Current Results on Biological Activities of Lichen ... - Lichens and Me

Review 

<strong>Current</strong> <strong>Results</strong> on Biological Activities of Lichen Secondary 

Metabolites: a Review 

Katalin Molnár a, * and Edit Farkas b 

a 

Duke University, Department of Biology, Durham, NC 27708-0338, USA. 

Fax: +1 91 96 60 72 93. E-mail: kmcz100@gmail.com 

b 

Institute of Ecology and Botany, Hungarian Academy of Sciences, H-2163 Vácrátót, 

Hungary 

* Author for correspondence and reprint requests 

Z. Naturforsch. 65 c, 157 – 173 (2010); received October 2/November 4, 2009 

Lichens are symbiotic organisms of fungi and algae or cyanobacteria. Lichen-forming 

fungi synthesize a great variety of secondary metabolites, many of which are unique. Developments 

in analytical techniques and experimental methods have resulted in the identification 

of about 1050 lichen substances (including those found in cultures). In addition 

to their role in lichen chemotaxonomy and systematics, lichen secondary compounds have 

several possible biological roles, including photoprotection against intense radiation, as well 

as allelochemical, antiviral, antitumor, antibacterial, antiherbivore, and antioxidant action. 

These compounds are also important factors in metal homeostasis and pollution tolerance 

of lichen thalli. Although our knowledge of the contribution of these extracellular products 

to the success of the lichen symbiosis has increased significantly in the last decades, their 

biotic and abiotic roles have not been entirely explored. 

Key words: Lichens, Secondary Compounds 

Introduction 

Biochemical research of lichenized fungi went 

through “exponential” development as it was 

summarized in a review by Culberson and W. L. 

Culberson (2001) who forecasted development 

in various directions. They greatly contributed to 

the development of this field by establishing new 

methods of chemical analysis (Culberson, 1972a, 

1974; Culberson and Kristinsson, 1970), compiling 

known compounds and structures (Culberson, 

1969a, 1970; Culberson et al., 1977a), and continuing 

research over decades (from W. L. Culberson, 

1955, 1957, 1958; Culberson 1963a, b; W. L. Culberson 

and Culberson, 1956; Culberson and W. 

L. Culberson, 1958; to Brodo et al., 2008). They 

emphasized that, while most of this research concerned 

the discovery and study of new substances, 

that knowledge was incomplete, even with the development 

of analytical methods. 

However, substantial changes are expected in 

this field with the exploration of the biological/ 

ecological role of lichen substances, along with increased 

use and importance of lichens. Molecular 

biological research on fungi (Fehrer et al., 2008; 

Lutzoni et al., 2004; Nelsen and Gargas, 2008, 2009; 

Nordin et al., 2007; Stenroos et al., 2002; Zhou et 

al., 2006) and experimental techniques (e.g., culturing: 

Brunauer et al., 2006, 2007; Culberson and 

Armaleo, 1992; Hager and Stocker-Wörgötter, 

2005; Hamada, 1989; Joneson and Lutzoni, 2009; 

Stocker-Wörgötter, 2001) are becoming more 

easily and widely adaptable to lichenology. These 

techniques have already revolutionized research 

on the use of lichen substances. This paper focuses 

on recent studies done since previous reviews 

(Boustie and Grube, 2005; Lawrey, 1986; Romagni 

and Dayan, 2002; Rundel, 1978), and shows various 

new possible applications for currently more 

than a thousand known lichen substances. 

The Lichens: Lichenized Fungi 

A lichen is a stable, ecologically obligate, selfsupporting 

mutualism between an exhabitant 

fungus (the mycobiont) and one or more inhabitant, 

extracellulary located unicellular or filamentous 

photoautotrophic partners (the photobiont: 

alga or cyanobacterium) (after Hawksworth 

and Honegger, 1994). Lichen thalli are complex 

ecosystems rather than organisms (Farrar, 1976; 

0939 – 5075/2010/0300 – 0157 $ 06.00 © 2010 Verlag der Zeitschrift für Naturforschung, Tübingen · http://www.znaturforsch.com · D

158 K. Molnár and E. Farkas · Biological Activities of Lichen Substances 

Lumbsch, 1998). According to recent estimations, 

lichens comprise about 18 500 species (Boustie 

and Grube, 2005; Feuerer and Hawksworth, 2007; 

Kirk et al., 2008). Since 1983, the name of a lichen 

refers to its mycobiont (Voss et al., 1983). Names 

of lichens in this paper follow the online database 

www.indexfungorum.org, the names originally 

used in the cited papers are in brackets. 

The fungal partners are mostly (98%) Ascomycota 

(Gilbert, 2000; Honegger, 1991) and the others 

belong to the Basidiomycota and anamorphic 

fungi. Approximately 21% of all fungi are able to 

act as a mycobiont (Honegger, 1991), thus lichens 

form the largest mutualistic group among fungi. 

Only 40 genera are involved as photosynthetic 

partners in lichen formation: 25 algae and 15 cyanobacteria 

(Kirk et al., 2008). The photobionts in 

approximately 98% of lichens are not known at 

the species level (Honegger, 2001). 

Lichenized fungi occur in a wide range of 

habitats: from arctic to tropical regions, from the 

plains to the highest mountains (Müller, 2001), 

and from aquatic to xeric conditions. Lichens 

can be found on or within rocks, on soil, on tree 

trunks and shrubs, on the surface of living leaves, 

on animal carapaces, and on any stationary, undisturbed 

man-made surface such as wood, leather, 

bone, glass, metal, concrete, mortar, brick, rubber, 

and plastic (Brightman and Seaward, 1977; 

Seaward, 2008). Lisická (2008) reported 18 lichen 

species on an acrylic-coated aluminum roof. Most 

lichens are terrestrial, but a few species occur in 

freshwater streams and others in marine intertidal 

zones (Nash, 2008). Lichens are able to survive 

in extreme environmental conditions; they can 

adapt to extreme temperatures, drought, inundation, 

salinity, high concentrations of air pollutants, 

and nutrient-poor, highly nitrified environments 

(Nash, 2008), and they are the first colonizers of 

terrestrial habitats (pioneers). In addition, both 

fungal and algal cells in the lichen thallus are 

known for their ability to survive in space (Sancho 

et al., 2007). Interactions between the symbiotic 

partners partially explain this spectacular success 

of lichens in unusual environments (Bačkor 

and Fahselt, 2008). Nevertheless, many lichens are 

very sensitive to various air pollutants, especially 

nitrogen-, sulfur- and heavy metal-based compounds; 

therefore they are widely used as bioindicators 

(Fernández-Salegui et al., 2007; Glavich 

and Geiser, 2008; Gries, 1996; Sheppard et al., 

2007 – only a few of many studies). 

