J 31(1):939.13Google Scholar
  11. Bouaid K, Vicente C (1998) Chlorophyll degradation effected by lichen substances. Ann Bot Fenn 35:71–74Google Scholar
  12. Buçukoglu TZ, Albayrak S, Gökhan Halici M et al (2013) Antimicrobial and antioxidant activities of extracts and lichen acids obtained from some Umbilicaria species from Central Anatolia, Turkey. J Food Process Preserv 37:1103–1110CrossRefGoogle Scholar
  13. Burkholder PR, Evans AW (1945) Further studies on the antibiotic activity of lichens. Bull Torrey Bot Club 72:157–164CrossRefGoogle Scholar
  14. Burkholder PR, Evans AW, McVeigh I et al (1944) Antibiotic activity of lichens. Proc Natl Acad Sci 30:250–255PubMedCrossRefGoogle Scholar
  15. Byron F, Brehm S, Eric AJ (2003) Sensitization of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids. Antimicrob Agents Chemother 47:3357–3360CrossRefGoogle Scholar
  16. Candan M, Yilmaz M, Tay T et al (2006) Antimicrobial activity of extracts of the lichen Xanthoparmelia pokornyi and its gyrophoric and stenosporic acid constituents. Z Naturforsch 61:319–323CrossRefGoogle Scholar
  17. Candan M, Yýlmaz M, Tay T et al (2007) Antimicrobial activity of extracts of the lichen Parmelia sulcata and its Salazinic acid constituent. Z Naturforsch 62:619–621CrossRefGoogle Scholar
  18. Cansaran D, Atakol O, Halici M et al (2007) HPLC analysis of usnic acid in some Ramalina species from Anatolia and investigation of their antimicrobial activities. Pharm Biol 45:77–81CrossRefGoogle Scholar
  19. Chauhan R, Abraham J (2013) In vitro antimicrobial potential of the lichen Parmotrema sp. extracts against various pathogens. Iran J Basic Med Sci 16:882–885PubMedPubMedCentralGoogle Scholar
  20. Clinical and Laboratory Standards Institude (2009) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-eighth edition M07-A8. National Committee for Clinical Laboratory Standards 29Google Scholar
  21. Cowan MM (1999) Plants products as antimicrobial agents. Clin Microbiol Rev 12:564–582PubMedPubMedCentralCrossRefGoogle Scholar
  22. Culberson CF (1970) Supplement to chemical and botanical guide to lichen products. Bryologist 73:1–28CrossRefGoogle Scholar
  23. Dickert H, Machka K, Braveny I (1981) The uses and limitations of disc diffusion in the antibiotic sensitivity testing of bacteria. Infection 9:18–24CrossRefGoogle Scholar
  24. Dixit A, Mishra M, Singh AN et al (2018) Antimicrobial and antifungal activity of Indian Lichen (Usnea sps. And Parmotrema sps.) against human phatogenic bacterial and fungal sps. World J Pharm Pharm Sci 7:711–720Google Scholar
  25. EIo 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. Naturwissenschaften 94:465–468CrossRefGoogle Scholar
  26. Epand RF, Savage PB, Epand RM (2007) Bacterial lipid composition and the antimicrobial efficacy of cationic steroid compounds. Biochim Biophys Acta 1768:2500–2509PubMedCrossRefGoogle Scholar
  27. Esimone CO, Adikwn MU (1999) Antimicrobial activity of the cytotoxicity of Ramalina farinacea. Fitoterapia 7:428–431CrossRefGoogle Scholar
  28. Farkaš V (2003) Structure and biosynthesis of fungal cell walls: methodological approaches. Folia Microbiol 48:469–478CrossRefGoogle Scholar
  29. Francolini I, Norris P, Piozzi A et al (2004) Usnic acid, a natural antimicrobialagent able to inhibit bacterial biofilm formation on polymer surfaces. Antimicrob Agents Chemother 48:4360–4365PubMedPubMedCentralCrossRefGoogle Scholar
  30. Goel M, Dureja P, Rani A et al (2011) Isolation, characterization and antifungal activity of major constituents of the Himalayan lichen Parmelia reticulate Tayl. J Agric Food Chem 59:2299–2307PubMedCrossRefGoogle Scholar
  31. Gomes AT, Honda NK, Roese FM et al (2002) Bioactive derivatives obtained from lecanoric acid, a constituent of the lichen Parmotrema tinctorum (Nyl.). Hale (Parmeliaceae). Rev Bras Farmacogn 12:74–75CrossRefGoogle Scholar
