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Determination of phytochemical contents by LC/QTOF/MS and evaluation of in-vitro biological activities of 2 Peltigera lichens from Bursa

Abstract

Lichens are symbiotic associations of algae and fungi. They are edible as food and have been used in traditional medicine for years. It is aimed to screen Peltigera praetextata (Flörke ex Sommerf.) Zopfand and Peltigera elisabethae Gyeln. phytochemically by LC/QTOF/MS and according to the constituents to evaluate the antioxidant, tyrosinase inhibitory, and antibacterial activities. In total 54 of metabolites detected by LC/QTOF/MS were common in both species. According to LC/QTOF/MS scanning results, alkaloids, iridoid glycosides, phenolics, cyanogenetic glycosides, and terpenic structures were detected. DPPH, ABTS, superoxide radical scavenging activities, and metal chelating capacity IC50 values were 84.55, 9.349; 51.27, 9.127; 95.01, 58.65 and 20.57, 70.08 µg/mL., respectively. The CUPRAC reducing power was determined as 4.69 and 9.57 TEACCUPRAC, respectively. Tyrosinase inhibitor activity were found to be 86.95 and 196.7 µg/mL. Both lichens did not show antimicrobial effects. As a result of the antioxidant and tyrosinase inhibitor activities it was seen that their activities were significant and further in vivo studies could be carried out on this lichens.

Key words
Antioxidant; LC/QTOF/MS; Lichen phenolics; Peltigera elisabethae Gyeln; Peltigera praetextata (Flörke ex Sommerf.); Tyrosinase inhibitor

INTRODUCTION

Lichens are symbiotic associations that spread almost worldwide with twenty-five thousand taxa. Lichens are formed due to the physiological and morphological associations of algae and fungi. They can occur as long as there is sufficient moisture. With the lichen acids they secrete and they can even decompose the stones and form humus soil. Therefore, they are of great importance as pionir organisms. According to the morphological forms of the thallus; they are divided into crustose, foliose, and fruticose lichens. According to their anatomical structures, they are divided into the homeomeric type and heteromeric type (Ivanova & Ivanov 2009IVANOVA D & IVANOV D. 2009. Ethnobotanical use of lichens: Lichens for food review. Scr Sci Med 41(1): 11- 16. http://dx.doi.org/10.14748/ssm.v41i1.456.
https://doi.org/10.14748/ssm.v41i1.456...
, Emsen 2019EMSEN B. 2019. The antioxidant antigenotoxic potential of Peltigera canina and Umblicaria nylanderiana based on their phenolic profile. Farmacia 67(5): 912-921. https://doi.org/10.31925/farmacia.2019.5.24.
https://doi.org/10.31925/farmacia.2019.5...
). Lichens also take place in ethnobotanical uses. Because it is rich in calcium and iron, it is consumed as food after boiling. Peltigera, like other lichens, is a genus often used in traditional medicine. It is known that they are used especially for skin disorders, wound healing, gynecological diseases, respiratory tract and digestive regulators (Rankovic & Kosanic 2015RANKOVIC B & KOSANIC M. 2015. Lichens as potential source of bioactive secondary metabolites. Lichen Secondary Metabolites. London: Springer.). They are very rich in secondary metabolites. They consist of aliphatic and aromatic compounds. Depsids, tridepsids and depsidones, dibenzofuran, cromon, and quinone derivatives are lichen secondary metabolites (Huneck & Yoshimura 1996HUNECK S & YOSHİMURA I. 1996. Identification of Lichen Substances (1). Verlag Berlin Heidelberg: Springer.). Lichen secondary metabolites have antioxidant, anticancer, antibiotic, antimicrobial, enzyme inhibitor, antiviral, and anti-genotoxic effects (Huneck & Yoshimura 1996HUNECK S & YOSHİMURA I. 1996. Identification of Lichen Substances (1). Verlag Berlin Heidelberg: Springer., Rankovic & Kosanic 2015RANKOVIC B & KOSANIC M. 2015. Lichens as potential source of bioactive secondary metabolites. Lichen Secondary Metabolites. London: Springer., Sivas 2019SIVAS HZ. 2019. Antigenotoxic effect of some lichen metabolites. Lichen Secondary Metabolites. Rankovic, B. London: Springer.).

