Abstract
Lichens are fungal and algal/cyanobacterial symbioses resulting in the production of specific metabolites. Some of these are forming an available biomass for phytochemical investigations, including the assessment of biological activities of the isolated compounds. The alpine or polar region are characterised by highly stressful environmental conditions for many organisms, but lichens are among the dominating organisms in these habitats. In the performant mutual protective system, lichen fungi often accumulate high amounts of metabolites with specific physicochemical properties (UV absorbents, hydrophobicity) which help the lichens to survive. Unique secondary metabolites and polysaccharides have been isolated and tested from these organisms. Even though this has been tested until now only with a low number of compounds so far, interesting activities have been recorded. We review here some of the antimicrobial, anti-inflammatory, antiproliferative and antioxidant activities properties described. Solutions with axenic biotechnological cultivation of each symbiotic partner and particularly the mycobiont to obtain the lichen secondary metabolites are challenging to overcome the limitations for the supply of these rare compounds. Additionally, these lichens appear to harbour a diversity of culturable microorganisms from which active compounds have also been isolated recently.
Similar content being viewed by others
References
Ara G, Teicher BA (1996) Cyclooxygenase and lipooxygenase inhibitors in cancer therapy. Prostaglandins Leukot Essent Fatty Acids 54:3–16
Asta J (1984) Flore et végétation lichéniques des étages alpin supérieur et nival des Alpes Nord-Occidentales françaises. Documents d’écologie Pyrénéenne 3–4:119–123
Asta J, Juge C, Gout E et al (1999) Lichens: models to study the adaptation to extrem high mountain environment. Bull Inf Ass Fr Lichénol Mémoires 3:131
Aubert S, Juge C, Boisson AM et al (2007) Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environments. Planta 226:1287–1297
Baron M, Iacomini M, Fanta ES, Gorin PAJ (1991) Galactomannan, lichenan and isolichenan from the polysaccharide-rich lichen Neuropogon aurantiaco-ater. Phytochemistry 30(9):3125–3126
Barry VC, Twomey D (1950) Antituberculous substances. VI. Derivatives of diploicin. Proc R Irish Acad 53B:55–59
Bartak M, Hajek J, Vrablikova H et al (2004) High-light stress and photoprotection in Umbilicaria antartica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. Plant Biol 6:333–341
Bazin MA, Le Lamer AC, Delcros JG et al (2008) Synthesis and cytotoxic activities of usnic acid derivatives. Bioorg Med Chem 16:8737–8744
Beckett RP, Kranner I, Minibayeva FV (2008) Stress physiology and the symbiosis. In: Nash TH (ed) Lichen biology. Cambridge University Press, Cambridge, pp 134–151
Behera BC, Adawadkar B, Makhija U (2003) Inhibitory activity of xanthine oxidase and superoxide-scavenging activity in some taxa of the lichen family Graphidaceae. Phytomedicine 10:536–543
Bézivin C, Tomasi S, Rouaud I et al (2004) Cytotoxic activity of compounds from the lichen: Cladonia convoluta. Planta Med 70:877–880
Bhattarai HD, Paudel B, Hong SG et al (2008) Thin layer chromatography analysis of antioxidant constituents of lichens from Antarctica. J Nat Med 62:481–484
Bjerke JW, Lerfall K, Elvebakk A (2002) Effects of ultraviolet radiation and PAR on the content of usnic and divaricatic acids in two arctic-alpine lichens. Photochem Photobiol Sci 1:678–685
Bjerke JW, Elvebakk A, Dominguez E et al (2005) Seasonal trends in usnic acid concentrations of Arctic, alpine and Patagonian populations of the lichen Flavocetraria nivalis. Phytochemistry 66:337–344
Bodo B, Molho D (1980) Structure des acides isomuronique et neuropogolique, nouveaux acides aliphatiques du lichen Neuropogon trachycarpus. Phytochemistry 19:1117–1120