  32. Gomes AT, Smania A Jr, Seidel C et al (2003) Antibacterial activity of orsellinates. Braz J Microbiol 34(3):194–196CrossRefGoogle Scholar
  33. Gulluce M, Aslan A, Sokmen M et al (2006) Screening the antioxidant and antimicrobial properties of the lichens Parmelia saxatilis, Platismatia glauca, Ramalina pollinaria, Ramalina polymorpha and Umbilicaria nylanderiana. Phytomedicine 13:515–521PubMedCrossRefGoogle Scholar
  34. Halama P, van Haluwin C (2004) Antifungal activity of lichen extracts and Lichenic acids. BioControl 49:95–107CrossRefGoogle Scholar
  35. Hauck M, Jurgens SR (2008) Usnic acid controls the acidity tolerance of lichens. Environ Pollut 156:115–122PubMedCrossRefPubMedCentralGoogle Scholar
  36. Heijenoort J (2001) Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11:25–36CrossRefGoogle Scholar
  37. Honda NK, Pavan FR, Coelho RG et al (2010) Antimycobacterial activity of lichen substances. Phytomedicine 17:328–332PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ingólfsdóttir K, Bloomfield SF, Hylands PJ (1985) In vitro evaluation of the antimicrobial activity of lichen metabolites as potential preservatives. Antimicrob Agents Chemother 28:289–292PubMedPubMedCentralCrossRefGoogle Scholar
  39. Ingolfsdottir K, Chung GAC, Skulason VG et al (1998) Antimycobacterial activity of lichen metabolites in vitro. Eur J Pharm Sci 6:141–144PubMedCrossRefPubMedCentralGoogle Scholar
  40. Ivanova V, Aleksieva K, Kolarova M et al (2002) Neuropogonines A, B and C, new depsidon-type metabolites from Neuropogon sp., an Antarctic lichen. Pharmazie 57:73–74PubMedPubMedCentralGoogle Scholar
  41. Ivanova V, Graefe U, Schlegel B et al (2004) Usnic acid, metabolite from Neuropogon Sp., an Antarctic lichen isolation, structure elucidation and biological activity. Biotechnol Biotechnol Equip 18:66–71CrossRefGoogle Scholar
  42. Javeria S, Shahi SK, Shahi MP et al (2013) Parmotrema nilgherrense: potential antimicrobial acti vity against drug resistant pathogens. Int J Microb Res Technol 2:36–40Google Scholar
  43. Karagoz A, Dogruoz N, Zeybek Z et al (2009) Antibacterial activity of some lichen extracts. J Med Plants Res 3:1034–1039Google Scholar
  44. Karthikaidevi G, Thirumaran G, Manivannan K et al (2009) Screening of the antibacterial properties of lichen Roccella belangeriana (Awasthi) from Pichavaram mangrove (Rhizophora sp.). Adv Biol Res 3:127–131Google Scholar
  45. Kekuda PTR, Vinayaka KS, Swathi D et al (2011) Mineral composition, total phenol content and antioxidant activity of a macrolichen Everniastrum cirrhatum (Fr.) Hale (Parmeliaceae). E-Journal of Chemistry 8:1886–1894CrossRefGoogle Scholar
  46. Kim JS, Kim Y (2007) The inhibitory effect of natural bioactives on the growth of pathogenic bacteria. Nutr Res Pract 1(4):273–278PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kinoshita K, Matsubara H, Koyama K et al (1994) Topics in the chemistry of lichen compounds. J Hattori Bot Lab 76:227–233Google Scholar
  48. Klancnik A, Piskernik S, Jersek B et al (2010) Evaluation of diffusion and dilution methods to determine the antibacterial activity of plant extracts. J Microbiol Methods 81:121–126PubMedCrossRefPubMedCentralGoogle Scholar
  49. Kosanić M, Ranković B (2011) Antioxidant and antimicrobial properties of some lichens and their constituents. J Med Food 14:1624–1630PubMedCrossRefGoogle Scholar
  50. Kosanić M, Ranković B, Slobodan S (2010) Antimicrobial activity of the lichen Lecanora frustulosa and Parmeliopsis hyperopta and their divaricatic acid and zeorin constituents. Afr J Micro biol Res 4:885–890Google Scholar
  51. Kosanić M, Manojlović N, Janković S et al (2013) Evernia prunastri and Pseudoevernia furfuraceae lichens and their major metabolites as antioxidant, antimicrobial and anticancer agents. Food Chem Toxicol 53:112–118PubMedCrossRefGoogle Scholar