In nature, most lichens are edible and provide nutrition for microflora and mammals. It is known that it is often consumed as a human food item. P. rufescens and P. apthosa lichens are used as flour. In addition to being consumed as food (flour etc.), their use in traditional medicine is also known. For example, it is known that P. canina is used in treating rabies among people, and it is known that it got its name from there. In addition, traditionally, Peltigera type lichens have been shown to have anti-inflammatory and antibacterial uses in jaundice (Rankovic & Kosanic 2015RANKOVIC B & KOSANIC M. 2015. Lichens as potential source of bioactive secondary metabolites. Lichen Secondary Metabolites. London: Springer., Sivas 2019SIVAS HZ. 2019. Antigenotoxic effect of some lichen metabolites. Lichen Secondary Metabolites. Rankovic, B. London: Springer.).

Today, lichens are one of the new focuses of attention, and the lack of studies about them has attracted our attention to contribute to the literature.

In this study, phytochemical screening of P. praetextata (PP) and P. elisabethae (PE) was performed with LC/QTOF/MS, and they were investigated for their antioxidant, antimicrobial, and tyrosinase inhibitor activities.

List of abbreviations

ABTS: 2,2’-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt CUPRAC: Copper(II) Ion Reducing Capacity

DPPH: 2,2’-diphenyl-1-picrylhydrazil

HPLC: High Performance Liquid Chromatography NBT; Nitroblue tetrazolium

PE: P. Elisabethea

PP: P. praetextata

TFC: Total flavonoid content TPC: Total phenolic content

Chemicals and reagents

Methanol (Sigma), Ethanol (Sigma), LC grade Formic acid (Sigma), LC grade acetonitrile (Sigma), Folin Ciocalteu reagent (Merck), Na2CO3 (Merck), Gallic acid (Sigma), AlCl3 (Merck), Quercetin (Sigma), DPPH (Sigma), DMSO (Sigma), ABTS(Sigma), Neocuproine(Sigma), Copper (II) chloride(Sigma), EDTA(Sigma), NBT (Nitroblue tetrazolium) (Sigma), Riboflavin(Sigma), Phosphate buffer(Sigma), Ascorbic acid(Sigma), Ferrozine(Sigma), L-Dopa(Sigma), Kojic acid (Sigma), tyrosinase enzyme(Sigma).

MATERIALS AND METHODS

Lichen collection, determination, drying, and extraction

PP and PE species distributed in Bursa province were investigated. The collected lichen samples were identified with the help of identification keys in various flora books (Wirth 1995WIRTH W. 1995. Die Flechten Baden-Württembergs. Stutttgart, DEU: Ulmer., Brodo et al. 2001BRODO IM, SHARNOFF SDVE & SHARNOFF S. 2001. Lichens of North America. New Haven and London, USA: Yale University Press., Smith et al. 2009SMITH CW, APTROOT A, COPPINS BJ, FLETCHER A, GILBERT OL, JAMES PW & WOLSELEY PA. 2009. The Lichens of Great Britain and Ireland. London, UK: Natural History Museum Publications in association with The British Lichen Society.).

Prof. Dr. Şule Öztürk and Assoc. Prof. Dr. Seyhan Oran identified them. The collected samples, especially the very moist ones of the species that spread on the soil, were kept in laboratory conditions for four days and dried as a pre-treatment proocedure. The thalli of the collected lichen samples were carefully cleaned from foreign materials such as moss, soil, and tree bark in a Leica MZ 6 stereomicroscope with dissection forceps, placed in paper bags, and stored in the refrigerator until the laboratory experiments began.

