Skip to main content
NCBI home page
Foods logoLink to Foods
. 2022 Nov 4;11(21):3516. doi: 10.3390/foods11213516

Nutritional Composition and Bioactive Properties of Wild Edible Mushrooms from Native Nothofagus Patagonian Forests

Maximiliano Rugolo 1,2,3, Rafael Mascoloti Spréa 2,3, Maria Inês Dias 2,3, Tânia C S P Pires 2,3, Mikel Añibarro-Ortega 2,3, Carolina Barroetaveña 1,*, Cristina Caleja 2,3,*, Lillian Barros 2,3
Editors: Rui Yang, Hai Chen
PMCID: PMC9654758  PMID: 36360128

Abstract

Nothofagus forests of the Andean Patagonian region are home to numerous wild edible mushroom (WEM) species with interesting organoleptic characteristics, although many of them have unknown nutritional and nutraceutical profiles. The proximal composition, fatty and organic acids, soluble sugars, phenolic compounds, ergosterol, as well as antioxidant and antimicrobial activity of 17 WEMs were analyzed. Carbohydrates, the most abundant macronutrients, varied between 49.00 g/100 g dw (C. magellanicus) and 89.70 g/100 g dw (F. antarctica). Significantly higher values were found for total fat in G. gargal (5.90 g/100 g dw) followed by A. vitellinus (4.70 g/100 g dw); for crude protein in L. perlatum (36.60 g/100 g dw) followed by L. nuda (30.30 g/100 g dw); and for energy in G. gargal (398 Kcal/100g) and C. hariotii (392 Kcal/100g). The most effective extracts regarding the TBARS antioxidant capacity were those of Ramaria. This is the first time that a study was carried out on the chemical composition of G. sordulenta, C. xiphidipus, F. pumiliae, and L. perlatum. The promotion of sustainable use of WEMs, including their incorporation in functional diets that choose WEMs as nutritious, safe, and healthy foods, and their use in an identity mycogastronomy linked to tourism development, requires the detailed and precise nutritional and nutraceutical information of each species.

Keywords: non-timber forest products, metabolites, functional food, antioxidant properties, antimicrobial activity

1. Introduction

Edible wild mushrooms are highly available functional foods. Its consumption has been developed and perpetuated in various countries from all over the world [1]. Their commercial and culinary importance is mainly due to their organoleptic properties, such as aroma and flavor, their nutritional qualities, and their medicinal characteristics [2,3,4,5], due to their high protein and fiber content, essential amino acids, bioactive compounds, and low lipids content [3,6].

Different mushrooms have been studied in search of new therapeutic alternatives, finding that they have bioactive properties [7,8,9] and that they constitute rich sources of nutraceuticals molecules [10,11], which are responsible for their antioxidant [12,13,14] and antitumor properties [15]. Antioxidants from edible natural products are currently widely studied for their ability to protect organisms and cells from damage caused by oxidative stress, which is one of the causes of aging and degenerative diseases [16].

Patagonian Andean forests comprise 3,240,996 h dominated by Nothofagus spp. (N. antarctica, N. dombeyi, and N. pumilio are the most representative species) [17]. The region harbors numerous species of wild fungi that are potentially edible, with high nutritional and medicinal value [18,19]. These species have been mentioned by Mapuche communities as having continuity of use over time, excellent organoleptic properties, and commercially viable [20]. The list of prominent and understudied species with consumption records includes Aleurodiscus vitellinus (Lev.) Pat., Cyclocybe aegerita (V. Brig.) Vizzini, Cyttaria hariotii E. Fisch., Cortinarius magellanicus complex Speg., Cortinarius xiphidipus M.M. Moser y E. Horak, Fistulina antarctica Speg., Fistulina endoxantha Speg., Fistulina pumiliae González, Barroetaveña & Pildain, Flammulina velutipes (Curtis) Singer, Grifola gargal Singer, Grifola sordulenta (Mont.) Singer, Hydropus dusenii (Bres.) Singer, Lepista nuda (Bull.) Cooke, Lycoperdon perlatum Pers., Ramaria botrytis (Pers.) Bourdot and R. patagonica (Speg.) Corner, and Pleurotus ostreatus (Jacq.) P. Kumm. [20,21,22,23,24]. Some of these and other cultivated fungi from Argentina and Chile were recently studied to check their nutritional and antioxidant potential [14,25]. However, the list of analyzed WEMs in this regard is not complete. New techniques are available to recheck and compare antioxidant contents, along with other bioactive properties such as antimicrobial activity [26], and compositions from specimens from different areas and habitats of already analyzed species should be carried out to know their variability [27]. Wild fungi have gained special interest in recent decades due to their value as functional foods and their promising future related to the development of local economies [19,28,29]. The combined study of their taxonomy and molecular genetic diversity [19,30,31,32,33,34,35], their phenology, ecology, and productivity [19,22], and the determination of their nutritional and nutraceutical profiles are required to expand the current variety of harvested species (mainly Morchella spp. and Suillus luteus [20]) for their sustainable and safe use, thereby creating novel modalities of products and services that locals could offer [28].