  52. Kosanić M, Ranković B, Stanojković T et al (2014a) Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. LWT – Food Sci Technol 59:518–525CrossRefGoogle Scholar
  53. Kosanić M, Seklic D, Markovic S et al (2014b) Antimicrobial and anticancer properties of selected lichens from Serbia. Dig J Nanomater Bios 9:273–287Google Scholar
  54. Kosanić M, Ranković B, Stanojković T et al (2014c) Biological activities and chemical composition of lichens from Serbia. EXCLI J 13:1226–1238PubMedPubMedCentralGoogle Scholar
  55. Kosanić M, Ranković B, Stanojković T et al (2016) Lasallia pustulata lichen as possible natural antigenotoxic, antioxidant, antimicrobial and anticancer agent. Cytotechnology 68:999–1008PubMedCrossRefPubMedCentralGoogle Scholar
  56. Kosanić M, Ristić S, Stanojković T et al (2018) Extracts of five Cladonia lichens as sources of biologically active compounds. Farmacia 66:644–651CrossRefGoogle Scholar
  57. Kumar KC, Müller K (1999) Lichen Metabolites. 2. Antiproliferative and cytotoxic activity of gyrophoric, usnic, and diffractaic acid on human keratinocyte growth. J Nat Prods 62(6):821–823CrossRefGoogle Scholar
  58. Kumar PSV, Kekuda PTR, Vinayaka KS et al (2010) Studies on proximate composition,antifungal and anthelmintic activity of macrolichen Ramalina hoss H. Magn and G.Awasthi. Int J Biotech Biochem 6:193–203Google Scholar
  59. Land CJ, Lundstrom J (1998) Inhibition of fungal growth by water extracts from the lichen Nephroma arcticum. Lichenologist 30:259–262Google Scholar
  60. Lauterwein M, Oethinger M, Belsner K et al (1995) In vitro activities of the lichen secondary metabolites vulpinic acid, (+)-usnic acid, and (−)-usnic acid against aerobic and anaerobic microorganisms. Antimicrob Agents Chemother 39(11):2541–2543PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lawrey JD (1986) Biological role of lichen substances. The Byrologist 89:111–122CrossRefGoogle Scholar
  62. 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 Microbiol Lett 353:57–62PubMedCrossRefPubMedCentralGoogle Scholar
  63. Madamombe IT, Afolajan AJ (2003) Evaluation of antimicrobial activity of extracts from south African Usnea barbata. Pharm Biol 41:199–202CrossRefGoogle Scholar
  64. Manojlović N, Solujić S, Sukdolak S (2002) Antimicrobial activity of an extract and anthraquinones from Caloplaca schaereri. Lichenologist 34:83–85CrossRefGoogle Scholar
  65. Manojlović NT, Solujic S, Sukdolak S et al (2005) Antifungal activity of Rubia tinctorum, Rhamnus frangula and Caloplaca cerina. Fitoterapia 76:244–246PubMedCrossRefPubMedCentralGoogle Scholar
  66. Manojlović NT, Vasiljevic PJ, Markovic ZS (2010) Antimicrobial activity of extracts and various fractions of chloroform extract from the lichen Laurera benguelensis. J Biol Res-Thessalon 13:27–34Google Scholar
  67. Manojlović N, Ranković B, Kosanić M et al (2012) Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine 19:1166–1172PubMedCrossRefPubMedCentralGoogle Scholar
  68. Martins MCB, Gonçalves de Lima MJ, Silva FP et al (2010) Cladia aggregata (lichen) from Brazilian northeast, chemical characterization and antimicrobial activity. Braz Arch Biol Technol 53:115–122CrossRefGoogle Scholar
  69. Matvieieva NA, Pasichnyk LA, Zhytkevych NV et al (2015) Antimicrobial activity of extracts from Ecuadorian lichens. Mikrobiol Z 77:23–27PubMedCrossRefPubMedCentralGoogle Scholar
  70. Micheletti AC, Beatriz A, de Lima DP et al (2009) Constituintes quımicos de Parmotrema lichexanthonicum Eliasaro & Adler – Isolamento, Modificacoes estruturais e avaliacao das atividades antibiotica e citotoxica. Quim Nova 32:12–20CrossRefGoogle Scholar