Borkowski B, Wozniak W, Gertig H et al (1964) Bacteriostatic action of some compounds from lichen Cetraria islandica and of usnic acid. Dissertationes Pharmaceuticae 16:189–194
Boustie J, Grube M (2005) Lichens, a promising source of bioactive secondary metabolites. Plant Genet Resour 3:273–287
Boustie J, Lohézic-Le Dévéhat F (2008) Lichen extracts and cancer. In: Watson RR, Preedy VR (eds) Botanical medicine in clinical practice. CAB International, Trowbridge, pp 356–364
Brunauer G, Hager A, Krautgartner WD et al (2006) Experimental studies on Lecanora rupicola (L.) Zahlbr.: chemical and microscopical investigations of the mycobiont and re-synthesis stages. Lichenologist 38:577–585
Brunauer G, Hager A, Grube M et al (2007) Alteration in secondary metabolism of aposymbiotically grown mycobionts of Xanthoria elegans and culture resynthesis stages. Plant Physiol Biochem 45:146–151
Bucar F, Schneider I, Ogmundsdottir H et al (2004) Anti-proliferative lichen compounds with inhibitory activity on 12(S)-HETE production in human platelets. Phytomedicine 11:602–606
Burkholder PR, Evans AW, McVeigh I et al (1945) Further studies on the antibiotic activity of lichens. Bull Torrey Bot Club 72:157–164
Burlando B, Ranzanto E, Volante A et al (2009) Antiproliferative effects on tumour cells and promotion of keratinocyte wound healing by different lichen compounds. Planta Med 75:607–613
Carbonero ER, Smiderle FR, Gracher AHP et al (2006) Structure of two glucans and a galactofuranomannan from the lichen Umbilicaria mammulata. Carbohydr Polym 63:13–18
Cetin H, Tufan-Cetin O, Turk OA, Tay T, Candan M, Yanikoglu A, Sumbul H (2008) Insecticidal activity of major lichen compounds, (-) and (+) usnic acid, against the larvae of house mosquito, Culex pipiens L. Parasitol Res 102:1277–1279
Cheenpracha S, Vidor NB, Yoshida WY, Davies J, Chang LC (2010) Coumabiocins A−F, aminocoumarins from an organic extract of Streptomyces sp. L-4-4. J Nat Prod 73:880–884
Choi H-S, Yim JH, Lee HK et al (2009) Immunomodulatory effects of polar lichens on the function of macrophages in vitro. Mar Biotechnol 11:90–98
Chooi YH, Stalker DM, Davis MA et al (2008) Cloning and sequence characterization of a non-reducing polyketide synthase gene from the lichen Xanthoparmelia semiviridis. Mycol Res 112:147–161
Choudhary MI, Saima Jalil A, Atta-ur-Rahman (2005) Bioactive phenolic compounds from a medicinal lichen, Usnea longissima. Phytochemistry 66:2346–2350
Correché ER, Carrasco M (2002) Cytotoxic screening activity of secondary lichen metabolites. Acta Farm Bonaerense 21:273–278
Correché ER, Enriz RD, Piovano M et al (2004) Cytotoxic and apoptotic effects on hepatocytes of secondary metabolites obtained from lichens. ATLA 32:605–615
Cox PA, Banack SA, Murch SJ et al (2005) Diverse taxa of cyanobacteria produce β-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci 102:5074–5078
Cragg GM, Newman EDJ (2009) Nature: a vital source of leads for anticancer drug development. Phytochem Rev 8:313–331
Czeczuga B, Obermayer W, Upreti DK, Sharma LR (1996) Carotenoids in lichens in various regions of the Himalayas. J Hattori Bot Lab 80:323–330
da Silva Santos NP, Nascimento SC, Wanderley MSO et al (2006) Nanoencapsulation of usnic acid: an attempt to improve antitumour activity and reduce hepatotoxicity. Eur Pharm Biopharm 64:154–160
Davies J, Wang H, Taylor T et al (2005) Uncialamycin, a new enediyne antibiotic. Org Lett 7:5233–5236
De Carvahlo EAB, Andrade PP, Silva NH, Pereira EC, Figueiredo RCBQ (2005) Effect of usnic acid from the lichen Cladonia substellata on Trypanosoma cruzi in vitro: an ultrastructural study. Micron 36:155–161
de la Torre R, Garcia-Sancho L, Horneck G (2007) Adaptation of the lichen Rhizocarpon geographicum to harsh high-altitude conditions: relevance to a habitable Mars. Eur Space Agency SP-1299:145–150