This study aimed to widen the comprehension of the biological properties and nutritional composition of endemic and cosmopolitan species of wild Patagonian edible mushrooms growing in Nothofagus forests. The bioactivity evaluation focused on phenolic compounds contents and antimicrobial and antioxidant properties. The chemical analysis comprised the determination of macronutrients (protein, lipids, carbohydrates, and ashes) and the composition of sugars, fatty acids, and organic acids. Comparison with previous reports for some species are included.

2. Materials and Methods

2.1. Fungi Identification and Sampling

Specimens of seventeen species (Figure 1) of WEMs (Aleurodiscus vitellinus, Cyclocybe aegerita, Cyttaria harioti, Cortinarius magellanicus, Cortinarius xiphidipus, Fistulina antarctica, F. endoxantha, F. pumiliae, Flammulina velutipes, Grifola gargal, G. sordulenta, Hydropus dusenii, Lepista nuda, Lycoperdon perlatum, Pleurotus ostreatus, Ramaria botrytis, and R. patagonica) were sampled during the mushroom fruiting seasons in Patagonia: fall (April–May) and spring (October–November) of 2019 and 2020, according to species phenology [22]. Locations included Nothofagus spp., Maytenus boaria, and Lomatia hirsuta forests from National Parks of the Chubut (PN Los Alerces and PN Lago Puelo), Río Negro (PN Nahuel Huapi), and Neuquén (PN Lanín) provinces, Argentina. Each sample (complete fruitbodies) was freeze-dried, pulverized, and stored in polyethylene bags at −18 °C in a freezer for subsequent analyses. Representative species of each species were dehydrated and incorporated in the Herbarium of the Patagonian Forest Research Center (CIEFAP; Esquel, Chubut, Argentina).

Figure 1.

Figure 1

Open in a new tab

Samples of the wild studied mushrooms. (A). Aleurodiscus vitellinus; (B). Fistulina antarctica; (C). Fistulina endoxantha; (D). Grifola sordulenta; (E). Cyclocybe aegerita; (F). Cyttaria hariotii; (G). Grifola gargal; (H). Lepista nuda; (I). Ramaria botrytis; (J). Cortinarius xiphidipus; (K). Ramaria patagonica; (L). Hydropus dusenii; (M). Lycoperdon perlatum; (N). Cortinarius magellanicus; (O). Pleurotus ostreatus; (P). Flammulina velutipes; (Q). Fistulina pumiliae.

2.2. Nutritional Characterization

Samples of each species were analyzed for nutritional composition (protein, carbohydrates, fat, ash, and energy) using AOAC procedures [36]. The total carbohydrates were obtained by difference, and the energy values were calculated with the equation Energy (kcal) = 4 × (g protein + g carbohydrates) + 9 × (g fat). The results are expressed in kcal per 100 g of dry weight (dw).