  71. Mitrović T, Stamenković S, Cvetković V et al (2011) Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Int J Mol Sci 12:5428–5448PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mohammed SG (2013) Comparative study of in vitro antibacterial activity of miswak extracts and different toothpastes. Am J Agric Biol Sci 8:82–88CrossRefGoogle Scholar
  73. Moreno S, Scheyer T, Romano CS et al (2006) Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic Res 40:223–231PubMedCrossRefPubMedCentralGoogle Scholar
  74. Nostro MP, Germano V, D’Angelo A et al (2000) Extraction methods and bioautography for evaluation of medical plant antimicrobial activity. Lett Appl Microbiol 30:379–384PubMedCrossRefPubMedCentralGoogle Scholar
  75. Odabasoglu F, Aslan A, Cakir A et al (2004) Comparison of antioxidant activity and phenolic content of three lichen species. Phytother Res 18:938–941PubMedCrossRefPubMedCentralGoogle Scholar
  76. Ofokansi KC, Esimone CO (2005) Evaluation of the in vitro antimicrobial activity and release behaviour of ointments and applications containing extract of lichen Ramalina farinaceae. Plant Prod Res J 9:6–10Google Scholar
  77. Oh JM, Kim YJ, Gang HS et al (2018) Antimicrobial activity of divaricatic acid isolated from the lichen Evernia mesomorpha against methicillin-resistant Staphylococcus aureus. Molecules 23:3068PubMedCentralCrossRefGoogle Scholar
  78. Oloke JO, Kolawole DO (1998) The antibacterial and antifungal activities of certain components of Aframomum meleguetea fruits. Fitoterapia 59:384–388Google Scholar
  79. Paudel B, Bhattarai HD, Lee JS et al (2008) Antioxidant activity of polar lichens from King George Island (Antarctica). Polar Biol 31:605–608CrossRefGoogle Scholar
  80. Paudel B, Bhattarai HD, Lee HK et al (2010) Antibacterial activities of Ramalin, usnic acid and its three derivatives isolated from the Antarctic lichen Ramalina terebrata. Z Naturforsch C 65:34–38PubMedCrossRefPubMedCentralGoogle Scholar
  81. Perry NB, Benn MH, Brennan NJ et al (1999) Antimicrobial, antiviral and citotoxic activity of New Zealand lichens. Lichenologist 31:627–636CrossRefGoogle Scholar
  82. Piovano M, Garbarino JA, Giannini FA et al (2002) Evaluation of antifungal and antibacterial activities of aromatic metabolites from lichens. Bol Soc Chil Quím 47:235–240CrossRefGoogle Scholar
  83. Ramos DF, Almeida da Silva PE (2010) Antimycobacterial activity of usnic acid against resistant and susceptible strains of and non-tuberculous mycobacteria. Pharm Biol 48(3):260–263PubMedCrossRefPubMedCentralGoogle Scholar
  84. Ramos Dalia BM, Gomes Francis S, Napoleo Thiago H et al (2014) Antimicrobial preparations on bacteria and fungi of medical importance. Chin J Biol 2014:219392Google Scholar
  85. Ranković B, Mišić M (2007) Antifungal activity of extract of the lichens Alectoria sarmentosa and Cladonia rangiferina. Mikol Fitopatol 41:276–281Google Scholar
  86. Ranković B, Mišić M (2008) The antimicrobial activity of the lichen substances of the lichens Cladonia furcata, Ochrolechia androgyna, Parmelia caperata and Parmelia conspresa. Biotechnol Biotech Equip 22:1310–2818CrossRefGoogle Scholar
  87. Ranković B, Mišić M, Sukdolak S et al (2007a) Antimicrobial activity of the lichens Aspicilia cinerea, Collema cristatum, Ochrolechia androgyna, Physcia aipolia and Physcia caesia. Ital J Food Sci 19:461–469Google Scholar
  88. Ranković B, Mišić M, Sukdolak S (2007b) Evaluation of antimicrobial activity of the lichens Lasallia pustulata, Parmelia sulcata, Umbilicaria crustulosa and Umbilicaria cylindrical. Microbiology 76:723–727CrossRefGoogle Scholar
  89. Ranković B, Mišić 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 24:1239–1242CrossRefGoogle Scholar
  90. Ranković B, Mišić M, Sukdolak S (2009) Antimicrobial activity of extracts of the lichens Cladonia furcata, Parmelia caperata, Parmelia pertusa, Hypogymnia physodes and Umbilicaria polyphylla. Biologia 64:53–58CrossRefGoogle Scholar