Demleitner S, Kraus J, Franz G (1991) Synthese und antitumoraktivitat von Licheninderivaten. Pharm Unserer Zeit 20:120
Denton GH, Karlén W (1973) Lichenometry: its application to Holocene moraine studies in Southern Alaska and Swedish Lapland. Arctic Alpine Res 5:347–352
Ding G, Li Y, Fu S et al (2009) Ambuic acid and torreyanic acid derivatives from the endolichenic fungus Pestalotiopsis sp. J Nat Prod 72:182–186
Durazo FA, Lassman C, Han SHB et al (2004) Fulminant liver failure due to usnic acid for weight loss. Am J Gastroenterol 99:950–952
Edwards HGM, Newton EM, Wynn-Williams DD (2003) Molecular structural studies of lichen substances II: atranorin, gyrophoric acid, fumarprotocetraric acid, rhizocarpic acid, calycin, pulvinic dilactone and usnic acid. J Mol Struct 651–653:27–37
Elix JA, Øvstedal DO (2004) A new Lecanora species from the Arctic with a remarkable chemistry. Graphis Scripta 15:57–59
Elix JA, Stocker-Wörgötter E (2008) Biochemistry and secondary metabolites. In: Nash TH III (eds) Lichen biology. Cambridge University Press, Cambridge, pp 353–363
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. Naturwissenschaften 94:465–468
Elvebakk A, Bjerke JW (2006) The Skibotn area in North Norway—an example of very high lichen species richness far to the north. Mycotaxon 96:141–146
Ernst-Russel MA, Elix JA, Chai CL et al (1999) Hybocarpone, a novel cytotoxic naphthazarin derivative from mycobiont cultures of the lichen Lecanora hybocarpa. Tetrahedron Lett 40:6321–6324
Fazio AT, Adler MT, Bertoni MD, Sepúlveda CS, Damonte EB, Maier MS (2007) Lichen secondary metabolites from the cultured lichen mycobionts of Teloschistes chrysophthalmus and Ramalina celastri and their antiviral activities. Z Naturforsch C 62:543–549
Fernandez E, Quilhot W, Rubio C et al (2006) Effects of UV radiation on usnic acid in Xanthoparmelia microspora (Müll. Arg. Hale). Photochem Photobiol 82:1065–1068
Feuerer T, Hawksworth DL (2007) Biodiversity of lichens, including a world-wide analysis of checklist data based on Takhtajan’s floristic regions. Biodivers Conserv 16:85–98
Francolini I, Norris P, Piozzi A et al (2004) Usnic acid, a natural antimicrobial agent able to inhibit bacterial biofilm and formation on polymer surfaces. Antimicrob Agents Chemother 48:4360–4365
Freysdottir J, Omarsdottir S, Ingolfsdottir K et al (2008) In vitro and in vivo immunomodulating effects of traditionally prepared extract and purified compounds from Cetraria islandica. Int Immunopharmacol 8:423–430
Friedmann EI, Sun H (2005) Communities adjust their temperature optima by shifting producer-to-consumer ratio, shown in lichens as models: I. hypothesis. Microb Ecol 49:523–527
Frisvad JC, Larsen TO, Dalsgaard PW et al (2005) Four psychrotolerant species with high chemical diversity consistently producing cycloaspeptide A, Penicillium jamesonlandense sp. nov., Penicillium ribium sp. nov., Penicillium soppii and Penicillium lanosum. Int J System Evol Microbiol 56:1427–1437
Fukuoka F, Nakanishi M, Shibata S et al (1968) Polysaccharides in lichens and fungi. II. Antitumor activities on sarcoma-180 of the polysaccharide preparations from Gyrophora esculenta Miyoshi, Cetraria islandica (L.) Ach. var. orientalis Asahina, and some other lichens. Gann 59:421–432
Gagunashvili AN, Daviðsson SP, Jónsson ZO et al (2009) Cloning and heterologous transcription of a polyketide synthase gene from the lichen Solorina crocea. Mycol Res 113:354–363
Gauslaa Y, Solhaug KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecol 126:462–471
Gissurarson S, Sigurdsson S, Wagner H, Ingolfsdottir K (1997) Effect of lobaric acid on cysteinyl-leukotriene formation and contractile activity of Guinea Pig Taenia coli. J Pharmacol Exp Ther 280:770–773