2.3. Chemical Composition

2.3.1. Free Sugars

Free sugars determination followed the methodology by Barros et al. [37]. Analysis was performed by liquid chromatography (HPLC, Knauer, Smartline 1000 systems, Berlin, Germany), coupled with a refraction index detector (Knauer Smartline 2300). The detected compounds were identified by comparison with the retention times of the standards. Trehalose was used as the internal standard. Results are expressed in g/100 g of dry weight (dw).

2.3.2. Fatty Acids

The fatty acids were identified by gas chromatography with flame ionization detection (GC-FID), as previously described by Pereira et al. [38]. The identification of fatty acids was made according to their relative retention times of the FAME peaks of the sample standards (mixture 37, 47885-U purchased from Sigma). To process the results, we used CSW 1.7 software (DataApex 1.7, Prague, Czech Republic); results are expressed as a relative percentage (%).

2.3.3. Ergosterol

The ergosterol was quantified after extraction following Vieira Junior et al. [39]. It was determined by high-performance liquid chromatography (HPLC) coupled to a UV detector (280 nm), as described by Cardoso et al. [40], and was identified and quantified by comparison with the pure chemical standard and expressed in mg/100g dw.

2.3.4. Organic Acids Composition

The organic acids were determined by high-performance liquid chromatography coupled to a photodiode detector (UFLC-PDA) following the methodology described by Barros et al. [37]. The detection of organic acids was achieved using a DAD system, applying a wavelength of 215 nm (and 245 nm for ascorbic acid). The quantification was carried out by comparing the area of their recorded peaks with the calibration curves obtained from the standards of the respective compound. The results are expressed in mg/100 g (fw).

2.3.5. Phenolic Composition

Samples of 0.5 g of freeze-dried specimens were used for the extract preparation. They were initially macerated at room temperature with the addition of a solution (30 mL) of ethanol/water (80:20, v/v), for 1 h (150 rpm). Ethanol was removed under reduced pressure. Afterwards, the aqueous phase of both extracts was frozen and lyophilized.

The identification and quantification of the phenolic compounds followed the previously optimized methodology [41], using a Dionex Ultimate 3000 UPLC system (Thermo Scientific, San Jose, CA, USA). The DAD and mass spectrometer (LTQ XL mass spectrometer, Thermo Finnigan, San Jose, CA, USA) were working in negative mode.

2.4. Bioactivities Evaluation

2.4.1. Evaluation of Antioxidant Activity

An in vitro assay based on the monitoring of malondialdehyde (MDA)-TBA complexes was carried out as previously reported [42] to measure the extract capacity to inhibit the formation of thiobarbituric acid reactive substances (TBARS). Porcine brain cells were used as biological substrates. The results are expressed as IC50 values (mg/mL).

For the oxidative hemolysis inhibition assay (OxHLIA), sheep erythrocytes were used, as previously described by Lockowandt et al. [43]. Results are expressed as half-maximal inhibitory concentrations (IC50 values, μg/mL) calculated for a Δt of 60 min. Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid, purchased from Sigma), was used as a positive control.

2.4.2. Evaluation of Antibacterial Activity

The extracts were tested against five Gram-negative bacteria, namely, Enterobacter cloacae (ATCC 49741), Escherichia coli (ATCC 25922), Pseudomonas aeruginosa (ATCC 9027), Salmonella enterica subsp. enterica serovar Enteritidis (ATCC 13076), and Yersinia enterocolitica (ATCC 8610), and three Gram-positive bacteria, namely, Bacillus cereus (ATCC 11778), Listeria monocytogenes (ATCC 19111), and Staphylococcus aureus (ATCC 25923). The minimum inhibitory (MIC) and minimum bactericidal concentrations were determined for all bacteria using colorimetric assays, following Pires et al. [44]. The MIC was defined as the lowest concentration inhibiting visible bacterial growth, determined by a change from yellow to pink coloration if the microorganisms are viable. The MBC was defined as the lowest concentration required to kill bacteria.