  91. Ranković B, Ranković D, Kosanić M et al (2010) Antioxidant and antimicrobial properties of the lichen Anaptychya cilaris, Nephroma parile, Ochrolechia tartarea and Parmelia centrifuga. Cent Eur J Biol 5:649–665Google Scholar
  92. Ranković B, Kosanić M, Stanojković T (2011) Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcata, Lecanora atra and Lecanora muralis. BMC Complement Altern Med 11:97.  https://doi.org/10.1186/1472-6882-11-97 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Ranković B, Kosanić M, Stanojković T et al (2012) Biological activities of Toninia candida and Usnea barbata together with their norstictic acid and usnic acid constituents. Int J Mol Sci 13:14707–14722PubMedPubMedCentralCrossRefGoogle Scholar
  94. Ranković B, Kosanić M, Stanojković T (2014a) Stereocaulon pashale lichen as antioxidant, antimicrobial and anticancer agent. Farmacia 62:306–317Google Scholar
  95. Ranković B, Kosanić M, Manojlović N et al (2014b) Chemical composition of Hypogymnia physodes lichen and biological activities of some its major metabolites. Med Chem Res 23:408–416CrossRefGoogle Scholar
  96. Rezanka T, Sigler K (2007) Hirtusneanoside, an unsymmetrical dimeric tetrahydroxanthone from the lichen Usnea hirta. J Nat Prod 70:1487–1491PubMedCrossRefPubMedCentralGoogle Scholar
  97. Ristić S, Ranković B, Kosanić M et al (2016a) Phytochemical study and antioxidant, antimicrobial and anticancer activities of Melanelia subaurifera and Melanelia fuliginosa lichens. J Food Sci Technol 53:2804–2816PubMedPubMedCentralCrossRefGoogle Scholar
  98. Ristić S, Ranković B, Kosanić M et al (2016b) Biopharmaceutical potential of two Ramalina lichens and their metabolites. Curr Pharm Biotechnol 17:651–658PubMedCrossRefGoogle Scholar
  99. Rundel PW (1978) The ecological role of secondary lichen substances. Biochem Syst Ecol 6:157–170CrossRefGoogle Scholar
  100. Saenz MT, Garcia MD, Rowe JG (2006) Antimicrobial activity and phytochemical studies of some lichens from south of Spain. Fitoterapia 77:156–159PubMedCrossRefGoogle Scholar
  101. Santiago KA, Borricano JN, Canal JN et al (2010) Antibacterial activities of fruticose lichens collected from selected sites in Luzon Island, Philippines. Philipp Sci Lett 3:18–28Google Scholar
  102. Santos PS, Lat B, Palo M (1964) The antibiotic activities of some Philippine lichens. Philipp J Sci 93:325–335Google Scholar
  103. Sariozlu NY, Cankilic MY, Candan M et al (2016) Antimicrobial activity of lichen Bryoria capillaris and its compound barbatolic acid. Biomed Res India 27:419–423Google Scholar
  104. Sasidharan S, Chen Y, Saravanan D et al (2011) Extraction, isolation and characterization of bioactive compounds from plants’ extracts. Afr J Tradit Complement Altern Med 8:1–10PubMedGoogle Scholar
  105. Schmeda-Hirschmann G, Tapia A, Lima B et al (2008) A new antifungal and antiprotozoal depside from the Andean lichen Protousnea poeppigii. Phytother Res 22:349–355PubMedCrossRefGoogle Scholar
  106. Senthil Prabhu S, Sudha SS (2015) Evaluation of the antibacterial properties of some lichen species against human pathogens. Int J Adv Res Biol Sci 2:177–181Google Scholar
  107. Sharma BC, Kalikotay S, Rai B (2012) Assessment of antimicrobial activity of extracts of few common lichens of Darjeeling hills. Ind J Fund Appl Life Sci 2:120–126Google Scholar
  108. Sheldon AT (2005) Antibiotic resistance: a survival strategy. Clin Lab Sci Summer 18:170–180Google Scholar
  109. Shrestha G, Raphael J, Leavitt SD et al (2014) In vitro evaluation of the antibacterial activity of extracts from 34 species of north American lichens. Pharm Biol 27:1–5Google Scholar