Lichen extraction

For the extraction process, 1 gram of powdered lichen thallus was extracted three times with methanol in an ultrasonic bath (Bandolin Sonorex) (25 °C) for 30 minutes. After each filtering, the solvent was removed in the rotavapor (Buchi) at 35-40 °C, and the collected extracts were combined and then stored at + 4 °C (Adams et al. 1993ADAMS WW, DEMMİG-ADAMS W & LANGE OL. 1993. Carotenoid composition and metabolism in green and blue-green algal lichens in the field. Oecologica 94: 576- 584. https://doi.org/10.1007/bf00566975.
https://doi.org/10.1007/bf00566975...
, Zagoskina et al. 2013ZAGOSKINA NV, NIKOLAEVA TN, LAPSHIN PV, ZAVARZIN AA & ZAVARZINA AG. 2013. Water-soluble phenolic compounds in lichens. Microbiol 82(4): 445-452. http://dx.doi.org/10.1134/S0026261713030132.
https://doi.org/10.1134/S002626171303013...
).

Qualification of compounds by LC/QTOF/MS

Chromatographic separation was carried out using an HPLC Agilent 1260 Infinity series (Agilent Technologies, Santa Clara, CA, USA) equipped with a binary pump, and an online degasser, an autosampler, and a Poroshell 120 EC-C18 (3.0X100 mm, particle size) 2.7 µm) (Agilent Technologies). A mobile phase system composed of water with 0.1% formic acid (A) and acetonitrile (B) was used in a gradient elution mode as follows: 0–0.5 min, 5% B; 0.5–7 min, 25% B; 7–16 min, 50% B; 16–23 min, 75% B; 23–30 min, 95% B; 30–40 min, 5% B for equilibration of the column. The column temperature was maintained at 35 °C. The injection volume was 10 µL, and the flow rate was 0.4 mL/min.

Ionization of chromatographic eluates was performed using an Agilent 6550 iFunnel high-resolution Accurate-Mass QTOF-MS, equipped with an Agilent Dual Jet Stream, and electrospray ionization (Dual AJS ESI) interface operating in negative ion was used at the following conditions: drying gas flow, 14.0 L/min; nebulizer pressure, 35 psi; gas drying temperature, 290 °C; sheath gas temperature, 400 °C; sheath gas flow, nitrogen at 14 L/min and nozzle voltage 1000 V. All spectra were collected in targeted MS/MS mode from m/z 50 to 1800 scan range for inducing MS/MS data collection. The collision energy was 20 eV during analysis.

Integration and data evaluation were performed using MassHunter Workstation software, and the MassHunter METLIN and the Accurate Mass Personal Compound Database and Library (METLIN_AM_PCDL) were used to detect phenolic compounds. (Agilent Technologies, Santa Clara, CA, USA). Agilent Dual Jet Stream electrospray ionization (Dual AJS ESI) interface operating in negative and positive ions.

Determination of total phenol and flavonoid content

Determination of Total Phenolic Content (TPC)

The analysis was carried out according to the Folin-Ciocalteu method. 2.8 mL of deionized water was added to 100 µL of extract (concentration range of 5µg/mL-1mg/mL). Then, 2 mL of 2% Na2CO3 and 0.1 mL of 50% Folin reagent were added, mixed, and incubated at 25 ˚C for 30 minutes in the dark. Gallic acid calibration curve and total phenolic content of lichens were determined by measuring absorbance against water at 750 nm by Optima SP-3000 Nano Spectrophotometer (Cheung et al. 2003CHEUNG LM, CHEUNG PCK & OOI VEC. 2003. Antioxidant activity and total phenolics of edible mushroom extracts. Food Chem 81: 249-255. https://doi.org/10.1016/S0308-8146(02)00419-3.
https://doi.org/10.1016/S0308-8146(02)00...
, Kanipandian et al. 2014KANIPANDIAN N, KANNAN S, RAMESH R, SUBRAMANIAN P & THIRUMURUGAN R. 2014. Characterization, antioxidant and cytotoxic evaluation of green synthesized silver nanoparticles using Cleistanthus collinus extract as surface modifier. Mater Res Bull 49: 494-502. https://doi.org/10.1016/j.materresbull.2013.09.016.
https://doi.org/10.1016/j.materresbull.2...
). Results are expressed as mg gallic acid/g extract.