To evaluate the antifungal activity, the methodology described by Heleno et al. [45], using Aspergillus fumigatus (ATCC 204305) and Aspergillus brasiliensis (ATCC 16404), was used. The organisms were obtained from Frilabo, Porto, Portugal. The minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC) were determined by a serial dilution technique using 96-well microplates. The lowest concentrations without visible growth (at the binocular microscope) were defined as the MICs. The lowest concentration with no visible growth was defined as the MFC, indicating 99.5% killing of the original inoculum. The commercial fungicide ketoconazole (Frilabo, Porto, Portugal) was used as positive control.

2.5. Statistical Analysis

Three independent samples per mushroom species were analyzed, and the data are expressed as the mean ± standard deviation. All statistical tests were performed at a 5% significance level in RStudio (version 1.1.485—© 2009–2022 RStudio, Inc.) [46]. The homogeneity of variance and normal distribution of the residuals were tested by means of the Shapiro–Wilk and Levene tests, respectively, to fulfill the one-way ANOVA requirements. All dependent variables were compared using Tukey’s tests. When normality or heteroscedasticity could not be verified, the variables were Box–Cox transformed before performing the ANOVA. Kruskal–Wallis tests were carried out when a normal distribution and heteroscedasticity were not achieved after Box–Cox transformation.

3. Results and Discussion

The obtained chemical compositions and energetic values are shown in Table 1. Protein contents varied between 3.20 g/100 g dw in F. antarctica and 36.60 g/100 g dw in L. perlatum. The top-five values concerning of highest protein content was L. perlatum (36.60 g/100 g dw), L. nuda (30.30 g/100 g dw), H. dusenii (22.20 g/100 g dw), R. patagonica (18.10 g/100 g dw), and C. magellanicus (14.40 g/100 g dw). Comparing with previous studies, Ramaria patagonica and R. botrytis showed similar results than those reported by other authors with a value of 19.68 g/100 g dw [25] and 16.60 g/100 g dw [14]. However, in a Portuguese mushroom study [16], R. botrytis showed higher protein values (39.8 g/100 g dw) than our results. Flammulina velutipes (17.89 g/100 g dw) and C. aegerita (19.65 g/100 g dw) showed lower levels than those reported by Jacinto-Azevedo et al. [14]. Other studies on G. gargal showed similar results with values of 5.96 [25] and 5.00 g/100 g dw [38]. Previous studies on Cyttaria have reported higher values than those reported here; for example, C. espinosae had values of 17.46 g/100 g dw [14] and C. darwini values of 17.20 g/100 g dw [38,47]. However, C. hariotii showed similar results (3.35 g/100 g dw) than those reported by Toledo et al. [25]. The protein values for A. vittelinus, C. magellanicus, F. antarctica, and F. endoxantha are in concordance with other reports [25]. On a dry weight basis, mushrooms normally contain 19 to 35% protein. Therefore, regarding the amount of crude protein, mushrooms are positioned below most animal meats but well above most other foods, including milk, rice, and wheat [48].

Table 1.