  110. Sinha SN, Biswas M (2011) Evaluation of antibacterial activity of some lichen from Ravangla, Sikkim, India. Int J Pharm Bio Sci 2:B23–B28Google Scholar
  111. Sisodia R, Geol M, Verma S et al (2013) Antibacterial and antioxidant activity of lichen species Ramalina roesleri. Nat Prod Res 27:2235–2239PubMedCrossRefGoogle Scholar
  112. Srivastava P, Logesh AR, Upreti DK et al (2013) In-vitro evaluation of some Indian lichens against human pathogenic bacteria. Mycosphere 4:734–743CrossRefGoogle Scholar
  113. Stocker-Worgotter E, Elix JA, Grube M (2004) Secondary chemistry of lichen-forming fungi: chemosyndromic variation and DNA-analyses of cultures and chemotypes in the Ramalina farinacea complex. Bryologist 107(2):152–162CrossRefGoogle Scholar
  114. Stoll A, Brack A, Renz J (1950) The effect of lichenic substances on the tubercle bacillus and certain other microorganisms; seventh article on antibacterial substances. Schweiz Z Pathol Bakteriol 13:729–751PubMedGoogle Scholar
  115. Sundset MA, Kohn A, Mathiesen SD (2008) Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften 95(8):741–749PubMedCrossRefGoogle Scholar
  116. Tasdemir D, Franzblau SG (2007) In vitro antituberculotic activity of several lichen metabolites. Planta Med 73:174Google Scholar
  117. Tay T, Özdemir Türk A, Yılmaz M et al (2004) Evaluation of the antimicrobial activity of the acetone extract of the lichen Ramalina farinacea and its (+)-usnic acid, norstictic acid, and protocetraric acid constituents. Z Naturforsch C 59(5–6):384–388PubMedCrossRefGoogle Scholar
  118. Tiwari P, Rai H, Upreti DK et al (2011) Assessment of antifungal activity of some Himalayan foliose lichen against plant pathogenic fungi. Am J Plant Sci 2:841–846CrossRefGoogle Scholar
  119. Tomasi S, Picard S, Lainé C et al (2006) Solid-phase synthesis of polyfunctionalized natural products: application to usnic acid, a bioactive lichen compound. J Comb Chem 8:11–14PubMedCrossRefPubMedCentralGoogle Scholar
  120. Tomović J, Kosanić M, Ristić S et al (2017) Chemical composition and bioactive properties of the lichen, Pleurosticta acetabulum. Trop J Pharm Res 16:2977–2984CrossRefGoogle Scholar
  121. Türk OA, Yılmaz M, Kıvanc M et al (2003) The antimicrobial activity of extracts of the lichen Cetraria aculeate and its protolichesterinic acid constituent. Z Naturforsch C 58:850–854PubMedCrossRefPubMedCentralGoogle Scholar
  122. Turk H, Yılmaz M, Tay T et al (2006) Antimicrobial activity of extracts of chemical races of the lichen Pseudoevernia furfuracea and their physodic acid, chloroatratorin, atratorin and olivetoric acid constituents. Z Naturforsch C 61(7–8):499–507PubMedCrossRefGoogle Scholar
  123. Vartia KO (1973) Antibiotics in lichens. In: Ahmadjian V, Hale ME Jr (eds) The lichens. Academic, New York, NY, pp 547–561CrossRefGoogle Scholar
  124. Verma N, Behera BC, Parizadeh H et al (2011) Bactericidal activity of some lichen secondary compounds of Cladonia ochrochlora, Parmotrema nilgherrensis and Parmotremasanctiangelii. Int J Drug Dev Res 3:222–232Google Scholar
  125. Vivek MN, Kambar Y, Manasa M et al (2014) Radical scavenging and antibacterial activity of three Parmotrema species from Western Ghats of Karnataka, India. J Appl Pharm Sci 4:086–091Google Scholar
  126. Whiton JC, Lawrey JD (1982) Inhibition of Cladonia cristatella and Sordaria fimicola ascospore germination by lichen acids. Bryologist 85:222–226CrossRefGoogle Scholar
  127. Yilmaz M, Turk AO, Tay T et al (2004) The antimicrobial activity of extracts of the lichen Cladonia foliacea and its (-)-usnic acid, atranorin and fumaprocetraric acid constituents. Z Naturforsch C 59:149–254CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Marijana Kosanić
    • 1
  • Branislav Ranković
    • 1
  1. 1.Department of Biology, Faculty of ScienceUniversity of KragujevacKragujevacSerbia

Personalised recommendations