Gonzales I, Ayuso-Sacido A, Anderson A et al (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 54:401–415
Gray D, Nicolaou KC (2004) Total synthesis of hybocarpone and analogues thereof. A facile dimerization of naphthazarins to pentacyclic systems. J Am Chem Soc 126:607–612
Grube M, Cardinale M, Vieira de Castro J et al (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbiosis. ISME J 3:1105–1115
Gulcin I, Oktay M, Kufrevioglu OI et al (2002) Determination of antioxidant activity of lichen Cetraria islandica (L) Ach. J Ethnopharmacol 79:325–329
Hamada N, Ueno T (1987) Depside from an isolated lichen mycobiont. Agric Biol Chem 51:1705–1706
Hamada N, Miyagawa H, Miyawaki H et al (1996) Lichen substances in mycobionts of crustose lichens cultured on media with extra sucrose. Bryologist 99:71–74
Haralsdottir S, Guolaugsdottir E, Ingolfsdottir K et al (2004) Anti-proliferative effects of lichen-derived lipoxygenase inhibitors on twelve human cancer cell lines of different tissue origin in vitro. Planta Med 70:1098–1100
Hauck M, Juergens S-R, Willenbruch K et al (2009) Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens. Ann Bot 103:13–22
Hausen BM, Emde L, Marks V (1993) An investigation of the allergic constituents of Cladonia stellaris (Opiz)Pous&Vezda (silver moss, reindeer moss or reindeer lichen). Contact Derm 28:70–76
He H, Bigelis R, Yang HY et al (2005) Lichenicolins A and B, new bisnaphthopyrones from an unidentified lichenicolous fungus, strain LL-RB0668. J Antibiot 58:731–736
Heber U, Bilger W, Bligny R et al (2000) Phototolerance of lichens, mosses and higher plants in an alpine environment: analysis and photoreactions. Planta 211:770–780
Hidalgo ME, Bascunan L, Quilhot W et al (2005) Spectroscopic and photochemical properties of the lichen compound lobaric acid. Photochem Photobiol 81:1447–1449
Hirayama T, Fujikawa F, Kasahara T et al (1980) Anti-tumor activities of some lichen products and their degradation products. Yakugaku Zasshi 100:755–759
Horhant D, Le Lamer AC, Boustie J et al (2007) Separation of a mixture of paraconic acids from Cetraria islandica (L.) Ach. employing a fluorous tag-catch and release strategy. Tetrahedron Lett 48:6031–6033
Huneck S (1999) The significance of lichens and their metabolites. Naturwissenschaften 86:559–570
Huneck S, Yoshimura I (1996) Identification of Lichen substances. Springer, Berlin, p 493
Iacomini M, Schneider CL, Gorin PAJ (1985) Comparative studies on the polysaccharides of Cladonia alpestris (reindeer moss), Cladonia confusa and Cladonia amaurocraea. Carbohydr Res 142:237–251
Ingolfsdottir K (2000) Bioactive compounds in Iceland moss. In: Paulsen BS (ed) Bioactive carbohydrate polymers, vol 44. Kluwer Academic Publishers, Dordrecht, pp 25–36
Ingolfsdottir K (2002) Molecules of interest – usnic acid. Phytochemistry 61:729–736
Ingolfsdottir K, Gudmundsdottir GF (2002) Effects of tenuiorin and methyl orsellinate from the lichen Peltigera leucophlebia on 5-/15-lipoxygenases and proliferation of malignant cell lines in vitro. Phytomedicine 9:654–658
Ingolfsdottir K, Bloomfield SF, Hylands PJ (1985) In vitro evaluation of the antimicrobial activity of lichen metabolites as potential preservatives. Antimicrobial Agents Chem 28:289–292
Ingolfsdottir K, Breu W, Huneck S et al (1994a) In vitro inhibition of 5-lipoxygenase by protolichesterinic acid from Cetraria islandica. Phytomedicine 1:187–191
Ingolfsdottir K, Jurcic K, Fischer B et al (1994b) Immunologically active polysaccharide from Cetraria islandica. Planta Med 60:527–531
Ingolfsdottir K, Gissurarson SR, Müller-Jakic B, Breu W, Wagner H (1996) Inhibitory effects of the lichen metabolite lobaric acid on arachidonate metabolism in vitro. Phytomedicine 2(3):243–246
