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. 2019 Aug 8;29(1):27–33. doi: 10.1007/s10068-019-00642-4

Antioxidant and antibacterial activity of Trametes polyzona (Pers.) Justo

Erute M Adongbede 1, Yogini S Jaiswal 2, Shurrita S Davis 2, Priscilla D Randolph 2, Li-Ni Huo 3, Leonard L Williams 2,✉
PMCID: PMC6949344  PMID: 31976124

Abstract

Polypores are cosmopolitan mushrooms, widely investigated for their beneficial properties in combatting multidrug resistant pathogens. The present study focuses on the need for new, naturally sourced antimicrobial and antioxidant compounds from mushrooms. The antioxidant and antibacterial activity of the phenolic extract of strains of Trametes polyzona (Pers.) Justo, were investigated. Strains of T. polyzona were analyzed for total phenolic content, Trolox antioxidant equivalent, DPPH radical scavenging and antibacterial activities. The amplification of the ribosomal DNA-ITS fragments from DNA of selected mushrooms was carried out using ITS1 and ITS4 primers. The antibacterial activity of phenolic extracts of T. polyzona was comparable to the antibiotics, ceftazidime and erythromycin. T. polyzona extracts inhibited the growth of the different strains of K. pneumoniae, E. coli, S. aureus, and S. enterica tested in this study. The results of the study demonstrate that, T. polyzona can be a potential source of antimicrobial and antioxidant compounds.

Electronic supplementary material

The online version of this article (10.1007/s10068-019-00642-4) contains supplementary material, which is available to authorized users.

Keywords: Nutraceuticals, Oxidative damage, Polypore, Polyphenols, Reactive oxygen species

Introduction

Polypores are the most abundant macro-fungi found in Southern parts of Nigeria (Adedokun et al., 2016). Interest in bioactive compounds from polypores is because of their use in folklore medicine and potential pharmaceutical value (Adedokun et al., 2016; Al-Fatimi et al., 2013; Côté et al., 2010; Oyetayo et al., 2012, 2013; Sánchez, 2017). These macro-fungi have high concentrations of polyphenols and polysaccharides, that are biologically important (Kosanić et al., 2012). The phenolic compounds in mushrooms can belong to pyrogallol, myricetin, caffeic acid, quercetin and catechin group of compounds (Pattar and Ramesh, 2010). There is a rising interest in antioxidants like polyphenols from natural sources, because of the adverse effects of certain synthetic antioxidants (Kozarski et al., 2015). Reports indicate that synthetic antioxidants can have carcinogenic effects (Tenore et al., 2011). Polyphenols from polypores are reported to have anticancer, antiviral and immunomodulating effects (Grienke el al., 2014). Of special interest are polyphenol extracts of species from Trametes genus, which have been shown to have antigenotoxic activity (Knežević et al., 2015). The genus Trametes has members that are cosmopolitan and can be found in all types of forest ecosystems in temperate, boreal and tropical regions (Justo and Hibbett, 2011). T. polyzona (Pers.) Justo is a polypore that is prevalent in the tropics and has medical values that have not been yet studied or utilized (Wasser, 2002; Zmitrovich et al., 2012). The polypore was initially classified as Coriolopsis polyzona (Pers.) Ryvarden in several literature reports (Oyetayo and Ogidi, 2011). T. polyzona, in literature has been reported to have both anti-oxidant and antimicrobial activities. Anti-microbial and anti-oxidant bioactive compounds mushrooms, have been extracted from their fruit bodies and mycelium (Barros et al., 2007; Ferreira et al., 2007). There are factors that can affect the content and concentration of phenolic compounds in mushrooms such as environment, soil/substrate and habitat conditions (Gąsecka et al., 2018).

It is reported that, drug resistant infections have caused up to 50,000 deaths in the US and Europe, and are a global concern (MacIntyre and Bui, 2017). These infections are difficult to treat with the current antibiotics, resulting in higher morbidity and mortality (Finley et al., 2013). According to Zjawlony et al. 75% of polypores that have been tested, exhibited strong antimicrobial activity (Zjawiony, 2004).