The Lichen Substances: Secondary Metabolic 

Products 

Lichens produce a great variety of secondary 

metabolites, and most of them are unique to 

lichen-forming fungi. These chemically diverse 

(aliphatic and aromatic) lichen substances have 

relatively low molecular weight (Türk et al., 

2003). They are produced by the mycobiont (Elix, 

1996; Huneck, 1999), and accumulate in the cortex 

(such as atranorin, parietin, usnic acid, fungal 

melanins) or in the medullary layer (such as physodic 

acid, physodalic acid, protocetraric acid) as 

extracellular tiny crystals on the outer surfaces of 

the hyphae (Figs. 1, 2). The photobiont might also 

have an influence on the secondary metabolism of 

the mycobiont (Brunauer et al., 2007; Yamamoto 

et al., 1993; Yoshimura et al., 1994). 

Approximately 1050 secondary compounds 

have been identified to date (Stocker-Wörgötter, 

2008). This number is much higher than that 

found in previous literature sources (e.g., Culberson 

and Elix, 1989; Elix, 1996; Elix and Stocker- 

Wörgötter, 2008; Galun and Shomer-Ilan, 1988; 

Huneck, 1999; Huneck and Yoshimura, 1996; 

Lumbsch, 1998). The large increase is due to the 

fact that, previously, only “natural” substances oc- 

Fig. 1. Cross-section of the stratified foliose thallus of 

Umbilicaria mammulata. (Micrograph by K. Molnár.)

K. Molnár and E. Farkas · Biological Activities of Lichen Substances 159 

Fig. 2. Cross-section of the foliose thallus of Hypogymnia 

physodes. Hyphae are covered by the extracellular 

crystals of secondary metabolites. (SEM micrograph by 

K. Bóka and K. Molnár.) 

curring in intact lichen thalli were counted, but 

now, substances identified from cultures are also 

being included. Mycobionts grown without their 

photobionts synthesize specific secondary lichen 

compounds under certain conditions (Culberson 

and Armaleo, 1992; Fazio et al., 2007; Hager et al., 

2008; Mattsson, 1994; Stocker-Wörgötter and Elix, 

2002), but can also produce substances that are 

different from the metabolites found in symbiosis 

(Brunauer et al., 2007; Yoshimura et al., 1994). 

Each lichen mycobiont prefers specially adapted 

culture conditions (such as nutrient medium, 

added sugars or polyols, pH, temperature, light, 

stress) to produce the specific secondary metabolites 

(Hager et al., 2008). Similarly, lichen “tissue” 

cultures, in many cases, can produce secondary 

substances (Yamamoto et al., 1985, 1993), but the 

chemistry is usually different from the chemosyndrome 

of the corresponding natural lichen thalli 

(Yamamoto et al., 1993). Lichenized Basidiomycota 

do not contain lichen substances (Lumbsch, 

1998). 

Lichen products are restricted to specific areas 

of the thallus (Feige and Lumbsch, 1995; Lawrey, 

1995; Nybakken and Gauslaa, 2007), which correlate 

with the different functions of lichen metabolites. 

These patterns are consistent within certain 

taxonomic units (Lawrey, 1995). Hyvärinen 

et al. (2000) reported that the concentrations of 

secondary compounds in the foliose lichens Hypogymnia 

physodes, Vulpicida pinastri, and Xanthoria 

parietina are higher in sexual (apothecia of 

X. parietina) and asexual (soredia of H. physodes 

and V. pinastri) reproductive structures than in the 

vegetative parts of the thallus. This pattern is concordant 

with the optimal defense theory (ODT), 

which states that the structures most important 

for fitness should be chemically better defended. 

Fluorescence microscopy is used to determine 

the location of fluorescent substances in lichen 

thalli (Kauppi and Verseghy-Patay, 1990). Scanning 

electron microscopy (SEM) and laser microprobe 

mass spectrometry (LMMS), together with 

fluorescence microscopy and transmission electron 

microscopy (TEM), have also been used to 

locate compounds (Elix, 1996; Elix and Stocker- 

Wörgötter, 2008). Additionally, FT-Raman spectroscopy 

is a non-destructive analytical method 

used to identify lichen substances spatially in the 

intact lichen thallus (Edwards et al., 2005). Lichens 

may contain substantial amounts of secondary 

metabolites, usually between 0.1 – 10% of the 

dry weight, but sometimes up to 30% (Galun and 

Shomer-Ilan, 1988; Solhaug et al., 2009; Stocker- 

Wörgötter, 2008). 

The distribution patterns of secondary metabolites 

are usually taxon-specific and, therefore, 

have been widely used in lichen taxonomy and 

systematics (Carlin, 1987; W. L. Culberson, 1969b; 

Fehrer et al., 2008; Hawksworth, 1976; Nelsen 

and Gargas, 2008; Nordin et al., 2007; Nylander, 

1866; Piercey-Normore, 2007; Schmitt and Lumbsch, 

2004). However, it has been shown that the 

production of lichen compounds can be homoplasious 

and, therefore, similarities in secondary 

chemistry may not necessarily indicate close 

phylogenetic relationships (Nelsen and Gargas, 

2008). The production of secondary compounds is 

genetically controlled (Culberson and W. L. Culberson, 

2001), and in some instances is correlated 

with morphology and geography in individuals at 

the species and genus levels (Egan, 1986; Zhou et 

al., 2006). 

Asahina and Shibata (1954) published a classification 

of about 80 lichen substances based on 

their chemical structures and biosynthetic pathways. 