Determination of Total Flavonoid Content (TFC)

1.5 mL of 95% ethanol was added to 500 µL of extract solution (concentration range of 5µg/ml- 1mg/ml). After, 100 µL of AlCl3 and 2.8 mL of deionized water were added to it and left to incubate for 40 minutes. The absorbance was measured against ethanol at 415 nm by Optima SP-3000 Nano Spectrophotometer. Quercetin was used as a standard (Cheung et al. 2003CHEUNG LM, CHEUNG PCK & OOI VEC. 2003. Antioxidant activity and total phenolics of edible mushroom extracts. Food Chem 81: 249-255. https://doi.org/10.1016/S0308-8146(02)00419-3.
https://doi.org/10.1016/S0308-8146(02)00...
, Kanipandian et al. 2014KANIPANDIAN N, KANNAN S, RAMESH R, SUBRAMANIAN P & THIRUMURUGAN R. 2014. Characterization, antioxidant and cytotoxic evaluation of green synthesized silver nanoparticles using Cleistanthus collinus extract as surface modifier. Mater Res Bull 49: 494-502. https://doi.org/10.1016/j.materresbull.2013.09.016.
https://doi.org/10.1016/j.materresbull.2...
). The results are reported as mg quercetin/g extract.

In vitro Antioxidant Activity Studies

DPPH (2,2’-diphenyl-1-picrylhydrazil) Radical Scavenging Activity

The method described by Esmaeli et al. was used with little modification (Esmaeili & Khadadadi 2002). DPPH solution prepared in DMSO was added to the tested samples in a certain concentration range (10 μg/mL – 1 mg/mL) and then incubated in the dark for 30 minutes. The absorbance of the resulting mixture was then measured at 517 nm by Optima SP-3000 Nano Spectrophotometer and methanol used as a blank. α-tocopherol was used as a standard. Results are given as IC50 (µg/mL) (GraphPad Prism 5).

ABTS+ Radical Cation Scavenging Activity

It was evaluated by modifying the ABTS+ decolorization method of Rer et al. (1999)RER A, PELLEGRINI N, PROTEGGENTE A, PANNOLA A, YONG M & RICE-EVANS C. 1999. Antioxidant activity applying an improved ABTS radical cotion decolorization assay. Free Rad Biol Med 26: 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3.
https://doi.org/10.1016/S0891-5849(98)00...
. In this method, ABTS radical was prepared by reacting stock ABTS solution with potassium persulfate (Rer et al. 1999RER A, PELLEGRINI N, PROTEGGENTE A, PANNOLA A, YONG M & RICE-EVANS C. 1999. Antioxidant activity applying an improved ABTS radical cotion decolorization assay. Free Rad Biol Med 26: 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3.
https://doi.org/10.1016/S0891-5849(98)00...
). It was diluted with ethanol until an absorbance of 0.750 at 734 nm was obtained. Then, 0.1 mL of extract (concentration range of 20 μg/mL-1 mg/mL) and 4 mL of ethanol were added to 1 mL of diluted ABTS solution, and its absorbance at 734 nm at 6 minutes was read by Optima SP-3000 Nano Spectrophotometer. α-tocopherol was used as a standard. Results are given as IC50 (µg/mL) (GraphPad Prism 5) Ethanol was used as a blank.

