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Cladonia foliacea lichen thallus with usnic acid in upper cortex and fumarprotocetraric in lower medullary layer
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The terricolous species Cladonia foliacea (Cladoniaceae, lichenised Ascomycota) widely distributed in open, dry lowland steppe and rocky mountain grassland vegetation in Europe was chosen as a potential test organism for ecological experiments, since their thalli are producing cortical solar radiation-protective and UV screening pigment dibenzofura...
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... foliacea (Huds.) Willd. (Cladoniaceae, lichenised Ascomycota) ( Fig. 1) is a relatively frequent, terricolous, foliose lichen species in Hungary and widely distributed over Europe both in open, dry and sun-exposed habitats in lowland steppe and mountain grassland communities, also found in northern hemisphere temperate region in North America ( Smith et al. 2009, Wirth et al. 2013). The different LSM ...
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... temperate region in North America ( Smith et al. 2009, Wirth et al. 2013). The different LSM content of the cortex (KC+ pale yellow for usnic acid) and the medulla (Pd+ yellow to red for fumarprotocetraric acid) was already indicated by spot tests ( Hillmann and Grummann 1957). The thallus has a thickened upper cortex containing usnic acid (Fig. 1) as a protective compound against UV radiation and other effects (e.g. Cochietto et al. 2002, Yilmaz et al. 2004). The photosynthetic layer contains coccoid green alga photobiont (Asterochloris sp., Trebouxiaceae -cf. Moya et al. 2015. The yellowish white, white lower surface lobes are turning upwards when they are dry and reflecting ...
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... al. 2004). The photosynthetic layer contains coccoid green alga photobiont (Asterochloris sp., Trebouxiaceae -cf. Moya et al. 2015. The yellowish white, white lower surface lobes are turning upwards when they are dry and reflecting the strong solar irradiation near soil surface. The species also produces a depsidone, the fumarprotocetraric acid ( Fig. 1) here in the medullary layer. There is no lower cortical layer ...
Citations
... Different localization of LSMs may imply their different biological and ecological roles. Being a cortical compound, UA primarily protects the photosynthesizing algal partner and the fungal hyphae (Farkas et al. 2020a, b;Veres et al. 2022a, b), UA from C. foliacea also exerts a phytotoxic or even a herbicidal effect on nearby bryophytes (Giordano et al. 1999). Furthermore, UA also shows antimicrobial effects (Lauterwein et al. 1995), insecticidal potential (Emmerich et al. 1993) and antioxidant activity (Anar et al. 2016;Odabasoglu et al. 2006). ...
... Both UA and FA contents in Cladonia foliacea were comparable to those previously measured (Farkas et al. 2020a, b;Veres et al. 2022a, b. This is the first study using chiral chromatography to confirm the production of (-)-UA in C. foliacea collected in Hungary and nearby countries. ...
Lichen specific metabolites (LSMs) have interesting biological activities and quantitative variations may be present intraspecifically. For example, variations in medullary fumarprotocetraric acid (FA) and cortical usnic acid (UA) were observed in the lichen Cladonia foliacea, but the mechanism of variation is not well understood. The current study aimed to characterise the quantitative variation of FA and UA and to investigate the association between lichen metabolite content and ecological / biological variables. Fungal and algal trees were constructed using fungal (nrITS, RPB2) and algal (nrITS) loci, respectively. Using a chiral chromatographic method, the contents of (-)-UA were determined in 29 C. foliacea specimens and range from 6.88 to 34.27 mg/g dry wt. The FA contents were lower and varied from 1.44 to 9.87 mg/g dry wt. Although the fungal tree showed two well resolved clades, no significant differences of UA or FA contents were found between the two fungal clades. However, a significantly higher UA/FA ratio as well as a unique habitat were found to be associated with specimens which contained the alga Asterochloris lobophora than those specimens associated other Asterochloris algae. Taking all predictive variables into account (i.e. substrate type, elevation, collection season, photobiont identity), the multivariate data analysis indicated that photobiont identity explained most of the variance of LSM contents in C. foliacea. Thus future LSM biosynthetic studies should take the photobiont into consideration when dealing with intraspecific quantitative variation.