This system was modified from time to 

time, as more was known about lichen chemistry 

through improved analytical methods. Lichen 

substances were reclassified by Culberson and 

Elix (1989) according to their biosynthetic origins 

and chemical structural features. Most secondary


lichen metabolites are derived from the acetylpolymalonyl 

pathway (including the polyketide 

pathway), while others originate from the mevalonic 

acid and shikimic acid pathways. 

The Development of Analytical Methods (and 

their Application in Lichenology) 

Nylander (1866) was the first lichenologist to 

use chemistry for taxonomical purposes. He detected 

the presence of various lichen substances 

by color spot tests. In the early 20th century, Zopf 

(1907) and Hesse (1912) described numerous lichen 

compounds, mostly without their structural 

characterization, as organic chemistry was in its 

infancy (Shibata, 2000). Asahina developed the 

microcrystallization technique to identify lichen 

metabolites (Asahina, 1936 – 1940). This simple 

and rapid technique allowed lichenologists to 

identify the major constituents in hundreds of 

lichen species, but it was not useful for detecting 

minor components and analyzing mixtures of 

lichen substances. In 1952, Wachtmeister introduced 

paper chromatography for the separation 

and characterization of lichen substances. Mitsuno 

(1953) explained the relationship between 

the chemical structures of lichen compounds and 

their paper chromatographic Rf values. Since paper 

chromatography could not always separate 

individual compounds, Ramaut (1963a, b) began 

using thin layer chromatography (TLC) with 

Pastuska’s solvent phase for depsides and depsidones. 

According to Lumbsch (1998), the vast majority 

of lichen secondary metabolites, especially 

substances which are unique to lichens, belong to 

these two groups. 

TLC has been used to study specific groups of 

lichen products (Bendz et al., 1965, 1966, 1967; 

Santesson, 1965, 1967a, b). Different authors used 

different solvent systems and chromatographic 

conditions, making it impossible to compare their 

results. This problem was solved when a standardized 

method was developed by Chicita F. Culberson 

and Hör-Dur Kristinsson in 1970. They 

introduced Rf classes, which depend only on the 

relative order of spots, and which are more reliably 

constant. This standardized method has 

been used for routine analyses of lichen products 

in chemotaxonomic and phytochemical studies, 

with various updates over time (Culberson, 

1972b, 1974; Culberson and Johnson, 1976, 1982; 

Culberson et al., 1981). Later the use of high-performance 

thin layer chromatography (HPTLC) in 

screening lichen substances was developed (Arup 

et al., 1993). HPTLC is more sensitive, allows the 

running of more samples in a shorter period of 

time, and requires smaller amounts of solvent. Because 

of its simplicity, this technique has become 

the most widely used microchemical method for 

identifying lichen substances (Fig. 3). 

The first use of high-performance liquid chromatography 

(HPLC) on crude lichen extracts was 

tried by Culberson (1972a), because most of the 

secondary natural products of lichens have low 

volatility and low thermal stability, and thus gas 

chromatography is not able to analyze them. She 

used normal-phase silica columns and isocratic 

elution with mobile phases of mixtures of hexane, 

isopropyl alcohol and acetic acid. Reversephase 

HPLC was first used for the separation 

of orcinol and β-orcinol depsides and depsidones 

on a C18 column and with a water/methanol/ 

acetic acid mobile phase (Culberson and W. L. 

Culberson, 1978a; W. L. Culberson and Culberson, 

1978b). 

Although these isocratic methods yielded excellent 

results for the separation and identifica- 

Fig. 3. Lichen substances on an HPTLC plate developed 

in solvent system B (cyclohexane/methyl tert-butyl 

ether/formic acid, 6.5:5:1) after being treated with sulfuric 

acid (according to Arup et al., 1993). A, atranorin 

(control); Z, zeorin (control); N, norstictic acid (control); 

P, physodic acid; O, oxyphysodic (= 3-hydroxyphysodic) 

and physodalic acids; Pr, protocetraric acid. (Scanned 

image.)


Fig. 4. HPLC chromatogram of the acetone extract of Hypogymnia physodes (collected on the mountain Látóhegy, 

Budapest, Hungary, collection no. 208/a) at 245 nm. Peaks: a, acetone; b, benzoic acid (internal standard); c, 

protocetraric acid; d, 3-hydroxyphysodic acid; e, physodalic acid; f, 2’-O-methylphysodic acid; g, physodic acid; h, 

atranorin; i, chloroatranorin; j, bis-(2-ethylhexyl)-phthalate (internal standard). 

tion of lichen substances, gradient elution is more 

effective for HPLC analysis of crude lichen extracts, 

which frequently contain compounds of 

wide-ranging hydrophobicities (Culberson and 

Elix, 1989). Gradient elution was introduced in 

lichenology by Strack et al. (1979), who separated 

13 phenolic lichen products, including examples of 

depsides, depsidones, dibenzofurans and pulvinic 

acid derivatives, using an RP-8 column with a 70- 

min linear gradient from water containing 2% 

acetic acid (solvent A) to 100% methanol (solvent 

B). Huovinen (1987) developed a standard 

HPLC method for the identification and accurate 

quantification of aromatic lichen compounds on 

three different reverse-phase columns (RP-8, RP- 

18 and RP-phenyl) using gradient elution with 

methanol and orthophosphoric acid, as well as 

two internal standards: benzoic acid (low retention 

time) and bis-(2-ethyl-hexyl)-phthalate (high 

retention time) (Fig. 4). Retention indices (R.I.) 

in relation to the internal standards were defined, 

which are more consistent markers than retention 

times. Later the standard method was improved 

by Feige et al. (1993), using benzoic acid and solorinic 

acid [more hydrophobic compound than bis- 

(2-ethyl-hexyl)-phthalate] as internal standards, 

making the method suitable for the identification 

of lichen extracts containing chloroxanthones or 

long-chain depsides as well. 

The use of 1 H and 13 C NMR spectroscopy, mass 

spectrometry and X-ray crystal analysis in structural 

elucidation have also increased the number 

of known lichen metabolites (Culberson and Elix, 

1989). 

The Significance of Lichen Substances 

Secondary metabolites are not absolutely essential 

for the survival and growth of lichens 

(Bentley, 1999), nevertheless, their study has revealed 

many possible advantages. We know more 

about these substances through experimental 

studies, but the functions of these compounds in 

the lichen symbioses are still poorly understood 

(Hager et al., 2008). They may impact biotic and 

abiotic interactions of lichens with their environment. 