Thus, based on the literature indicating strong potential for mushrooms of genus Trametes to be sources of novel anti-microbial and antioxidant agents, extracts of T. polyzona species were selected for evaluation of their anti-oxidant and anti-bacterial activity.

Materials and methods

Sample collection and identification

Trametes polyzona samples were collected in Lagos State, Nigeria from April to August 2015. Fresh fruiting bodies of T. polyzona were collected from University of Lagos (Akoka) and the Lekki Conservation Center (Lekki Peninsula), Nigeria. Three different sites from each location were selected for thee study. The samples collected from the University of Lagos (Voucher no. BKW01) and the Lekki Conservation Center (Voucher no. BKW004) are designated as M1 and M2, respectively. The GPS coordinates of sampling locations are listed in (Table 1). The Lekki Conservation Center is an undisturbed forest with little or no human activities, and thus has a plethora of mushroom varieties growing in this area. The collected specimens were taken to the lab and morphological features needed for identification were recorded. Prior to performing any investigation, the collected mushrooms were cleaned and washed to remove any soil debris. The mushroom samples were then sliced and dried in a Stockli (Switzerland), food grade dehydrator at 40 °C for 12 h. The morphological identification was carried by identifying the macroscopic and microscopic features. After DNA extraction and sequencing, the molecular identifications were carried out using the nblast tool on the NCBI website. The mushrooms collected from the two different locations were confirmed as T. polyzona by matching their sequences with herbarium voucher specimens on the NCBI website using the sequence alignment and megablast tool. After identification, the current name from the website www.mycobank.org was established and adopted (Glenn and Bodri, 2012).

Table 1.

Location of sampling area with GPS co-ordinates and identity match from NCBI gene bank website

Parameters M1 samples M2 samples
Site 1
GPS co-ordinate 6031′06.5″N 3024′04.1″E 6026′28.5″N 3032′09.2″E
JN164980.1 JN164978.1
E-value 0.0 0.0
ID match (%) 99.0 99.0
Site 2
GPS co-ordinate 6031′04.3″N 3024.016E 6026′29.3″N 3032′07.6″E
JN164978.1 JN164978.1
E-value 0.0 0.0
ID match (%) 99.0 99.0
Site 3
GPS co-ordinate 6031′00.7″N 3023′56.0″E 6026′28.1″N 3032′09.3″E
JN164980.1 JN164978.1
E-value 0.0 0.0
ID match (%) 99.0 99.0
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DNA extraction

Identification was confirmed using molecular means and DNA extraction was carried out with Norgen Plant/Fungi DNA Isolation kit (Xiao et al., 2015; Ziv et al., 2014). Dried mushroom tissues were crushed into powder with the aid of liquid nitrogen and DNA were extracted following manufacturer’s instructions. The DNA were qualitatively and quantitatively analyzed using the Nanodrop 2000 spectrophotometer (Thermo Fisher Scientific Inc., Wilmington, Delaware US) and electrophoresis, respectively.

PCR amplification and sequencing

The primers ITS 1 forward, 5′-TCC GTA GGT GAA CCT GCG G-3′ and ITS 4 reverse 5′-TCC TCC GCT TAT TGA TAT GC-3′ were used to amplify the fragments of the extracted ribosomal DNA (rDNA) (Zhang et al., 2000). PCR analysis was carried out using the Norgen’s 2 × PCR master mix, with a final volume of 20 µL. The master mix comprised of 2 µL of primers (ITS-1F and ITS-4R), 10 µL of master mix and 8 µL of DNA free water. Amplification was done carried out in a thermocycler with heated lid and started with an initial denaturation step at 94 °C for 3 min, followed by a 30 cycles series of denaturation at 94 °C for 1 min. Annealing was then carried out for 1 min at 56 °C, and elongation for 1 min at 72 °C. Amplification was concluded with a final extension for 10 min at 72 °C (Martin and Rygiewicz, 2005; Thompson et al., 1997; White et al., 1990) PCR products were further analyzed by electrophoresis in a 1% agarose gel tank with standard TBE buffer. The gel run was viewed, and images were captured in a UV chamber. The amplified PCR products were cleaned using the PCR purification kit from Norgen Biotek Corp. ON, Canada.