... Due to the photoprotective role by atranorin (Nguyen et al., 2021) and usnic acid (Farkas et al., 2019;Veres et al., 2022) in a lichen thallus, their use as compounds against excessive sun exposure in skin tanning cosmetics is included (Ara ujo et al., 2015;Loh ezic-Le D ev ehat et al., 2013). However, these compounds can cause allergy/photosensitisation (Ara ujo et al., 2015 and literature cited therein;Varol et al., 2015). ...
A meta-analysis of literature data with statistical analysis concerning the effect of lichen substances on the inhibition of 10 yeast species (Candida albicans, C. dubliniensis, C. glabrata, C. parapsilosis, C. sake, C. tropicalis, Colacogloea diffluens, Cryptococcus neoformans, Issatchenkia orientalis and Saccharomyces cerevisiae) is provided. Lichen extracts were obtained using 16 solvents from 100 epiphytic, 51 epigeic and 37 epilithic lichen species. The most studied lichen taxa at the generic level belonged to the family Parmeliaceae. 67 individual secondary metabolites belonging to 12 biochemical classes were subjected to experiments. The MIC was used most frequently. Candida albicans was the most commonly tested species; other fungal species remain relatively less or very poorly tested. Against C. albicans, a stronger antifungal potential is demonstrated by extracts from numerous lichen species, including Evernia prunastri, Hypotrachyna vexans, Pseudevernia furfur-acea, Ramalina pollinaria, R. polymorpha, Cladonia foliacea, C. pocillum, C. rangiformis and Umbilicaria cylin-drica, which generated secondary compounds such as atranorin, a-collatolic acid, ethyl everninate, lecanoric acid, methyl 2,6-dihydroxy-4-methylbenzoate, protolichesterinic acid, retigeric acid A and B, scrobiculin and usnic acid. The potential of the extracts and secondary metabolites makes it possible to replace several commercial antibiotics in the future, in particular clotrimazole and fenticonazole. For the purpose of future experiments, this review stresses the need to standardizse research methodology, especially for the simultaneous determination of MIC and IZ and, if possible, MFC. There is a need for greater use of water as a solvent to extract lichen substances as a safe and feasible method for phytopharmaceutical and cosmetic purposes. The conclusions drawn highlight the prospective use of lichen extracts and secondary metabolites against yeast in the medical, phytopharmaceutical and cosmetic fields and as preservatives.
... To explain the network collapse in the +BSC-H microcosms the authors considered reports on the strong inhibitory effect of C. rangiformis' secondary metabolites atranorin and usnic acid, specifically relating to instability over time, thermal and light liability, and the temporal changes in concentration (Farkas et al., 2020;Gheza et al., 2021) and reasoned as follows: Prior to the first rain event the crust survived inactive under extreme drought conditions for 2.5 months (including the summer period in the field and the conditioning phase). The first rainfall was adequate just to trigger the photosynthetic activity of the crust but not adequate enough to induce the leaching of the secondary metabolites, a fact that affected slightly the soil microbial community. ...
We assess the recovery of microbial networks underneath crust to repeated rainfall. Biological soil crusts (BSCs) are an important multi-trophic component of arid ecosystems in the Mediterranean region. In a mesocosm experiment , the authors investigated how the network of interactions among the members of the soil microbial communities in four types of soil sample responded when soils were exposed to two simulated extreme rain events. The four types of soil samples were: covered by Cladonia rangiformis and previously hydrated (+BSC+H), covered by C. rangiformis and dried (+BSC-H), uncovered and hydrated (-BSC+H), uncovered and dried (-BSC-H). Network analysis was based on the co-occurrence patterns of microbes; microbes were assessed by the phospholipid fatty acids analysis. The authors further explored the relations between networks' metrics and soil functions denoted by enzymatic activity and soil chemical variables. All networks exhibited Small world properties, moderate values of clustering coefficient and eigen centrality, indicating the lack of hub nodes. The networks in-BSC-H soils appeared coherent during the pre-rain phases and they became modular after rains, while those in +BSC-H soils kept their connectivity till the second rain but this then collapsed. The network metrics that were indicative of cohesive networks tended to be related to enzyme activity while those that characterized the loose networks were related to Ca, K, Mg, NH 4 + and organic N. In all mesocosms except for +BSC-H, networks' fragmentation after the second heavy rain was milder than after the first one, supporting the idea of community acclimatization. The response of microbial networks to heavy rains was characterized by the tendency to exhibit degradation-reconstruction phases. The network collapse in the crusted only mesocosms showed that the communities beneath crusts in arid areas were extremely vulnerable to recurring heavy rain events.