They may help to protect the thalli against 

herbivores, pathogens, competitors and external 

abiotic factors, such as high UV irradiation. Many 

of them exhibit multiple biological activities, such 

as the dibenzofuran usnic acid (e.g., antimicrobial 

and larvicidal effects, anticancer activities, known 

also for its UV absorption) (Fig. 5). When we analyze 

the biological activities of lichen substances, 

we must consider and observe their role in natural 

processes, but also study their role in special 

circumstances seldom occurring in nature, e.g., 

in experimental situations and with their use as 

medicines in humans or animals. 

Fig. 5. Chemical structure of usnic acid.


Structurally closely related metabolites often 

have essentially different biological actions. Hager 

et al. (2008) reported that barbatic and diffractaic 

acids, which differ in only one functional 

unit, have diverging biological effects. Barbatic 

acid (extracted from a metabolite-forming Heterodea 

muelleri mycobiont culture) strongly inhibits 

the growth of Trebouxia jamesii (the photobiont 

in H. muelleri) and slows down the mitosis rate 

of the alga at a concentration comparable to the 

quantity found in the lichen thallus (in nature). It 

can cause cell death in higher concentrations. At 

the same time, diffractaic acid (from a mycobiont 

culture, as before) has no effect on algal growth 

at all. On the basis of this result, barbatic acid 

may regulate algal growth and mitosis in the lichen 

thalli. 

Antioxidant Activity 

Free radicals (reactive oxygen species, such as 

the hydroxyl radical, superoxide anion, and hydrogen 

peroxide, and reactive nitrogen species, such 

as nitric oxide) play an important role in many 

chemical processes in the cells, but they are also 

associated with unwanted side effects, causing cell 

damage. They attack proteins and nucleic acids, as 

well as unsaturated fatty acids in cell membranes. 

Food deterioration, aging processes and several 

human chronic diseases, such as Alzheimer’s disease, 

atherosclerosis, emphysema, hemochromatosis, 

many forms of cancer (for example, melanoma), 

Parkinson’s disease, and schizophrenia, may 

be related to free radicals. Oxidative stress occurs 

also in lichen thalli, and secondary compounds afford 

protection against free radicals generated by 

UV light (Marante et al., 2003). 

The damaging effects of free radicals can be 

ameliorated by free radical scavengers and chain 

reaction terminators – enzymes such as superoxide 

dismutase, catalase, glutathione peroxidase, 

and glutathione reductase, as well as antioxidants 

such as glutathione, polyphenols (lignins, flavonoids), 

carotenoids, melanins, and vitamins E and 

C. 

Since synthetic antioxidants are often carcinogenic, 

finding natural substitutes is of great interest. 

Lichens have been found to contain a variety 

of secondary lichen substances with strong antioxidant 

activity. These are substances which have 

high ability to scavenge toxic free radicals due 

their phenolic groups. Hidalgo et al. (1994) reported 

the antioxidant activity of some depsides, such 

as atranorin (isolated from Placopsis sp.) and divaricatic 

acid (isolated from Protousnea malacea), 

and depsidones, such as pannarin (isolated from 

Psoroma pallidum) and 1’-chloropannarin (isolated 

from Erioderma chilense). All of these secondary 

compounds inhibited rat brain homogenate 

auto-oxidation and β-carotene oxidation, and 

depsidones were found to be the most effective. 

Russo et al. (2008) found that both sphaerophorin 

(depside) and pannarin (depsidone) inhibited superoxide 

anion formation in vitro, pannarin being 

more efficient, confirming Hidalgo et al. (1994). 

A methanol extract of Lobaria pulmonaria reduced 

the oxidative stress induced by indomethacin 

in the stomachs of rats, increasing the levels 

of superoxide dismutase and glutathione peroxidase 

(Karakus et al., 2009). Similarly, usnic acid 

was shown to be a gastroprotective compound, 

since it reduced oxidative damage and inhibited 

neutrophil infiltration in indomethacin-induced 

gastric ulcers in rats (Odabasoglu et al., 2006). 

Methanol extracts of Dolichousnea longissima 

(as Usnea longissima) and Lobaria pulmonaria 

have been shown to have significant antioxidant 

effects in vitro (Odabasoglu et al., 2004). According 

to Luo et al. (2009), the extreme conditions 

in Antarctica (such as low temperature, drought, 

winter darkness, high UV-B and solar irradiation) 

increase oxidative stress, consequently, antarctic 

lichens contain larger amounts of antioxidant 

substances and have higher antioxidant activity 

than tropical or temperate lichens. An acetone 

extract of Umbilicaria antarctica was found to 

be the most effective antioxidant in free radical 

and superoxide anion scavenging, as well as in reducing 

power assays among tested lichen species 

collected from King George Island, Antarctica. 

Lecanoric acid was identified as the main active 

compound. Methanol-water extracts of five lichens 

(Caloplaca regalis, Caloplaca sp., Lecanora 

sp., Ramalina terebrata, Stereocaulon alpinum) 

from Antarctica were screened for their antioxidant 

effects by Bhattarai et al. (2008), who found 

varying antioxidant success against the stable free 

radical diphenylpicrylhydrazyl (DPPH) on a TLC 

plate. 

All of these studies show that lichens and lichen 

substances might be novel sources of natural 

antioxidants.


Effect on Metal Homeostasis and Pollution 

Tolerance 

Lichen secondary metabolites are sensitive 

to heavy metal accumulation and might play a 

general role in metal homeostasis and pollution 

tolerance. Their sensitivity to heavy metals is species-specific. 