CUPRAC (Copper(II) Ion Reducing Capacity) Method

The copper(II) reducing power was determined according to the method of Apak et al. (2004)APAK R, GÜÇLÜ K, ÖZYÜREK M & KARADEMİR SE. 2004. A novel total antioxidant capacity index for dietarypolyphenols, vitamin C and E, using their cupric ion reducing capability in the presence of neocuproine: The CUPRAC method. J Agric Food Chem 52: 7970-7981https://doi.org/10.1021/jf048741x.
https://doi.org/10.1021/jf048741x....
. After the mixture of neocuprine and Copper (II) was prepared at pH 7, sample solution (5 μg/mL-1 mg/mL) was added and incubated for 30 minutes. The absorbance against the blank methanol at 450 nm was measured by Optima SP-3000 Nano Spectrophotometer. Trolox solution was used as standard. Results are given as TEACCUPRAC.

Superoxide Radical Scavenging Activity

It was carried out according to the research conducted by Patel et al. (2010)PATEL A, PATEL A & PATEL NM. 2010. Determination of polyphenols and free radical scavenging activity of Tephrosia pupurea linn leaves. Pharmacognosy Res 2: 152-158. https://doi.org/10.4103/0974- 8490.65509.
https://doi.org/10.4103/0974- 8490.65509...
. 10 µL of extracts and standards at different concentrations, 15 µL 12 mM EDTA, 10 µl 0,1 mg/mL NBT (nitro blue tetrazolium), 5 µL 0.2 mg/mL riboflavin, and 160 µL 0.067mM Potassium Phosphate Buffer (pH 7.4) are placed in a Thermo Scientific- Varioscan Flash microplate reader and incubated at fluorescence light for 5 minutes. Ascorbic Acid was used as a standard. The absorbance at 560 nm was then measured by Optima SP-3000 Nano Spectrophotometer. Results are given as IC50 (µg/mL) (GraphPad Prism 5) (Patel et al. 2010PATEL A, PATEL A & PATEL NM. 2010. Determination of polyphenols and free radical scavenging activity of Tephrosia pupurea linn leaves. Pharmacognosy Res 2: 152-158. https://doi.org/10.4103/0974- 8490.65509.
https://doi.org/10.4103/0974- 8490.65509...
).

Metal Chelating Activity

The metal chelating activity was modified using the Fe (II)-Ferrozine method. In this method, 5 mL of test solutions at concentrations of 31.25-500 µg/mL were added to 100 µL of 2 mM FeCl2 and incubated for 30 minutes at room temperature in the dark. At the end of the period, 200 µL of 5 mM ferrozine solution was added and incubated again for 10 minutes in the dark and at room temperature. EDTA was used as a standard. Its absorbance at 562 nm was measured by Optima SP-3000 Nano Spectrophotometer. Results are given as IC50 (µg/mL) (GraphPad Prism 5) (Decker, 1997DECKER E. 1997. Phenolics: prooxidants or antioxidants. Nutr Rev 55: 396-398. https://doi.org/10.1111/j.1753-4887.1997.tb01580.x.
https://doi.org/10.1111/j.1753-4887.1997...
).

In vitro Tyrosinase Inhibitor Activity

The method of Masuda et al. (2005)MASUDA T, YAMASHITA D, TAKEDA Y & YONEMORI S. 2005. Screening for tyrosinase inhibitors among extracts of seashore plants and identification of potent inhibitors from Garcinia subelliptica. Biosci Biotechnol Biochem 69: 197-201. https://doi.org/10.1271/bbb.69.197.
https://doi.org/10.1271/bbb.69.197...
was modified. 110 µL phosphate buffer (0.01 M, pH: 6,8), 10 µL plant extract (different concentrations), and 20 µL tyrosinase solution (200 unit/mL) were mixed. After 10 minutes of incubation at 37 °C, the reaction was initiated by adding 20 µL of L-Dopa and allowed to incubate at 37 °C for 10 minutes. The absorbance was measured at 475 nm by Thermo Scientific Varioskan Flash Microplate Reader. Kojic Acid was used as a standard. Results are given as IC50 (µg/mL) (GraphPad Prism 5) (Masuda et al. 2005MASUDA T, YAMASHITA D, TAKEDA Y & YONEMORI S. 2005. Screening for tyrosinase inhibitors among extracts of seashore plants and identification of potent inhibitors from Garcinia subelliptica. Biosci Biotechnol Biochem 69: 197-201. https://doi.org/10.1271/bbb.69.197.
https://doi.org/10.1271/bbb.69.197...
).