... The thallus exhibits a thickened upper cortex (Osyczka and Rola 2013) containing usnic acid (Fig. 1c) as a UV-protectant compound. Fumarprotocetraric acid (Fig. 1d) is also detected in the medullary and photosynthetic layer (Farkas et al. 2020b;Hillmann and Grummann 1957;Honegger 1986Honegger , 1997Honegger , 2012. No lower cortical layer is developed and the photobiont is Asterochloris sp., Trebouxiaceae (cf. ...
... After the first collection, the samples were cleaned from plant and moss particles and randomised within each locality (lowland and mountain samples). Then, acetone rinsing was carried out two times for half an hour (Farkas et al. 2020b). After the treatment, the acetone soaked and control samples were placed in the experimental area in National Botanical Garden (Vácrátót, Hungary, 47.705821°N, 19.229580°E) for a 3year experiment (Fig. 1e). ...
Terricolous lichens are abundant in semi-arid areas, where they are exposed to high irradiation. Photoprotection is essential for the algae as the photobiont provides the primer carbon source for both symbionts. The UV-protectant lichen metabolites and different quenching procedures of the alga ensure adequate photoprotection. Since the long-term effect of diminishing UV-protectant lichen metabolites is unknown, a major part of lichen secondary metabolites was removed from Cladonia foliacea thalli by acetone rinsing, and the lichens were then maintained under field conditions to investigate the effect on both symbionts for 3 years. Our aim was to determine if the decreased level of UV-protectant metabolites caused an elevated photoprotection in the algae and to reveal the dynamics of production of the metabolites. Photosynthetic activity and light protection were checked by chlorophyll a fluorescence kinetics measurements every 6 months. The concentrations of fumarprotocetraric and usnic acids were monitored by chromatographic methods. Our results proved that seasonality had a more pronounced effect than that of acetone treatment on the function of lichens over a long-term scale. Even after 3 years, the acetone-treated thalli contained half as much usnic acid as the control thalli, and the level of photoprotection remained unchanged in the algae. However, the amount of available humidity was a more critical limiting environmental factor than the amount of incoming irradiation affecting usnic acid production. The lichenicolous fungus Didymocyrtis cladoniicola became relatively more abundant in the acetone-treated samples than in the control samples, indicating a slight change caused by the treatment.
Supplementary information:
The online version contains supplementary material available at 10.1007/s11557-022-01831-y.
... In the hydrated state, the cortical transmittance (Dietz et al. 2000) and the production of light screening fungal metabolites increase (Solhaug et al. 2003). Similar results for C. foliacea were found by Farkas et al. (2020): the amount of usnic acid and fumarprotocetraric acid showed higher concentrates in winter than summer. The concentration of usnic acid in Cladina mitis was also significantly higher in autumn and winter (BeGora and Fahselt 2001). ...