Remarkable changes in the levels of secondary 

compounds were found in Hypogymnia physodes 

thalli transplanted to areas polluted with heavy 

metals and acidic inorganic sulfur compounds 

(Białonska and Dayan, 2005). For example, the 

levels of atranorin, physodic acid and hydroxyphysodic 

acid were significantly decreased in 

thalli transplanted to the vicinity of a chemical 

plant producing chromium, phosphorous and sulfur 

compounds. In contrast, the level of physodalic 

acid was significantly increased, suggesting 

that this compound might be effective against 

pollution stress. The present authors have found 

similar results with the analyses of thalli growing 

naturally under various environmental conditions 

and pollution levels (Molnár and Farkas, manuscript 

under preparation). Hauck and Huneck 

(2007a) demonstrated the ion-specific increase or 

decrease of heavy metal adsorption at cation exchange 

sites (hydroxy groups) on cellulose filters 

coated with four lichen substances produced by 

Hypogymnia physodes (atranorin, physodic acid, 

physodalic acid and protocetraric acid). They 

used this model system to imitate lichen cell walls, 

which contain many hydroxy and carboxy groups 

as binding sites for metal cations. The alkali metal 

ion Na + , the alkaline earth metal ions Ca 2+ and 

Mg 2+ , and the transition metal ions Cu 2+ , Fe 2+ , 

Fe 3+ and Mn 2+ were studied. Lichen compounds 

significantly inhibited the adsorption of Na + , Ca 2+ , 

Mg 2+ , Cu 2+ and Mn 2+ , whereas they increased the 

adsorption of Fe 3+ . The level of Fe 2+ was not affected. 

The depsidone physodalic acid was found 

to be the most effective. 

Hauck and Huneck (2007b) also used cellulose 

filter strips to simulate cell wall surfaces. 

The depsidone fumarprotocetraric acid, the main 

lichen compound in Lecanora conizaeoides, has 

been shown to reduce Mn 2+ adsorption at cation 

exchange sites in vitro. This capability of fumarprotocetraric 

acid may be a key factor in the high 

Mn tolerance of this lichen species. 

Similar results have been found by Hauck 

(2008) using lichen thalli instead of an artificial 

system. The intracellular uptake of Cu 2+ and Mn 2+ 

was significantly lower in intact Hypogymnia 

physodes thalli containing a set of seven lichen 

metabolites compared to lichens treated with acetone. 

The intracellular uptake of Fe 2+ and Zn 2+ 

was not affected by the lichen substances. These 

impacts are consistent with the ecology of Hypogymnia 

physodes, i.e., Cu 2+ and Mn 2+ might be 

toxic in ambient concentrations on acidic bark 

(the preferred substrate of H. physodes), but Fe 2+ 

and Zn 2+ have never been found to limit the survival 

of this species. 

The dibenzofuran usnic acid and the depside 

divaricatic acid were both found to significantly 

increase the intracellular uptake of Cu 2+ in Evernia 

mesomorpha and in Ramalina menziesii (usnic 

acid only) originating from nutrient-poor habitats 

(Hauck et al., 2009). At the same time, the intracellular 

uptake of Mn 2+ was reduced. Since Cu 2+ 

is one of the rarest micronutrients in acidic tree 

bark and Mn 2+ often reaches toxic concentration, 

the influence of the compounds facilitates the survival 

of the two lichen species. 

These results show that lichen metabolites control 

metal homeostasis in lichens by promoting 

the uptake of certain metal cations, reducing the 

adsorption of others, thereby enhancing the tolerance 

of lichens to heavy metals in polluted areas. 

Photoprotection 

Lichens use a number of strategies to protect 

the light-sensitive algal symbionts against high 

levels of light and the damaging effects of UV radiation, 

mainly the xanthophyll cycle in the algal 

thylakoid membranes, as well as light screening 

and UV-B protection by lichen compounds. 

The light-screening theory was formulated by 

Ertl (1951), who found that cortical lichen compounds 

increase the opacity of the upper cortex, 

and thus decrease high incident irradiance reaching 

the algal layer. 

Light-screening pigments (such as parietin, 

usnic acid, vulpinic acid) regulate the solar irradiance 

reaching the algal layer (Galloway, 1993; 

Rao and LeBlanc, 1965; Rundel, 1978; Solhaug 

and Gauslaa, 1996) by absorbing much of the 

incident light and thus protecting the photosynthetic 

partner from intense radiation (Rao and 

LeBlanc, 1965). 

UV-B light inhibits photosynthesis and damages 

DNA. Several lichen secondary metabolites


(including atranorin, calycin, pinastric acid, pulvinic 

acid, rhizocarpic acid, usnic acid, vulpinic 

acid) have strong UV absorption abilities and 

might function as filters for excessive UV-B irradiation 

(Galloway, 1993; Rundel, 1978; Solhaug 

and Gauslaa, 1996). UV-B light might be essential 

for the synthesis of UV-B absorbing pigments 

(Nybakken and Julkunen-Tiitto, 2006; Nybakken 

et al., 2004). Rao and LeBlanc reported (1965) that 

the fluorescence spectrum of the cortical depside 

atranorin coincides with the absorption spectrum 

of algal chlorophyll; therefore, the light emitted 

by atranorin can be used in photosynthesis. 

Allelopathy 

Lichen secondary metabolites can function as 

allelopathic agents (called allelochemicals), i.e., 

they may affect the development and growth of 

neighboring lichens, mosses and vascular plants, 

as well as microorganisms (Kershaw, 1985; Lawrey, 

1986, 1995; Macías et al., 2007; Romagni et al., 

2004; Rundel, 1978). Allelopathic compounds are 

released into the environment and might influence 

other organisms’ photosynthesis, respiration, 

transpiration, protein and nucleic acid synthesis, 

ion membrane transport, and permeability (Chou, 

2006; Macías et al., 2007). 

Culberson et al. (1977b) reported that Lepraria 

sp. had a non-random distribution on two morphologically 

similar but chemically very different 

Xanthoparmelia species, which were growing 

together. The lichenicolous Lepraria sp. occurred 

commonly on 73% of the thalli of Xanthoparmelia 

verruculifera (as Parmelia verruculifera) examined. 

In contrast, only 13% of Xanthoparmelia 

loxodes (as Parmelia loxodes) specimens served as 

a host for the same species of Lepraria. The lichen 

substances presumably had allelopathic effects 

on Lepraria, and the secondary metabolites of X. 

loxodes were more detrimental to the growth of 

Lepraria. Whiton and Lawrey (1984) found that 

vulpinic and evernic acids severely inhibited ascospore 

germination of the crustose lichens Graphis 

scripta and Caloplaca citrina. Atranorin had 

an inhibitory effect only on C. citrina, completely 

eliminating its spore germination. Neither species 

was affected by stictic acid. Spore germination of 

Cladonia cristatella was also inhibited by vulpinic 

acid, but not by evernic and stictic acids (Whiton 

and Lawrey, 1982). 