Antimicrobial Activity

In antimicrobial tests, Gram-positive bacteria Bacillus cereus (ATCC 7064), Enterococcus faecalis (ATCC 29212), Staphylococcus aureus (ATCC 6538-P), Gram-negative bacteria Escherichia coli (ATCC 25922), Klebsiella pneumoniae (ATCC 13883), Pseudomonas aeruginosa (ATCC 27853), and two yeast strains Candida albicans (ATCC 90028), Candida parapsilosis (ATCC 22019) were used.

Agar Well Diffusion Method

Fresh cultures of bacteria and standard yeast strains were adjusted to a 0.5 McFarland turbidity by suspending in physiological saline water and inoculated under aseptic conditions on cation-added Mueller Hinton Agar (MHA) and Sabouraud Dextrose Agar (SDA) plates respectively. 50 µl of the stock solutions (4mg/ml) of the extracts prepared in deionized and sterilized water were filled into the opened wells on the agar plates. The final extract loads were 200 µg in each well. Ciprofloxacin 5 µg and fluconazole 25 µg were used as positive controls. An evaluation was made by measuring the zone diameters seen at the end of 24-48 hours of incubation at 37 ºC (Korkak et al., 2022).

Microdilution Method

50 µL cation-added Mueller Hinton Broth (MHB) medium for yeasts, and Sabouraud Dextrose Broth (SDB) medium for yeasts were added to the wells in a sterile U-bottom microplate. Stock solutions of the extracts in water (4mg/mL) were distributed on the microplate with a concentration range of 2-2048 µg/mL. Microorganisms, whose fresh cultures prepared from the stock were suspended in physiological saline and adjusted to 0.5 McFarland turbidity, were diluted 1:100 with MHB and SDB media, then distributed in equal amounts to the wells. The first well without visible turbidity at the end of 24-48 hours of incubation was considered as minimum inhibitory concentration (MIC). Growth control and medium controls were also included. Ciprofloxacin and fluconazole were used as positive controls (Korkak et al., 2022).

Statistical analysis

All results are expressed as mean ± SD. One Way ANOVA test at a level of p < 0.05 in IBM SPSS (ver. 25). Were performed (Table V).

Table V
Statistical Analysis (One way ANOVA).