Sequence editing involved trimming and assembling of sequences using the Sequencher 5.4.6 software. Sequences were aligned with the multiple sequence alignment program—the Clustal tool in the sequencer software. The identity of the mushrooms was confirmed with the megablast tool available on the NCBI GenBank (Martin and Rygiewicz, 2005; Zhang et al., 2000).

Extraction of phenolic compounds

Extraction of polyphenols was done by adopting the methods described by Vieira et al., with slight modifications (Vieira et al., 2012). Dehydrated mushroom tissues were pulverized with a mill. Polyphenols were extracted from 3 g of pulverized mushroom tissues with 60 mL of acidified methanol at room temperature (23 °C) (Vieira et al., 2012). The extraction was carried out with a magnetic stirrer at 2.5 Hz for 1 h, and then filtered with Whatman filter. The extraction process was repeated twice, and the extracts were combined and concentrated with a rotary evaporator, under reduced pressure. The concentrated extracts were reduced to dryness at 40 °C and reconstituted with 70% methanol to obtain a concentration of 20 mg/mL.

Total phenolic contents

The total phenolic contents of the extracts of T. polyzona were determined adopting the method of Vieira et al., with some modifications (Pérez-Jiménez et al., 2014; Vieira et al., 2012). The methanolic extract solutions (1 mL) were added to Folin–Ciocalteu reagent previously diluted in water (1:10). The mixed solutions were left undisturbed for 5 min, and 4 mL of sodium carbonate (75 g/L) was added to the resultant mixture. The tubes were vortexed and allowed to stand for 1 h in the dark for color development. Gallic acid was used as the standard and a standard calibration curve (0.01–0.15 mg/mL) was constructed. The results were expressed as gallic acid equivalents (GAE) per 100 g of extract.

2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity

The free radical scavenging activities of the mushroom extracts from the different locations were determined by using 2, 2-diphenyl-1-picrylhydrazyl (DPPH) as free radicals. The DPPH powder was dissolved in methanol to obtain a concentration of 6 × 10 mol/L. The percentage inhibition of these radicals was determined using an ELX800 microplate reader. The reaction mixture in each well of 96 well microtiter plate consisted of the methanolic extracts (30 µL) and the methanolic solution of DPPH radicals (270 µL). The reaction mixtures were left un-disturbed for about 40 min in the dark. The radical scavenging activity was calculated as a percentage of DPPH radical discoloration with the below mentioned formula:

RSA=ADPPH-AS×100/ADPPH

where AS = absorbance of the mix of sample extracts and DPPH radical solution, and ADPPH is the absorbance of the DPPH radical solution, used as control. A standard curve was constructed from the reaction between different concentrations of Trolox solutions and DPPH radicals to determine the Trolox antioxidant equivalent capacity (Wang et al., 2013; Yuan et al., 2012).

Determination of antimicrobial activity of phenolic extract of Trametes polyzona

Test microorganisms: Klebsiella pneumoniae [(ATCC 1100975), (ATCC 1100975), (BAA1705), and (ATCC 1100770)] Escherichia coli [(ATCC 700972), (ATCC 25922) and (ATCC 25927)], Staphylococcus aureus (ATCC 700698) and Salmonella enterica were purchased from American Type Culture Collection (ATCC), and used as test organisms. The bacterial specimens were provided by the Center for Excellence in Post-Harvest Technologies, NC A& T State University at The North Carolina Research Campus, Kannapolis, NC. The antimicrobial assay was carried out using the paper disc diffusion method, (Jayakumar et al., 2009; Schinor et al., 2007). Test bacteria were cultured overnight using Tryptic soy broth. The cultures were standardized by serial dilution to a 0.5 McFarland solution using the McFarland standards. Petri plates (150 × 15 mm) were plated using the spiral plater and sterilized paper discs (6 mm) impregnated with 30 µL of extracts solution (20 mg/mL) were placed on the surface of the agar. The inoculated plates were incubated at 37 °C overnight. Post incubation, the zones of inhibition were recorded by measuring diameter of the clear visible zones to the nearest mm. The antibiotics ciprofloxacin, clindamycin, ceftazidime, penicillin, erythromycin and azithromycin were used as positive controls. Methanol was used as the negative control.