Proximate composition (g/100 g) and energetic value (kcal/100 g) of the studied wild mushrooms (mean ± SD). For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Species Total Fat Crude Protein Carbohydrates Ash Energy
A. vitellinus 4.70 ± 0.20b 5.26 ± 0.01kl 81.00 ± 1.00c 8.90 ± 0.30ef 387.74 ± 0.04bc
C. magellanicus 4.40 ± 0.20b 14.40 ± 0.10e 49.00 ± 2.00i 32.00 ± 1.00a 293.00 ± 4.00i
C. xiphidipus 2.01 ± 0.04e 12.30 ± 0.40fg 74.80 ± 0.10d 10.9 ± 0.30d 366.00 ± 1.00f
C. aegerita 2.60 ± 0.20d 10.70 ± 0.30h 63.00 ± 1.00f 23 ± 1.00b 320.00 ± 5.00h
C. hariotii 2.60 ± 0.20d 5.87 ± 0.07jk 86.20 ± 0.20b 5.3 ± 0.30h 392.00 ± 2.00ab
F. antarctica 0.70 ± 0.02f 3.20 ± 0.10m 89.70 ± 0.20a 6.4 ± 0.30g 378.00 ± 1.00de
F. endoxantha 0.77 ± 0.04f 4.70 ± 0.20l 80.00 ± 1.00 c 15 ± 1.00c 345.00 ± 2.00g
F. pumiliae 1.02 ± 0.02f 6.53 ± 0.04j 82.00 ± 1.00c 10 ± 1.00de 364.00 ± 2.00f
F. velutipes 1.70 ± 0.01e 11.40 ± 0.30gh 66.00 ± 1.00f 21.20 ± 0.40b 324.00 ± 2.00h
G. gargal 5.90 ± 0.30a 5.20 ± 0.10kl 81.10 ± 0.10c 7.90 ± 0.40f 398.00 ± 3.00a
G. sordulenta 1.90 ± 0.10e 12.60 ± 0.10f 71.00 ± 1.00e 14.00 ± 1.00c 353.00 ± 3.00g
H. dusenii 3.10 ± 0.10cd 22.00 ± 1.00c 63.00 ± 1.00f 11.30 ± 0.30d 370.40 ± 0.40ef
L. nuda 3.30 ± 0.20c 30.30 ± 0.10b 57.60 ± 0.20g 8.70 ± 0.40f 382.00 ± 3.00cd
L. perlatum 3.32 ± 0.10c 36.60 ± 0.10a 52.00 ± 0.30h 8.10 ± 0.40f 384.00 ± 2.00bcd
P. ostreatus 1.05 ± 0.05f 7.65 ± 0.01i 86.53 ± 0.01b 4.80 ± 0.10h 386.00 ± 1.00bcd
R. botrytis 3.40 ± 0.10c 12.60 ± 0.40f 73.00 ± 1.00de 11.00 ± 1.00d 373.00 ± 1.00ef
R. patagonica 0.90 ± 0.02f 18.10 ± 0.20d 72.40 ± 0.30de 8.60 ± 0.10f 370.00 ± 1.00ef
Open in a new tab

The fat content ranged from 0.70 g/100 g dw (F. antarctica) to 5.90 g/100 g dw (G. gargal). High values were also observed in A. vitellinus (4.70 g/100 g dw) and C. magellanicus (4.40 g/100 g dw). Furthermore, the crude fat content of C. aegerita (1.05 g/100 g dw) was higher than those obtained by Jacinto-Azevedo et al. [14], while F. velutipes (1.70 g/100 g dw) was similar as that reported by other authors [14,38]. In addition, levels in A. vitellinus (3.49 g/100 g dw), C. magellanicus (2.75 g/100 g dw), C. hariotii (1.31 g/100 g dw), G. gargal (1.79 g/100 g dw), and L. nuda (0.84 g/100 g dw) were higher than those obtained by Toledo et al. [25], but were lower in F. antarctica (0.83 g/100 g dw), F. endoxantha (1.19 g/100 g dw), H. dusenii (4.29 g/100 g dw), and R. patagonica (2.51 g/100 g dw) compared to these authors’ findings. The fat content in C. hariotii was similar (2.10 g/100 g dw) than previous reports [47]. Low fat contents in edible mushrooms are one of the reasons why they are recognized as healthy food sources. Chang and Miles [48] have reported fat contents varying between 1 to 15% per 100 g of dried weight, including all types of lipids.

Ash varied from 4.80 g/100 g in P. ostreatus to 32.00 g/100 g in C. magellanicus. Cyttaria hariotii yielded lower values (7.0 g/100 g dw) than what Schmeda-Hirschmann et al. [47] previously reported, and similar values than those reported by Jacinto-Azevedo et al. [14] for C. espinosae (4.90 g/100 g dw). However, lower values were observed in F. velutipes, C. aegerita, and R. botrytis [14], in G. gargal [47], and in F. antarctica and F. endoxantha [25]. Similar results to Toledo et al. [25] were found for L. nuda (8.58 g/100 g dw) and R. patagonica (8.47 g/100 g dw), but lower for L. nuda (18.5 g/100 g dw) compared to Barros et al. [11]. The ash content in edible mushrooms ranges from 1 to 29 g/100 g dry matter and comprise a source of essential minerals. Concentrations of P, K, Ca, Na, and Mg constitute more than 56% of the total ash content [48].