Competition occurs between lichen thalli for 

space and light on a variety of substrates, and 

plays important roles in determining the structure 

of lichen communities and the distribution of 

individual species (Armstrong and Welch, 2007). 

Lichen secondary chemistry might play a role in 

this competition (Armstrong and Welch, 2007). 

Populations of mosses and lichens frequently 

occur together on rocks, soil, and trees, and they 

compete for light, substrate, nutrients, and water 

(Lawrey, 1977). Lichen substances also have inhibitory 

effects against other cryptogams in overlapping 

niches, such as mosses, and might significantly 

influence the competitive interactions in 

cryptogam communities. In the Great Smoky 

Mountains of the eastern United States, Heilman 

and Sharp (1963) observed that the lichen 

Thelotrema petractoides (as Ocellularia subtilis) 

was inhibiting and overgrowing a colony of Frullania 

eboracensis on the bark of Aesculus octandra. 

Similarly, the saxicolous lichen Lecidea albocaerulescens 

inhibited a community of bryophytes 

on greywacke boulders (including Anomodon attenuatus, 

Hedwigia ciliata, Porella platyphylla, and 

Sematophyllum sp.). The 4-O-methylated depsides 

evernic and squamatic acids retarded spore 

germination and protonemal growth of three 

common moss species occurring with the lichens: 

Ceratodon purpureus, Funaria hygrometrica and 

Mnium cuspidatum (Lawrey, 1977). 

Lichens have also long been known to inhibit 

or greatly retard the growth of higher plants (Pyatt, 

1967). Cladonia stellaris (as C. alpestris) and C. 

rangiferina, two common species in boreal forests, 

have been shown to have allelopathic effects on 

jack pine (Pinus banksiana) and white spruce (Picea 

glauca) (Fisher, 1979). Lichen mulch containing 

both species significantly reduced the growth 

as well as N and P concentrations of both seedlings 

and transplants of these coniferous trees. Compared 

to control plants, the roots of the seedlings 

treated with lichen mulch were longer, but less 

massive, and have significantly less mycorrhizae. 

Marante et al. (2003) reported that twelve lichen 

substances identified in “Letharal,” the phenolic 

fraction of Lethariella canariensis, showed allelopathic 

activity against the seeds of common garden 

plants, and inhibited the germination process 

of cabbage, lettuce, pepper, and tomato. It was 

also demonstrated that rainwater carries the lichen 

compounds into the soil by lixiviation.


Lichen substances were found to inhibit mycorrhizal 

fungi and their plant hosts (Fisher, 1979; 

Lawrey, 1995; Rundel, 1978). Henningsson and 

Lundström (1970) stated that the epiphytic lichen 

Hypogymnia physodes had a fungistatic effect on 

various wood-decaying fungi, and in this way lichens 

can protect their substrates from decay. 

Antimicrobial Activity 

Lichens produce antibiotic secondary metabolites 

that provide defense against most of the 

pathogens in nature. Several examples (from the 

species indicated) are described below. 

Atranorin (from Physcia aipolia), fumarprotocetraric 

acid (from Cladonia furcata), gyrophoric 

acid (from Umbilicaria polyphylla), lecanoric 

acid (from Ochrolechia androgyna), physodic 

acid (from Hypogymnia physodes), protocetraric 

acid [from Flavoparmelia caperata (as Parmelia 

caperata)], stictic acid [from Xanthoparmelia 

conspersa (as Parmelia conspersa)] and usnic acid 

(from Flavoparmelia caperata) showed relatively 

strong antimicrobial effects against six bacteria 

and ten fungi, among which were human, animal 

and plant pathogens, mycotoxin producers and 

food-spoilage organisms (Ranković and Mišić, 

2008; Ranković et al., 2008). Usnic acid was found 

to be the strongest antimicrobial agent (comparable 

to streptomycin), and physodic and stictic 

acids the weakest. 

According to Schmeda-Hirschmann et al. 

(2008), dichloromethane and methanol extracts of 

Protousnea poeppigii had strong antifungal effects 

against the fungal pathogens Microsporum gypseum, 

Trichophyton mentagrophytes and T. rubrum. 

The extracts were also active against the yeasts 

Candida albicans, C. tropicalis, Saccharomyces 

cerevisiae and the filamentous fungi Aspergillus 

niger, A. flavus and A. fumigatus, but with much 

higher strength. Isodivaricatic acid, divaricatinic 

acid and usnic acid, the main lichen metabolites 

in Protousnea poeppigii, also displayed antifungal 

action against Microsporum gypseum, Trichophyton 

mentagrophytes and T. rubrum, usnic acid 

being less active. In the same assay, extracts of 

Usnea florida also showed strong antifungal properties. 

Methanol extracts of five lichens from Antarctica 

(Caloplaca regalis, Caloplaca sp., Lecanora sp., 

Ramalina terebrata, Stereocaulon alpinum) exhibited 

target-specific antibacterial activity, especially 

strong against Gram-positive bacteria, compared 

to previously described lichen compounds (Paudel 

et al., 2008). 

Whiton and Lawrey (1982) reported that ascospore 

germination of Sordaria fimicola was significantly 

inhibited by evernic and vulpinic acids. 

Aqueous, ethanol and ethyl acetate extracts of 

Alectoria sarmentosa and Cladonia rangiferina 

were found to have moderate antifungal action 

against different species of fungi, including human 

pathogens (Ranković and Mišić, 2007), ethanol 

extracts showing the highest activity. 

Halama and Van Haluwin (2004) reported that 

acetone extracts of Evernia prunastri and Hypogymnia 

physodes showed a strong inhibitory effect 

on the growth of some plant pathogenic fungi, 

i.e., Phytophthora infestans, Pythium ultimum, 

and Ustilago maydis. 