Results and discussion

Trametes polyzona is a polypore and studies report that most polypores have phenolic compounds that are biologically active. The species from Trametes genus are mostly regarded as medicinal mushrooms. Phenolic compounds extracted from T. polyzona exhibited significant antioxidant and antimicrobial activities in this study. Factors such as environment, soil/substrate and habitat conditions can affect the content and concentration of phenolic compounds in mushrooms (Gąsecka et al., 2018). Images of representative mushroom samples included in the study, are provided in Fig. 1.

Fig. 1.

Fig. 1

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Images of samples of T.polyzona mushrooms included in the study. (A) horizontal view, (B) vertical view

The ITS region of the genomic ribosomal DNA were analysed using ITS1 and ITS4 primers. The data obtained upon analysis, suggests that the mushrooms collected from various locations belonged to the same species of the Trametes genus. The identity of the mushrooms were confirmed to be T. polyzona. Thus, it can be inferred that although the mushrooms were collected from various geographical variations and indicated some variations in their morphological appearences, they did not have any genetic differences.

The total phenolic content of the strains of T. polyzona collected from the two sampling sites (M1 and M2) varied from 11.09 to 35.08 mg/GAE per g of extract (see Fig. 2). A higher variation in the phenolic content of the strains collected from three different sites of M1 location was observed, than among those collected from the M2. T. polyzona species from M2 site had lower concentrations of polyphenols (Fig. 2). The variation in the phenolic content of mushrooms based on the location of collection (higher human activity or least human activity) were reported by Yildirim et al., for Pleurotus eryngii (2012). The reports indicate higher concentrations of polyphenol in extracts of the mushrooms collected from regions with more human activity than those collected from areas with less human activity (Pop et al., 2018; Yildirim et al., 2012).

Fig. 2.

Fig. 2

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Graphical representation of Total Phenolic Content of T. polyzona samples used in this study. M1 location: site 1-Lagoon front; site 2-Botanic garden; site 3-Indomie bridge, M2 location: site 1-Nature’s choice café; site 2-Lekki conservation park; site 3-Lekki conservation road trail

The Trolox equivalents in the strains of T. polyzona varied from 0.27 to 3.23 mg Trolox/g of dry sample (Fig. 3). Strains from M2 location had the highest Trolox equivalent antioxidant capacity (TEAC) (Fig. 3). There was however no significant difference between the TEAC of strains from the M1 and M2 location (Fig. 3). The GPS coordinates and identity match percentages are listed in Table 1.

Fig. 3.

Fig. 3

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Graphical representation of Trolox Equivalents Capacity of strains of T. ployzona. M1 location: site 1-Lagoon front; site 2-Botanic garden; site 3-Indomie bridge M2 location: site 1-Nature’s choice café; site 2-Lekki conservation park; site 3-Lekki conservation road trail

Strains of T. polyzona collected from the site 3 of location M1, had the highest percentage inhibition of DPPH radicals (81.75%) (Fig. 4). The least radical scavenging activity was recorded in extracts from tissues of T. polyzona collected from site 1 at location (29.59%). There was however no significant difference between the other two sites in M2 location (Fig. 4).

Fig. 4.

Fig. 4

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Radical scavenging activity of phenolic extracts from strains of T. polyzona

The effect of the crude phenolic compounds extracted from T. polyzona from the different sites varied in their degree of inhibition of K. pneumoniae. The extracts from the site 2 at location M1 had the highest degree of inhibition (20.94 mm) compared to the extracts obtained from the samples collected from other sites with K. pneumoniae (ATCC 1100975) (Table 2). All four strains tested were susceptible to azithromycin while only K. pneumoniae (BAA1705) was resistant to Ceftazidime. The strain K. pneumoniae (1002565) showed intermediate susceptibility to ciprofloxacin. All three strains of E. coli tested, were susceptible to all antibiotics tested, except ceftazidime. The crude phenolic extracts from T. polyzona from all sites did not show any significant inhibition against E. coli (ATCC 700972) but showed intermediate susceptibility with E. coli (ATCC 25922) and E. coli (ATCC 25927). The crude phenolic compounds extracted from tissues collected at site 2 of M2 location, did not significantly inhibit any of the three strains of E. coli tested (Supplementary file Table S1).