Carbohydrates represent the most abundant nutrient, varying between 49.00 g/100 g dw (C. magellanicus) and 89.70 g/100 g dw (F. antarctica), closely followed by P. ostreatus and C. hariotii. Previous reports showed similar results for F. endoxantha, G. gargal, and R. botrytis, lower for A. vitellinus, C. magellanicus, C. aegerita, C. hariotii, F. velutipes, H. dusenii, and L. nuda, and higher for P. ostreatus and R. patagonica [14,25].

Energetic values ranged from 293.00 Kcal/100 g dw in C. magellanicus to 398.00 Kcal/100 g dw in G. gargal. Other species with high energetic values were C. hariotii (392.00 kcal/100 g dw), A. vitellinus (387.00 kcal/100 g dw), and P. ostreatus (386.00 kcal/100 g dw).

Concerning sugar composition (Table 2), mannitol and trehalose were the principal sugars, which is in agreement with the data presented in the literature; they are essential in energetic metabolism and necessary in the synthesis of storage or structural polysaccharides [38]. Mannitol content was significantly higher for A. vitellinus (8.83 g/100 g dw), R. botrytis (6.34 g/100 g dw), and R. patagonica (8.64 g/100 g dw), although absent in F. endoxantha, in concordance with Toledo et al. [25]. The support and expansion of the mushroom fruiting bodies is guaranteed by the presence of mannitol [49]. Trehalose predominated in C. xiphidipus (17.60 g/100 g dw), P. ostreatus (15.81 g/100 g dw), C. aegerita (13.54 g/100 g dw), and G. sordulenta (11.25 g/100 g dw), but was absent in R. botrytis and R. patagonica. The ingestion, hydrolysis, absorption, and metabolism of trehalose is highly similar to all the other digestible disaccharides [49]. On the other hand, fructose and one unidentified sugar were predominant in all three Fistulina species (F. endoxantha, F. antarctica, and F. pumiliae) in concordance with previous reports [25]. Fructose was also the predominant sugar in Flammulina velutipes (8.56 g/100 g dw), agreeing with Reis et al. [50], while it was absent in A. vitellinus, C. magellanicus, L. perlatum, and P. ostreatus, and present in lower abundance in the rest of the species. In terms of total sugar content, F. endoxantha revealed the highest value (33.88 g/100 g dw), while G. gargal the lowest (3.63 g/100 g dw). This is the first study that reports the composition in free sugars of endemic species C. xiphidipus, F. pumiliae, and G. sordulenta.

Table 2.