Since microorganisms have developed resistance 

to many antibiotics, pharmacologists need to 

pursue new sources for antimicrobial agents. All 

these results suggest that lichens and their metabolites 

yield significant new bioactive substances 

for the treatment of various diseases caused by 

microorganisms. 

Lichen compounds can provide protection 

against lichenicolous fungi, but some of these 

fungi are tolerant of the lichen metabolites. Lawrey 

(2000) showed that Fusarium sp., a lichen 

inhabitant, enzymatically degrades lecanoric 

acid in Punctelia subflava (as Punctelia rudecta), 

thus permiting Nectriopsis parmeliae (as Nectria 

parmeliae), an obligate lichenicolous fungus, to 

colonize the lichen thallus. 

Antiherbivore and Insecticidal Activity 

Lichens are grazed by herbivores, e.g., insects, 

mites, snails, slugs, lepidopteran larvae, caribou, 

and reindeer. However, herbivory on lichens 

seems to be rare, presumably due to their low 

nutritional quality, specific structural features 

(for example, the gelatinous sheath in Collemataceae, 

thick cortex), and the production of defense 

compounds (Lawrey, 1986; Rundel, 1978). Zukal 

(1895) first proposed that secondary compounds 

might protect lichens from herbivory, and this 

idea was later supported by strong experimental 

evidence (e.g., Asplund and Gauslaa, 2007, 2008; 

Gauslaa, 2005; Nimis and Skert, 2006; Pöykkö et 

al., 2005). Lichen secondary compounds also play 

an important role in the food preference of her-


bivores (Baur et al., 1994; Pöykkö and Hyvärinen, 

2003; Reutimann and Scheidegger, 1987). 

Both enantiomers of usnic acid, a widespread 

cortical dibenzofuran, exhibited strong larvicidal 

activity against the third and fourth instar larvae 

of the house mosquito (Culex pipiens), and larval 

mortality was dose-dependent (Cetin et al., 2008). 

Antifeedant activity and acute toxicity (injected 

into the larval haemolymph) of (–)- and (+)-usnic 

acids and vulpinic acid against the polyphagous 

larvae of the herbivorous insect Spodoptera littoralis 

have also been reported (Emmerich et al., 

1993). All three lichen compounds caused severe 

growth retardation at concentrations comparable 

or even below those present in lichens, as well as 

increased the larval period (delayed the pupation) 

in a dose-dependent manner. 

It is known that natural plant-derived products 

have a less detrimental impact on the environment 

than synthetic chemicals, and thus lichen 

substances could be good candidates for new pesticides 

(Cetin et al., 2008; Dayan and Romagni, 

2001; Fahselt, 1994; Romagni and Dayan, 2002). 

Harmful effects of lichen substances on vertebrate 

herbivores have also been reported. Poisoning 

and subsequent death of an estimated 

400 – 500 elk (Cervus canadensis) was reported in 

Wyoming during the winter of 2004 (Cook et al., 

2007; Dailey et al., 2008), putatively due to ingestion 

of the lichen Xanthoparmelia chlorochroa. 

This lichen was found in the area and in the rumen 

of elks as well (Cook et al., 2007). Clinical 

signs were red urine, ataxia, and muscular weakness, 

which rapidly progressed to recumbency 

and myodegradation. To identify the toxin, ewes 

were dosed with (+)-usnic acid extracted from X. 

chlorochroa. It was shown that high doses caused 

selective skeletal muscle damage in these animals. 

Since the toxic dose was very high, other lichen 

substance(s), in addition to (+)-usnic acid, may 

have interacted to cause the poisoning in elks. 

This sort of poisoning takes place periodically in 

western North America, when elks have to leave 

their regular winter habitats and move to lower 

elevations due to harsh weather conditions (Elix 

and Stocker-Wörgötter, 2008). 

Effects on Human Organisms 

Cytotoxic, antitumor, and antiviral activity 

Many lichen secondary metabolites exhibit cytotoxic 

and antiviral properties and could be potential 

sources of pharmaceutically useful chemicals. 

The cytotoxic activity of eight lichens [Cladonia 

convoluta, C. rangiformis, Evernia prunastri, Flavoparmelia 

caperata (as Parmelia caperata), Parmotrema 

perlatum (as Parmelia perlata), Platismatia 

glauca, Ramalina cuspidata, Usnea rubicunda] 

on two murine and four human cancer cell lines 

was reported by Bézivin et al. (2003). The lichens 

were extracted with three solvents (n-hexane, 

diethyl ether, and methanol). Only three of the 

24 extracts were not cytotoxic against any of the 

tested cell lines (diethyl ether extracts of E. prunastri 

and P. glauca, and methanolic extract of U. 

rubicunda). The n-hexane extracts were usually 

the most active and methanolic fractions were 

generally less selective. C. convoluta (diethyl ether 

fraction), C. rangiformis (diethyl ether fraction), 

and F. caperata (n-hexane fraction) were the most 

active species. Diethyl ether and methanolic extracts 

of C. convoluta and C. rangiformis showed 

the highest selectivity on various cell lines. 

(+)-Usnic acid was found to be a strong hepatotoxic 

agent against monogastric murine hepatocytes, 

due to its ability to uncouple and inhibit 

the electron transport chain in mitochondria 

and induce oxidative stress in cells (Han et al., 

2004). The (–)-enantiomer of usnic acid (isolated 

from Cladonia convoluta) induced apoptotic 

cell death in murine lymphocytic leukemia cells 

and was moderately cytotoxic to various cancer 

cell lines, such as murine Lewis lung carcinoma, 

human chronic myelogenous leukemia, human 

brain metastasis of a prostate carcinoma, human 

breast adenocarcinoma and human glioblastoma 

(Bézivin et al., 2004). Usnic acid also decreased 

proliferation of human breast cancer cells and human 

lung cancer cells without any DNA damage 

(Mayer et al., 2005). Finding cancer therapies that 

do not have DNA-damaging effects and that do 

not cause the development of secondary malignancies 

later in life, is of great interest. Accordingly, 

usnic acid may represent a novel source for 

a natural non-genotoxic anticancer drug (chemotherapeutic 

agent). 