Ingolfsdottir K, Gissurarson SR, Nenninger A et al (1997a) Biologically active alkamide from the lichen Stereocaulon alpinum. Phytomedicine 4:331–334
Ingolfsdottir K, Hjalmarsdottir K, Sigurdsson MA et al (1997b) In vitro susceptibility of Helicobacter pylori to protolichesterinic acid from the lichen Cetraria islandica. Antimicrobial Agents Chem 41:215–217
Ingolfsdottir K, Wiedemann B, Birgisdottir M et al (1997c) Inhibitory effects of baeomycesic acid from the lichen Thamnolia subuliformis on 5-lipoxygenase in vitro. Phytomedicine 4:125–128
Ingolfsdottir K, Chung GA, Skulason VG et al (1998) Antimycobacterial activity of lichen metabolites in vitro. Eur J Pharm Soc 6:141–1444
Ivanova V, Schlegel R, Grafe U (2000) 2-Methoxy-4, 5, 7-trihydroxy-anthraquinone, a new lichen metabolite produced by Xanthoria parietina. Pharmazie 55:785–786
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 57:73–74
Kim J-W, Song K-S, Yoo I-D et al (1996) Two phenolic compounds isolated from Umbilicaria esculenta as phospholipase A2 inhibitors. Han’guk Kyunhakhoechi 24:237–242
Kranner I, Cram WJ, Zorn M et al (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci 102:3141–3146
Kristmundsdottir T, Aradottir HA, Ingolfdottir K et al (2002) Solubilization of the lichen metabolite (+)-usnic acid for testing in tissue culture. Pharm Pharmacol 54:1447–1452
Kumar S, Muller K (1999) Lichen metabolites. II. Antiproliferative and cytotoxic activity of gyrophoric, usnic and diffractaic acid on human keratinocyte growth. J Nat Prod 62:821–823
Kupchan S, Kopperman H (1975) Usnic acid: tumor inhibitor isolated from lichens. Experientia 31:625
Lawrey JD, Diederich P (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106:81–120
Leuckert C, Buschardt A, Hertel H (1981) Die Verteilung der Chemotypen von Dimelaena oreina (Lichenes) auf verschiedene Hohenstufen an einem Transekt im Vinschagau (Sudtirol, Italien). Nova Hedwigia 34:623–631
Leuckert C, Ahmadjian V, Culberson CF et al (1990) Xanthones and depsidones of the lichen Lecanora dispersa in nature and of its mycobiont in culture. Mycologia 82:370–378
Lin X, Cai Y-G, Li Z-X et al (2003) Structure determination, apoptosis induction and telomerase inhibition of CFP-2, a novel lichenin from Cladonia furcata. Biochem Biophys Acta 1622:99–108
Lohézic-Le Dévéhat F, Tomasi S, Bernard A et al (2007) Stictic acid derivatives from the lichen Usnea articulata L. and their antioxidant activities. J Nat Prod 70:1218–1220
Lopes TIB, Coelho RG, Yoshida NC et al (2008) Radical-scavenging activity of Orsellinates. Chem Pharm Bull 56:1551–1554
Magarvey NA, Beck ZQ, Golakoti T et al (2006) Biosynthetic characterization and chemoenzymatic assembly of the cryptophycins. Potent anticancer agents from cyanobionts. ACS Chem Biol 1:766–779
Manojlovic NT, Solujic S, Sukdolak S et al (1998) Anthraquinones from the lichen Xanthoria parietina. J Serb Chem Soc 63:7–11
Margesin R, Jud M, Tscherko D et al (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol Ecol 67:208–218
Mayer M, O’Neill MA, Murray KE et al (2005) Usnic acid: a non-genotoxic compound with anti-cancer properties. Anticancer Drugs 16:805–809
Micheletti AC, Beatriz A, de Lima DP et al (2009) Constituintes químicos de Parmotrema lichexanthonicum Eliasaro & Adler—isolamento, modificações estruturais e avaliação das atividades antibiótica e citotóxica. Quim Nova 32:12–20
Min T-J, Bae K-G (1996) Structure and antibiotic activities of phenolic compounds from Umbilicaria vellea. Kor J Chem Soc 40(9):623–629
Molina MC, Crespo A, Vicente C et al (2003) Differences in the composition of phenolics and fatty acids of cultured mycobiont and thallus of Physconia distorta. Plant Physiol Biochem 41:175–180
Morita H, Tsuchiya T, Kishibe K et al (2009) Antimitotic activity of lobaric acid and a new benzofuran, sakisacaulon A from Stereocaulon sasakii. Bioorg Med Chem Lett 19:3679–3681