Organic acid and sugar composition (mg/100 g) of the studied wild mushrooms (mean ± SD). For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Organic Acids Sugars
Species Oxalic Quinic Malic Shikimic Citric Succinic Fumaric Not Identified Fructose Mannitol Trehalose
A. vitellinus nd nd 74.58 ± 1.03a nd 31.10 ± 0.40b 452.00 ± 2.00a 0.05 ± 0.01n 0.17 ± 0.01i nd 8.80 ± 0.10a 3.16 ± 0.03hi
C. magellanicus 2.02 ± 0.05fg nd 10.90 ± 0.30f nd 57.40 ± 0.03a 8.10 ± 0.20d 11.02 ± 0.02a 0.15 ± 0.01i nd 4.80 ± 0.20c 3.04 ± 0.12hi
C. xiphidipus 0.93 ± 0.01gh 542.00 ± 3.00a nd nd nd nd 3.93 ± 0.01c nd 0.70 ± 0.01e 3.30 ± 0.10d 17.60 ± 0.40a
C. aegerita 0.49 ± 0.01jk nd 17.29 ± 0.04d 0.72 ± 0.04b nd nd 3.40 ± 0.02e nd 0.31 ± 0.02f 1.22 ± 0.04g 13.54 ± 0.02c
C. hariotii 0.09 ± 0.01m nd 13.40 ± 0.30e nd 23.40 ± 0.20a nd 2.39 ± 0.01i 3.19 ± 0.02d 2.10 ± 0.10c 0.33 ± 0.01j 2.10 ± 0.10j
F. antarctica 0.05 ± 0.02m 0.50 ± 0.10b 13.60 ± 0.30e nd nd nd 2.54 ± 0.01h 12.00 ± 1.00a 10 ± 1.00b 1.00 ± 0.10h 8.00 ± 1.00e
F. endoxantha 0.35 ± 0.01lm nd 16.80 ± 1.10d nd nd nd 5.34 ± 0.04b 7.00 ± 0.40b 23.18 ± 1.02a nd 3.70 ± 0.10h
F. pumiliae 0.44 ± 0.01kl nd 35.00 ± 1.00b nd nd nd 5.33 ± 0.01b 6.60 ± 0.30b 9.10 ± 0.40b 3.40 ± 0.10d 5.30 ± 0.20fg
F. velutipes 3.90 ± 0.10cd nd 32.60 ± 0.50b nd nd nd 5.40 ± 0.02b 1.87 ± 0.01e 8.60 ± 0.10b 1.64 ± 0.02f 4.70 ± 0.40g
G. gargal 2.40 ± 0.10ef nd 1.90 ± 0.02h nd nd nd 0.34 ± 0.01m 0.16 ± 0.01i 0.77 ± 0.04d 0.25 ± 0.01k 2.50 ± 0.10ij
G. sordulenta 0.72 ± 0.02hi nd 21.40 ± 0.30c nd nd nd 2.79 ± 0.02g nd 0.30 ± 0.01f 0.50 ± 0.02i 11.30 ± 0.20d
H. dusenii 3.39 ± 0.03de nd nd nd nd nd 1.74 ± 0.01j 0.26 ± 0.02h 0.18 ± 0.01g 2.30 ± 0.10e 5.70 ± 0.10f
L. nuda 66.70 ± 1.90a 488.00 ± 38.00a nd nd nd 277.00 ± 2.00b 1.31 ± 0.01k 0.57 ± 0.01g 0.17 ± 0.01g 1.29 ± 0.01g 7.10 ± 0.10e
L. perlatum 4.90 ± 0.10def nd 8.70 ± 0.20g nd nd 87.00 ± 3.00c 1.20 ± 0.10l 3.88 ± 0.03c nd nd 5.50 ± 0.10fg
P. ostreatus 0.59 ± 0.03ij nd 11.90 ± 0.30ef 1.07 ± 0.03a nd 83.00 ± 1.00c 2.54 ± 0.01h nd nd 3.30 ± 0.10d 15.80 ± 0.40b
R. botrytis 25.36 ± 0.02b nd nd nd nd nd 3.02 ± 0.02f 1.59 ± 0.05f 0.76 ± 0.04de 6.34 ± 0.04b Nd
R. patagonica 25.60 ± 0.10ab nd nd nd 57.30 ± 0.80c nd 3.67 ± 0.01d nd 0.86 ± 0.04d 8.60 ± 0.40a Nd
Open in a new tab

Organic acids comprise a group of mono-, di-, and tricarboxylic acids physiologically occurring as intermediates in a variety of intracellular metabolic pathways, such as catabolism of amino acids, the tricarboxylic acid cycle, and neurotransmitters, as well as in cholesterol biosynthesis [51]. The organic acid composition is presented in Table 2. Most of the analyzed specimens had oxalic, malic, and fumaric acids in their composition. On the other hand, quinic, shikimic, citric, and succinic acids were present just in a few species. Citric acid was detected in high amounts in C. magellanicus (57.40 mg/100 g dw), R. patagonica (57.31 mg/100 g dw), A. vitellinus (31.11 mg/100 g dw), and C. hariotii (23.41 mg/100 g dw). The oxalic acid content was significantly higher for L. nuda (66.72 mg/100 g dw). Shikimic acid was present just in C. aegerita (0.72 mg/100 g dw) and P. ostreatus (1.07 g/100 mg dw). Quinic acid was only present in C. xiphidipus (541.57 mg/100 g dw), F. antarctica (0.54 mg/100 g dw), and L. nuda (487.50 mg/100 g dw). High amounts of succinic acid were detected in A. vitellinus (452.79 mg/100 g dw) and L. nuda (277.39 mg/100 g dw). Aleurodiscus vitellinus and C. magellanicus showed the most optimum amount of malic acid (74.58 mg/100 g dw) and fumaric acid (11.02 mg/100 g dw), respectively. Ascorbic acid was not detected. Analyzing the total organic acids profile, the highest value was revealed by L. nuda (832.92 mg/100 g dw), while the lowest by H. dusenii (5.13 mg/100 g dw).