Russo et al. (2008) reported that the depside 

sphaerophorin (isolated from Sphaerophorus globosus) 

and the depsidone pannarin [isolated from 

Psoroma pholidotoides (as Psoroma reticulatum), 

P. pulchrum, and P. pallidum] inhibited the growth 

of M14 human melanoma cells, triggering apoptotic 

cell death. The anticancer activities of these


lichen metabolites are promising in the treatment 

of this aggressive, therapy-resistant skin tumor. 

An ethyl acetate-soluble fraction (ET4) of the 

crude methanolic extract of Ramalina farinacea 

was found to be a broad-spectrum antiviral agent 

against RNA (respiratory syncytal virus and HIV- 

1) and DNA (adenovirus and herpes simplex virus 

type 1) viruses (Esimone et al., 2009). Anti-HIV 

effects of ET4 target both entry and post-entry 

stages in the viral replication cycle. 

Usnic acid (isolated from the aposymbiotic mycobionts 

of Ramalina celastri) exhibited specific 

antiviral activity against the Junin virus (Arenaviridae), 

which is the agent of Argentine hemorrhagic 

fever in humans, as well as against Tacaribe 

virus, a non-pathogenic arenavirus (Fazio et 

al., 2007). Parietin (isolated from the aposymbiotic 

mycobionts of Teloschistes chrysophthalmus) 

showed virucidal effects against the same viruses. 

Allergy to lichen substances 

Lichens and lichen substances can be contact 

allergens in people who are susceptible. They can 

cause occupational allergic contact dermatitis in 

forestry and horticultural workers (“woodcutter’s 

eczema”), and in lichen harvesters, as well as 

cause non-occupational allergic dermatitis during 

all kinds of outdoor activities, such as cutting and 

handling firewood, picking berries, hunting, and 

using cosmetics (perfumes, after-shave lotions, 

deodorants, and sunscreen products) that contain 

lichen metabolites (Aalto-Korte et al., 2005); see 

data for 11 lichen substances that cause allergic 

reactions (Table I). 

Contact dermatitis seems to be immunologically 

specific, inasmuch as the person is sensitive 

to only a single lichen compound or to a group 

of structurally similar compounds (Mitchell and 

Champion, 1965). Various skin and respiratory 

symptoms have been observed, such as erythema, 

itching, scaling, contact urticaria, rhinitis, and asthma 

(Aalto-Korte et al., 2005; Mitchell and Champion, 

1965). Several lichen compounds (such as 

atranorin and stictic acid) are able to photosensitize 

human skin causing photocontact dermatitis, 

where the exposure to sunlight leads to an aggravation 

of symptoms (Elix and Stocker-Wörgötter, 

2008; Thune and Solberg, 1980). 

Candidates for antipyretic and analgesic drugs 

Some lichen substances have been shown to relieve 

pain effectively or reduce fever and inflammation 

in various mammals, and it is reasonable 

to assume that these compounds also could be 

effective in humans. Vijayakumar et al. (2000) reported 

that (+)-usnic acid, isolated from Roccella 

montagnei, showed significant, dose-dependent 

anti-inflammatory activity in rats, reducing carrageenin-induced 

paw edema. Diffractaic and usnic 

acids have an analgesic effect in mice in vitro 

(Okuyama et al., 1995), and usnic acid also is an 

antipyretic against lipopolysaccharide-induced fever. 

Table I. Literature sources mentioning data for 11 lichen substances responsible for allergic reactions to lichens. 

Lichen substance Reference 

Atranorin Dahlquist and Fregert, 1980; Thune and Solberg, 1980; Gonçalo et al., 1988; 

Hausen et al., 1993; Stinchi et al., 1997; Aalto-Korte et al., 2005; Cabanillas et al., 2006 

Diffractaic acid Thune and Solberg, 1980 

Evernic acid Dahlquist and Fregert, 1980; Thune and Solberg, 1980; Gonçalo et al., 1988; 

Hausen et al., 1993; Aalto-Korte et al., 2005; Cabanillas et al., 2006 

Fumarprotocetraric acid Dahlquist and Fregert, 1980; Thune and Solberg, 1980; Gonçalo et al., 1988; 

Hausen et al., 1993 

Lobaric acid Thune and Solberg, 1980 

Perlatolic acid Hausen et al., 1993 

Physodalic acid Thune, 1977; Thune and Solberg, 1980 

Physodic acid Thune, 1977; Thune and Solberg, 1980 

Salazinic acid Thune and Solberg, 1980 

Stictic acid Thune and Solberg, 1980; Hausen et al., 1993 

Usnic acid Mitchell and Champion, 1965; Thune and Solberg, 1980; Gonçalo et al., 1988; 

Hausen et al., 1993; Stinchi et al., 1997; Aalto-Korte et al., 2005; Cabanillas et al., 2006


Conclusions 

More than 1000 secondary products have been 

identified to date in lichens, and new compounds 

will certainly be found from poorly studied or 

newly discovered lichens, especially from the 

under-collected tropics. Here we have shown that 

lichen secondary substances exhibit a huge array 

of remarkable biological activities, and many of 

them have important ecological roles. Some of the 

activities already mentioned (e.g., photoprotection, 

reaction to pollution) should be thoroughly 

studied. Furthermore, the properties of lichen 

substances make them possible pharmaceuticals. 

At the same time, we have to be aware that lichens 

are slow-growing ecosystems, and exploitation 

of their secondary products could threaten 

their survival. However, improved culture methods 

and varied growing conditions can positively 

influence secondary metabolite production in 

aposymbiotically grown mycobionts (Stocker- 

Wörgötter, 2008) and in cultured lichens (Behera 

et al., 2009), without having to harvest and put at 

risk the extinction of natural communities. 

Acknowledgements 

Our sincere thanks are due to Chicita F. Culberson 

for her invaluable help with the literature 

and useful comments on the manuscript. The authors 

are grateful to Molly McMullen for revision 

of the text. We would like to thank Lucyna Śliwa, 

Suzanne Joneson, and Ester Gaya for their helpful 

comments on an earlier version of the manuscript. 

K. M. is also thankful to François Lutzoni 

for his support during the completion of her thesis 

on Hypogymnia physodes. Special thanks are 

due to Duke University Libraries for providing 

the literature. The preparation of this paper was 

supported also by the Hungarian Scientific Research 

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