RESULTS AND DISCUSSION

As a result of the extractions, PE and PP extracts were obtained wtih a yield of 18.11% and 16.31% respectively. According to LC-QTOF-MS library scanning, a total of 441 items were identified (Supplemantary files-Tables), including both secondary and primary metabolites. All chromatograms are listed in Figure 1, 2, 3 and 4. Alkaloids, iridoid glycosides, phenolics, cyanogenetic glycosides, and terpenic compounds were determined as secondary metabolites. Xanthosine, C16 Sphinganine, Tortuosamine, Erythronolide B, Prosopinine, 14,19- Dihyroaspidospermatine, Tetradecylamine, Fenpiclonil, Eudesmin, n-Pentadecylamine, Triclofos, Gemfibrozil M1, 9-nonadecene, 1-Eicosene, Spermine derivates, Diisobutyl/diisononyl phthalate, Luteolin derivate, Nonoxynol-9 and Harderoporphyrin were biologically active compounds and detected in both PP and PE (Figure 1,2,3,4). According to the literature research (Table I), it was seen that these substances have antioxidant, tyrosinase inhibitor, and antimicrobial effects, and it was decided to screen the activities of the extracts based on this. TPC (Total phenolic content), TFC (Total flavonoid content) and in vitro antioxidant activities were evaluated and summarized (Tables II and III). It has been observed that the radical scavenging activities of PE, which has more TPC and TFC and contains more secondary metabolites known to be antioxidants, are much higher. Tyrosinase inhibitory activity results are summarized in Table IV. It was observed that activity of PP is higher than PE. This suggests that this may be due to the amount of tyrosinase inhibitor substances and synergistic effects in their content. There are a few studies on PE and PP. When they were evaluated, it was determined that PP had an antimutagenic effect (Nardemir et al. 2015NARDEMIR G, YANMIŞ D, ALPSOY L, GULLUCE M & AGAR G. 2015. Genotoxic, antigenotoxic and antioxidant properties of methanol extracts obtained from Peltigera horizontalis and Peltigera praetextata. Toxicol Indust Health 31(7): 602-613.). Its antimutagenicity is important as it supports the consumability of edible lichens. In another study involving both PP and PE, their antiproliferative effects were determined. In the same study it was also stated that PP does not contain secondary metabolites in contrast to our study (Munzi et al. 2014MUNZI S, TRIGGIANI D, CECCARELLI D, CLIMATI E, TIEZZI A & PISANI T. 2014. Antiproliferative activity of three lichen species belonging to the genus Peltigera. Plant Biosyst 148(1): 83-87.).

Figure 1
Negative ion mode LC/QTOF/MS Chromatogram of PE.
Figure 2
Negative ion mode LC/QTOF/MS Chromatogram of PP.
Figure 3
Positive ion mode LC/QTOF/MS Chromatogram of PE.
Figure 4
Positive ion mode LC/QTOF/MS Chromatogram of PP.
Table I
Compounds detected in PP and PE and biological activities in literature
Table II
TPC, TFC and in vitro antioxidant activity results.
Table III
CUPRAC slope values.
Table IV
Tyrosinase inhibitor activity results.

When the studies on the other species in Peltigera genus were examined, it was seen that acetone extract of P. horizontalis were effective as an antioxidant. Still, it was not found to have an antibacterial effect in 5 different strains. In this study, while antioxidant activity was observed in our species, antibacterial activity was not observed in similar strains. The DPPH scavenging activity of P. laciniata ethanol extract was given as percent inhibition (80%). It can be seen that it shows a very strong scavenging activity. Since our results are given as IC50 value in this study it cannot be compared exactly (Plaza et al. 2014PLAZA CM, DIAZ DE TORRES LE, LUCKING RK, VIZCAYA M & MEDINA GE. 2014. Antioxidant activity, total phenols and flavonoids of lichens from Venazuelan Andes. J Pharm Pharmacognosy Res 2(5): 138-147. https://doi.org/10.4067/s0716-97602012000400010.
https://doi.org/10.4067/s0716-9760201200...
). However we can indicate that the results are compatible. In a different study, DPPH radical scavenging and metal chelating activities of P. canina methanol extract were determined and expressed as IC50 value. These values were 42,37, and 50,33 mg/L, respectively (Emsen, 2019). Compared to our current research results, P. canina’s activity is between PP (84,55-20,57 µg/mL) and PE (9,349-70,08 µg/mL) in our research. A research with P. rufescens stated that it is effective as an antioxidant (Aydin & Turkez 2011AYDİN E & TURKEZ H. 2011. Effects of Lichenic extracts (Bryoria capillaris, Peltigera rufescens and Xanthoria elegans) on human blood cells: a cytogenetic and biochemical study. Fresenius Environ Bull 20: 2992- 2998.). Compared to our results, it is true that both of them have antioxidant effects. As a result of a study with Nepal mountain lichens, Peltigera sp. was ineffective against Bacillus subtilis and Staphillococcus aurens as our study. Again in the same study, the radical scavenging effects of DPPH and ABTS were examined, and their IC50 values were reported as 5.6 and 6.9 µg/mL, respectively, closer to PE in our study (Paudel et al. 2012PAUDEL B, BHATTARAI HD, PANDEY DP, HUR JS & HONG SG. 2012. Antioxidant, antibacterial activity and Brine shrimp toxicity test of some mountainous lichens from Nepal. Biol Res 45: 387-391. https://doi.org/10.4067/s0716-97602012000400010.
https://doi.org/10.4067/s0716-9760201200...
).