Motohashi K, Takagi M, Yamamura H, Hayakawa M, Shin-ya K (2010) A new angucycline and a new butenolide isolated from lichen-derived Streptomyces spp. J Antibiot 63:545–548
Muggia L, Schmitt I, Grube M (2009) Lichens as treasure chests of natural products. Sim News 59:85–97
Muller K (2001) Pharmaceutically relevant metabolites from lichens. Appl Microbiol Biotechnol 56:9–16
Neff GW, Reddy KR, Durazo FA et al (2004) Severe hepatotoxicity associated with the use of weight loss diet supplements containing ma huang or usnic acid. J Hepatol 41:1062–1064
Neufeld JD, Mohn WW (2005) Unexpectedly high bacterial diversity in arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl Environ Microbiol 71:5710–5718
Nimis PL, Skert N (2006) Lichen chemistry and selective grazing by the coleopteran Lasioderma serricorne. Environ Exp Bot 55:175–182
Nishikawa Y, Ohno H (1981) Studies on the water-soluble constituents of lichens. IV. Effect of the antitumor lichen-glucans and related derivatives on the phagocytic activity of the reticuloendothelial system in mice. Chem Pharm Bull 29:3407–3410
Nishikawa Y, Takeda T, Shibata S et al (1969) Polysaccharides in lichens anf fungi. III. Further investigation on the structures and the antitumor activity of the polysaccharides from Gyrophora esculenta Miyoshi and Lasallia papulosa Llano. Chem Pharm Bull 17:1910–1916
Nolan TJ, Algar J, McCann EP et al (1948) Chemical constituents of lichens found in Ireland Buellia canescens. III. Constitution of diploicin. Sci Proc R Dublin Soc 24A:319–334
Nybakken L, Solhaug KA, Bilger W et al (2004) The lichens Xantoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats. Oecol 140:211–216
Odabasoglu F, Aslan A, Cakir A et al (2005) Antioxidant activity, reducing power and total phenolic content of some lichen species. Fitoterapia 76:216–219
Ogmundsdottir HM, Zoega GM, Gissurarson SR et al (1998) Anti-proliferative effects of lichen-derived inhibitors of 5-lipoxygenase on malignant cell-lines and mitogen-stimulated lymphocytes. J Pharm Pharmacol 50:107–115
Oksanen I (2006) Ecological and biotechnological aspects of lichens. Appl Microbiol Biotechnol 73:723–734
Oksanen I, Jokela J, Fewer DP et al (2004) Discovery of rare and highly toxic microcystins from lichen-associated cyanobacterium Nostoc sp. strain IO-102-I. Appl Environ Microbiol 70:5756–5763
Olafsdottir ES, Ingolfdottir K (2001) Polysaccharides from lichens: structural characteristics and biological activity. Planta Med 67:199–208
Olafsdottir ES, Omarsdottir S, Smestad Paulsen B et al (1999) Rhamnopyranogalactofuranan, a new immunologically active polysaccharide from Thamnolia subuliformis. Phytomedicine 6:273–279
Olafsdottir ES, Omarsdottir S, Paulsen BS et al (2003) Immunologically active O6-branched (1–3)-b-glucan from the lichen Thamnolia vermicularis var. subuliformis. Phytomedicine 10:318–324
Omarsdottir S, Olafsdottir ES, Freysdottir J (2006a) Immunomodulating effects of lichen-derived polysaccharides on monocytes-derived dentritic cells. Int Immunopharmacol 6:1642–1650
Omarsdottir S, Petersen H, Barsett H et al (2006b) Structural characterisation of a highly branched galactomannan from the lichen Peltigera canina by methylation analysis and NMR-spectroscopy. Carbohydr Polym 63:54–60
Omarsdottir S, Freysdottir J, Olafsdottir ES (2007) Immunomodulating polysaccharides from the lichen Thamnolia vermicularis var. subuliformis. Phytomedicine 14:179–184
Paudel B, Bhattarai HD, Lee HG et al (2008) Antibacterial potential of Antarctic lichens against human pathogenic gram-positive bacteria. Phytother Res 22:1269–1271
Pengsuparp T, Cai L, Constant H et al (1995) Mechanistic evaluation of new plant-derived compounds that inhibit HIV-1 reverse transcriptase. J Nat Prod 58:1024–1031