In lichens, each symbiotic partner cooperates for the survival of the symbiotic association. The protection of the susceptible photosynthetic apparatus is essential for both participants. The mycobiont and photobiont contribute to the protection against the damaging effect of excess light by various mechanisms. The present study investigated the effect of seasonality and microhabitat exposure on photoprotection and photoacclimation in the photo- and the mycobiont of six lichen species with different thallus morphology in inland dune system in the Kiskunság region (Hungary) with shaded, more humid and exposed, drier dune sides. High-Performance Liquid Chromatography, spectrophotometry, chlorophyll a fluorescence kinetic technique were used, and micrometeorological data were collected. The four years data series revealed that the north-east-facing side was characterized by higher relative humidity and lower light intensities compared to the south-west-facing drier and more exposed sides. The south-west facing side was exposed to direct illumination 3–4 hours longer in winter and 1–2 hours shorter in summer than the north-east facing side of the dune, influencing the metabolism of sun and shade populations of various species. Because rapid desiccation caused short active periods of lichens during bright and drier seasons and on exposed microhabitats, the rapid, non-regulated non-photochemical quenching mechanisms in the photobiont had a significant role in protecting the photosynthetic system in the hydrated state. In dehydrated conditions, thalli were mainly defended by the solar screening metabolites produced by the mycobiont and curling during desiccation (also caused by the mycobiont). Furthermore, the efficacy of light use (higher chlorophyll and carotenoid concentration) increased because of short hydrated periods. Still, a lower level of received irradiation was appropriate for photosynthesis in dry seasons and on sun exposed habitats. In humid seasons and microhabitats, more extended active periods lead to increased photosynthesis and production of solar radiation protectant fungal metabolites, allowing a lower level of photoprotection in the form of regulated non-photochemical quenching by the photobiont. Interspecific differences were more pronounced than the intraspecific ones among seasons and microhabitat types.
... In terms of UV radiation, lichens have developed various photoprotect mechanisms such as screening, quenching, and repair mechanisms [13,14]. An important protective mechanism of lichens is the production of UV screening compounds, such as phenolic compounds (depsides, depsidones, diphenyl ethers), anthraquinones, xanthones, or shikimic acid derivatives (calycin, mycosporines, scytonemin) [15][16][17][18]. Compounds isolated from lichens have been suggested as potential UV blockers due to their absorption on the UV region and their antioxidant activity and photostability [19][20][21][22][23][24]. ...
Lichens are an excellent source for the discovery and development of new photoprotective compounds. However, investigation on their bioactivities remains limited, especially in Vietnam. In this study, six lichen extracts (Parmotrema poolii, P. sancti-angelii, P. tinctorum, Usnea baileyi, U. pulvinulata, U. undulata) and five isolated compounds from commonly distributed species P. tinctorum (methyl β-orcinol carboxylate (1), atranorin (2), lecanorol (3), salazinic acid (4), 1β-acetoxyhopan3β,22-diol (5)) have been screened in vitro for their photoprotective activity. The photoprotective potential was investigated by determination of their absolute (UV-PF, lc, UVA-PF) and relative indexes (SUI, ISP). The structures of isolated compounds were elucidated by spectroscopic methods and confirmed by X-ray diffraction. The results showed that P. poolii, P. sancti-angelii, P. tinctorum, U. baileyi, U. undulata, and compounds of methyl β-orcinol carboxylate (1) and salazinic acid (4) acted as strict UVB filters, and their photoprotective activities are comparable to that of the commercial UVB filter (4-methylbenzylidene camphor). Meanwhile, U. pulvinulata acted as a UVA booster. Compound (3) presented characteristics of a UVA filter, (2) protected well from both UVA and UVB while (5) exhibited a weak photoprotective activity. For the first time, this work successfully extracted several highly potential solar photoprotective compounds from Vietnam's lichens.
... The difference is explained by the high natural variation of the concentrations of LSMs in lichen thalli ranging from c. 0.1% to 10%(-30%) of their dry weight [17]. The larger necessary concentration of the crude extract is explained by the amount of the LSM present in the thallus [49]. ...
Since the long-term application of synthetic chemicals as insecticides and the chemotherapy of protozoal diseases have had various negative effects (non-target effects, resistance), research on less harmful biological products is underway. This review is focused on lichens with potential insecticidal and antiprotozoal activity. Literature sources (27) were surveyed from five bibliographic databases and analyzed according to the taxonomic group of the insect, the protozoal disease and the lichen, the type of bioactive compounds (including method of application and mount applied), and the potential bioactivity based on mortalities caused after 24 h of exposure on insects and on parasitic protozoa. Six species of protozoa and five species of mosquitoes, three kinds of larval stages of insects and three protozoa stages were tested. Insecticidal and antiprotozoal effects of crude extracts and seven lichen secondary metabolites (mostly usnic acid) of 32 lichen species were determined. Physiological and morphological changes on parasitic protozoa were observed. Mortality rates caused by LSMs on insect vectors closer to (or somewhat above) the WHO threshold were considered to be insecticides. The results are based on laboratory experiments; however, the efficacy of metabolites should be confirmed in the field and on non-human primates to control the insect vectors and human protozoal diseases transmitted by insects.