Enzyme inhibitory activities in lichens have been studied before, and interesting results were obtained. Of these, lichens showing tyrosinase inhibitory activity were Flavoparmelia caperata, Letharia vulpina, Cetraria juniperina, Parmotrema perlatum (Malaspina et al. 2020MALASPINA P ET AL. 2020. Depigmenting potential of lichen extracts evaluated by in vitro and in vivo tests. Peer J 8: e9150. https://doi.org/10.7717/ijfs.14098.
https://doi.org/10.7717/ijfs.14098...
), Hypogymnia physodes, Bulbothrix setschwanensis, Usnea species (Zhao et al., 2021), Cetraria islandica (Akbulut & Yildiz 2010AKBULUT G & YILDIZ A. 2010. An Overview to Lichens: The Nutrient Composition of Some Species. Kafkas Üniv Fen Bil Enst Derg 3(2): 79-86.) and Himantormia (Areche et al. 2022ARECHE C, PARRA JV, SEPULVEDA B, GALCIA-BELTRAN O & SIMIRGIOTIS MJ 2022. UHPLC-MS Metabolomic Fingerprinting, Antioxidant, and Enzyme Inhibition Activities of Himantormia lugubris from Antarctica. Metabolites 12: 560-581. https://doi.org/10.3390/metabo12060560.
https://doi.org/10.3390/metabo12060560...
) species. However, studies of tyrosinase inhibitory activity in Peltigera lichens have not been done before. Since many substances showing tyrosinase inhibitory activity were detected in our study, the activities of the extracts were examined and determined as 86.95 and 196.7 µg/mL (IC50) in PP and PE, respectively. Standart compound kojic acid’s inhibitory activity was 37,40 µg/mL (IC50) (Table IV). Compared to kojic acid, PP and PE’s IC50 values were found to be close and that indicated the strong tyrosinase inhibitor activity.

According to antibacterial and antifungal compounds C16 sphinganine, tetradecyl amine, diisobutyl phthalate, nonoxynol-9, erythronolide B, 14, 19- dihydroaspidospermatine, fenpiclonil, eudesmin, 1- eiocosene, 9- nonadecene, triclofoteolin and 8-hydroxyluciferol extracts, which are known to exist in both lichens, extracts antibacterial and antifungal effects were tested. They did not show activity against any of the strains. It was observed that similar results were obtained in antibacterial tests performed on Peltigera species before. It is thought that this may be due to the synergistic effects of different substances in the extract.

CONCLUSIONS

It has been determined that PP and PE lichens contain lichen phenolics, alkaloids, terpenic metabolites and flavonoids. They showed antioxidant and tyrosinase inhibitor activities, which are among the expected effects in line with the substances they contain. Although many substances with antibacterial and antifungal properties were detected, they were found to have no effect, suggesting that this result was due to the synergistic effect of the substances contained in it. It was determined that PP and PE have strong antioxidant and tyrosinase inhibitor activities and it was envisaged that further studies could be conducted. Peltigera lichens showed antioxidant and tyrosinase inhibitory activity in line with the secondary metabolites but showed no antimicrobial effect.

ACKNOWLEDGMENTS

The research was carried out with the support of Ege University BAP project no. 30782.

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Publication Dates

  • Publication in this collection
    14 June 2024
  • Date of issue
    2024

History

  • Received
    19 June 2023
  • Accepted
    03 Feb 2024
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