Piovano M, Garbarino JA, Giannini FA et al (2002) Evaluation of antifungal and antibacterial activities of aromatic metabolites from lichens. Bol Soc Chil Quim 47:235–240
Podterob AP (2008) Chemical composition of lichens and their medical application. Pharm Chem J 42:582–588
Rancan F, Rosan S, Boehm K et al (2002) Protection against UVB irradiation by natural filters extracted from lichens. J Photochem Photobiol B 68:133–139
Rankovic B, Misic M, Sukdolak S (2007) Evaluation of antimicrobial activity of the lichens Lasallia pustulata, Parmelia sulcata, Umbilicaria crustulosa, and Umbilicaria cylindrica. Microbiol 76:723–727
Reddy VM, O’Sullivan JF, Gangadharam PR (1999) Antimycobacterial activities of riminophenazines. J Antimicrob Chemother 43:616–623
Rezanka T, Dembitsky V (1999) Novel brominated lipidic compounds from lichens of central Asia. Phytochemistry 51:963–968
Rezanka T, Guschina IA (2000) Glycosidic compounds of murolic, protoconstipatic and allo-murolic acids from lichens of central Asia. Phytochemistry 54:635–645
Rezanka T, Guschina IA (2001) Macrolactone glycosides of three lichen acids from Acarospora gobiensis, a lichen of central Asia. Phytochemistry 58:1281–1287
Riedel K, Boustie J, Eberl L et al (2008) Effect of lichen secondary metabolites on bacterial functions and biofilm formation. Planta Med 74:960
Rubio C, Fernandez E, Hidalgo ME et al (2002) Effects of solar UV-B radiation in the accumulation of rhizocarpic acid in a lichen species from alpine zones of Chile. Bol Soc Chil Quim 47:213–217
Russo A, Piovano M, Lombardo L et al (2006) Pannarin inhibits cell growth and induces cell death in human prostate carcinoma DU145 cells. Anticancer Drugs 17:1163–1169
Russo A, Piovano M, Lombardo L et al (2008) Lichen metabolites prevent UV light and nitric-oxide mediated plasmid DNA damage and induce apoptosis in human melanoma cells. Life Sci 83:468–474
Sankawa U, Shibuya M, Ebizuka Y et al (1982) Depside as potent inhibitor of prostaglandin biosynthesis: a new active site model for fatty acid cyclooxygenase. Prostaglandins 24:21–34
Schmeda-Hirschmann G, Tapia A, Lima B et al (2008) A new antifungal and antiprotozoal depside from the Andean Lichen Protousnea poeppigii. Phytother Res 22:349–355
Schmitt I, Kautz S, Lumbsch HT (2008) 6-MSAS-like polyketide synthase genes occur in lichenized ascomycetes. Mycol Res 112:289–296
Seephonkai P, Isaka M, Kittakoop P et al (2002) Evaluation of antimycobacterial, antiplasmodial and cytotoxic activities of preussomerins isolated from the lichenicolous fungus Microsphaeropsis sp. BCC 3050. Planta Med 68:45–48
Selbmann L, Zucconi L, Ruisi S et al (2010) Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance. Polar Biol 33:71–83
Seo C, Sohn JH, Park SM et al (2008a) Usimines A-C, bioactive usnic acid derivatives from the Antarctic Lichen Stereocaulon alpinum. J Nat Prod 71:710–712
Seo C, Yim JH, Lee HK et al (2008b) Stereocalpin A, a bioactive cyclic depsipeptide from the Antarctic lichen Stereocaulon alpinum. Tetrahedron Lett 49:29–31
Seo C, Sohn JH, Ahn JS et al (2009) Protein tyrosine phosphatase 1B inhibitory effects of depsidone and pseudodepsidone metabolites from the Antarctic lichen Stereocaulon alpinum. Bioorg Med Chem Lett 19:2801–2803
Singh J, Upreti DK, Bajpai R et al (2008) Effect of altitudinal changes on photosynthetic pigment concentration in some cryptogams. J Ecophys Occup Health 8:107–110
Smestad Paulsen B, Olafsdottir ES, Ingolfdottir K (2002) Chromatography and electrophoresis in separation and characterization of polysaccharides from lichens. J Chromatogr A 967:163–171
Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in arctic subglacial ice. Microb Ecol 52:207–216