... According to the Farkas et al. research, the concentration of fumarprotocetraric acid of C. foliacea acetone extract varied between 2.26 and 5.81 mg g -1 in winter collected samples. The higher content of C. foliacea in our study may be due to the samples obtained from different countries, the time of collection, and extraction method (Farkas et al., 2020). DPPH • radical scavenging method is a rapid method for evaluating the free radical scavenging effect of extracts. ...
In traditional medicine, Cladonia lichens are used for several disorders like hypertension, headaches, dizziness, cough, and menstrual disorders. The study aimed to determine the biological activities of 70% methanol extracts of nine Cladonia species from Turkey. The chemical composition was analyzed via spectrophotometric and chromatographic (HPLC) techniques. DPPH● (1,1-diphenyl-2-picrylhydrazyl) and ABTS+● (2,2'-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) radical scavenging activities, inhibition of β-carotene/linoleic acid co-oxidation, and cytotoxicity on A549 and COLO205 cell lines were studied. Anti-inflammatory activity was assessed on the Raw 264.7 mouse macrophage cell line by determining nitric oxide (NO) levels. Among the studied Cladonia species Cladonia firma was found the most active extract in ABTS+● test system (2.58±0.07 mmol/L/Trolox) and also in the cytotoxicity and anti-inflammatory experiments. Cladonia pocillum, Cladonia rangiformis, and Cladonia foliaceae were also found to be active. Fumarprotocetraric acid amounts are between 1.89 -23.82 mg/gextract and fumarprotocetraric acid content did not show linearity with biological activities. It has been proved with this study that lichens traditionally used in treatment have as much biological activity as plants and can be evaluated in pharmaceuticals and cosmetics.
... Some of them show cytotoxic activity and are much studied for their pharmacological potential [17][18][19], but their ecological roles have been addressed more rarely. More investigated are allelopathic [44][45][46] and anti-herbivorous [47][48][49] effects, rarer are ecological studies that investigated their roles in photoprotection [50][51][52] and in regulating species' preferences for substrate pH [20][21][22]53]. ...
... Research has suggested photoprotection activity for usnic acid [52] and facilitation in exploiting low light intensities for atranorin [63]. This can explain their correlations with vascular plants which produce a thicker canopy than herbs and forbs, i.e., chamephytes and phanerophytes, which occur in mature stages of dry grasslands. ...
Terricolous lichen communities in lowlands occur especially in open dry habitats. Such communities are often dominated by species of the genus Cladonia, which are very variable in morphology, reproduction strategies, and secondary metabolites. In this work, we investigated traits-environment relationships considering vegetation dynamics, substrate pH, disturbance, and climate. A total of 122 plots were surveyed in 41 acidic dry grasslands in the western Po Plain (Northern Italy). Relationships between Cladonia traits and environmental variables were investigated by means of a model-based Fourth Corner Analysis. Thallus morphology and metabolites responded to vegetation dynamics, substrate pH, disturbance, and climate, whereas reproduction strategies responded only to vegetation dynamics. Traits' correlations with vegetation dynamics elucidate their colonization patterns in open dry habitats or suggest biotic interactions with bryo-phytes and vascular plants. In addition, correlations between metabolites and environmental factors support interpretations of their ecological roles. Our results also stress the importance of studying traits' relationships with climatic factors as an alert towards lichen reactions to climate change.
... Therefore, we can conclude that it is possible to apply C. foliacea as a test lichen for acetone rinsing experiments; however, the extraction efficiency of its lichen compounds needs to be quantified (cf. Farkas et al. 2020). Lichen species with coccoid green-algal (Trebouxia sp.) photobionts from sun-exposed habitats have wide ranges of tolerance, as has the investigated species containing a taxonomically related, Asterochloris sp. ...
Acetone rinsing tolerance of the lichen species Cladonia foliacea is considerable - Volume 52 Issue 4 - Edit Farkas, Bernadett Biró, Zsolt Csintalan, Katalin Veres