Table 2.

Inhibition zones of four strains Klebsiella pneumoniae with antibiotics and phenolic extracts of T. polyzona

Sampling location Test sample K. pneumoniae K. pneumoniae K. pneumoniae K. pneumoniae
1100975 1002565 BAA1705 1100770
Ciprofloxacin 7.10 ± 0.47 6.33 ± 0.19 7.21 ± 0.92 6.29 ± 0.45
Clindamycin 9.05 ± 1.02 19.52 ± 1.28 6.35 ± 0.27 8.92 ± 0.24
Ceftazidime 20.66 ± 1.83 24.55 ± 1.15 8.00 ± 0.35 21.45 ± 1.45
Penicillin 8.55 ± 0.61 8.10 ± 0.83 7.24 ± 0.57 7.55 ± 0.65
Erythromycin 7.04 ± 0.60 8.19 ± 0.78 6.91 ± 0.65 8.06 ± 0.42
Azithromycin 25.22 ± 1.19 26.45 ± 1.98 22.81 ± 1.68 25.75 ± 1.65
M1 Site 1 9.19 ± 0.83 8.35 ± 0.14 7.48 ± 0.31 6.39 ± 0.55
Site 2 20.94 ± 2.18 9.03 ± 0.39 9.23 ± 1.04 8.45 ± 0.58
Site 3 15.09 ± 1.29 8.23 ± 0.94 15.08 ± 1.48 7.22 ± 0.61
M2 Site 1 9.11 ± 0.36 6.95 ± 0.10 7.12 ± 0.91 9.08 ± 0.63
Site 2 8.60 ± 0.24 7.22 ± 0.73 6.10 ± 0.54 8.21 ± 0.75
Site 3 7.78 ± 0.37 6.38 ± 0.37 8.00 ± 0.64 8.92 ± 0.56
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The above stated values indicate the inhibition zones in millimetres (mm)

S. enterica exhibited intermediate to complete resistance to the crude phenolic compounds extracted from T. polyzona collected from both locations M1 and M2. However, S. aureus was susceptible to the phenolic extracts from T. polyzona collected from site 3, of M1 location. Intermediate susceptibility towards S. enterica was found in polyphenol extracts, when tested with the disc diffusion method (Supplementary file Table S2).

This clearly indicates that the phenolic compounds in T. polyzona have robust antimicrobial activity. The control antibiotics exhibited better anti-microbial activity than the polyphenol extracts. Clindamycin and penicillin exhibited the least zone of inhibition values against S. enterica, compared to all other antibiotics tested (see Supplementary file Table S2).

The polyphenol extracts of T. polyzona tested in this study, demonstrated a good potential for antioxidant effect by exhibiting up to 80% DPPH radical scavenging activity. In anti-microbial assays, the extracts inhibited the growth of the different strains of K. pneumoniae, E. coli, S. aureus, S. enterica tested in this study.

Thus, from the results of this study we infer that, T. polyzona is a potential source of new antibacterial and anti-oxidant agents. Variations in geographical locations and other environmental factors can qualitatively and quantitatively affect the bioactive constituents of plant materials. The polyphenol extracts of T. polyzona mushrooms can serve as potential candidates in design of therapeutically beneficial agents, for treatment of diseases and complications resulting due to free radical damage and anti-microbial drug resistance.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb) (18.1KB, docx)

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Footnotes

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Contributor Information

Erute M. Adongbede, Email: e.adongbede@gmail.com

Yogini S. Jaiswal, Email: yoginijaiswal@gmail.com

Shurrita S. Davis, Email: sd017437@ncat.edu

Priscilla D. Randolph, Email: pdrandol@ncat.edu

Li-Ni Huo, Email: huolini@126.com.

Leonard L. Williams, Email: llw@ncat.edu

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