Stepanenko LS, Krivoshchekova OE, Skirina IF (2002) Functions of phenolic secondary metabolites in lichens from far east Russia. Symbiosis 32:119–131
Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep 25:188–200
Stocker-Wörgotter E, Elix JA (2006) Morphogenetic strategies and induction of secondary metabolite biosynthesis in cultured lichen-forming Ascomycota, as exemplified by Cladia retipora (Labill.) Nyl. and Dactylina arctica (Richards) Nyl. Symbiosis 41:9–20
Sundset MA, Kohn A, Mathiesen SD et al (2008) Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften 95:741–749
Takahashi K, Kinoshita K, Yamamoto Y et al (2005) Chemical constituents from lichens for pharmaceutical and industrial uses. Folia Cryptogam Est 41:109–114
Takai M, Uehara Y, Beisler JA (1979) Usnic acid derivatives as potential antineoplastic agents. J Med Chem 22:1380–1384
Thune PO, Solberg PO (1980) Photosensitivity and allergy to aromatic lichen acids, compositae oeoresins and other plant substances. Contact Derm 6:64–71
Tomasi S, Picard S, Lainé C et al (2006) A solid-phase synthesis of polyfunctionalized natural products: application to usnic acid, a bioactive lichen compound. J Comb Chem 8:11–14
Torres A, Hochberg M, Pergament I et al (2004) A new UV-B absorbing mycosporine with photo protective activity from the lichenized ascomycete Collema cristatum. Eur J Biochem 271:780–784
Troll C (1973) High mountain belts between the polar caps and the equator: their definition and lower limit. Arctic Alpine Res 5:19–27
Turk OA, Meral Y, Merih K et al (2003) The antimicrobial activity of extracts of the lichen Cetraria aculeata and its protolichesterinic acid constituent. Z Naturforsch C 58:850–854
Vegar Storeheier P, Mathiesen SD, Tyler NJC et al (2002) Nutritive value of terricolous lichens for reindeer in winter. Lichenologist 34:247–257
Weerapreeyakul N, Anorach R, Khuansawad T et al (2007) Synthesis of bioreductive esters from fungal compounds. Chem Pharm Bull 55:930–935
Weissman L, Garty J, Hochman A (2005a) Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration. Appl Environ Microbiol 71:6508–6514
Weissman L, Garty J, Hochman A (2005b) Rehydration of the lichen Ramalina lacera results in production of reactive oxygen species and nitric oxide and a decrease in antioxidants. Appl Environ Microbiol 71:2121–2129
Williams DE, Davies J, Patrick BO et al (2008) Cladoniamides A-G, tryptophan-derived alkaloids produced in culture by Streptomyces uncialis. Org Lett 10:3501–3504
Wynn-Williams DD, Edwards HGM (2000) Adaptation of the lichen Rhizocarpon geographicum to harsh high-altitude conditions: relevance to a habitable Mars. Planet Space Sci 48:1065–1075
Yamamoto Y, Mizuguchi R, Takayama S et al (1987) Effects of culture conditions on the growth of Usneaceae lichen tissue cultures. Plant Cell Physiol 28:1421–1426
Yamamoto Y, Miura Y, Kinoshita Y et al (1995) Screening of tissue cultures and thalli of lichens and some of their active constituents for inhibition of tumor promoter-induced Epstein-Barr virus activation. Chem Pharm Bull 43:1388–1390
Yang X, Shimiazu Y, Steiner JR et al (1993) Nostoclide I and II, extracellular metabolites from a symbiotic cyanobacterium, Nostoc sp., from the lichen Peltigera canina. Tetrahedron Lett 34:761–764
Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020
Acknowledgments
Authors acknowledge Juliette Asta, University of Grenoble for very useful documentation and suggestion to visit http://jlcheype.free.fr/classification/Lichens/Lichens.htm, for alpine mushrooms and lichens pictures, thanking Jean-Louis Cheype for his support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Boustie, J., Tomasi, S. & Grube, M. Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem Rev 10, 287–307 (2011). https://doi.org/10.1007/s11101-010-9201-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-010-9201-1