Table 3 presents the fatty acid composition of each species, along with the values of the total saturated fatty acids (SFAs), polyunsaturated fatty acids (PUFAs), and monounsaturated fatty acids (MUFAs). Linoleic acid (C18:2), oleic acid (C18:1), and palmitic acid (C16:0) were the major fatty acid found in the studied species, in concordance with different studies [10,25]. In total, 27 fatty acids were identified and quantified. Due to the high contribution of linoleic acid, PUFAs were the main group of fatty acids in C. xiphidipus (43%), C. aegerita (48.70%), C. hariotii (48.40%), F. antarctica (48.40%), L. nuda (54.30%), and L. perlatum (68%). MUFAs were the main group of fatty acids in A. vitellinus (54.59%), G. gargal (58.9%), H. dusenii (52.60%), R. botrytis (43.91%), and R. patagonica (39.37%), due to the high contribution of oleic acid, in concordance with Toledo et al. [25]. SFAs predominate in C. magellanicus, F. endoxantha, F. pumiliae, F. velutipes, G. sordulenta, and P. ostreatus due to the palmitic acid content.

Table 3.

Fatty acid composition (%) of the studied wild mushrooms (mean ± SD). (C8:0) caprylic acid; (C10:0) capric acid; (C11:0) undecanoic acid; (C12:0) lauric acid; (C13:0) tridecanoic acid; (C14:0) myristic acid; (C15:0) pentadecanoic acid; (C16:0) palmitic acid; (C16:1) palmitoleic acid; (C17:0) heptadecanoic acid; (C18:0) stearic acid; (C18:1n9) oleic acid; (C18:2n6) linoleic acid; (C18:3n3) α-linolenic acid; (C20:0) arachidic acid; (C20:1) cis-11-eicosaenoic acid; (C20:2) cis-11,14-eicosadienoic acid; (C20:4n6) arachidonic acid; (C20:5n3) cis-5,8,11,14,17-eicosapentaenoic acid; (C21:0) heneicosanoic acid; (C22:0) behenic acid; (C22:1) erucic acid; (C22:2) Cis-13,16-docosadienoic acid; (C23:0) tricosanoic acid; (C24:0) lignoceric acid; (C24:1) nervonic acid; (C22:6n3) docosahexaenoic acid; (SFAs) saturated fatty acids; (MUFAs) monounsaturated fatty acids; (PUFAs) polyunsaturated fatty acids. For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Species A. vitellinus C. magellanicus C. xiphidipus C. aegerita C. hariotii F. anta rctica F. endoxantha F. pumiliae F. velutipes
C8:0 nd 0.63 ± 0.02b nd 0.05 ± 0.01d nd nd nd 0.81 ± 0.02a nd
C10:0 nd nd nd nd nd nd nd nd nd
C11:0 nd nd nd nd nd nd 1.50 ± 0.03a 0.86 ± 0.04b 1.70 ± 0.03a
C12:0 nd 0.11 ± 0.01c nd 0.10 ± 0.01c nd 0.28 ± 0.01b nd nd nd
C13:0 0.15 ± 0.04cd 0.37 ± 0.01a 0.18 ± 0.01bcd 0.24 ± 0.01b 0.13 ± 0.01d nd nd nd nd
C14:0 0.28 ± 0.01g 0.35 ± 0.01f 0.23 ± 0.01gh 0.37 ± 0.01ef 0.22 ± 0.01hi 1.33 ± 0.02b 1.80 ± 0.05ab 2.4 ± 0.10a nd
C15:0 0.82 ± 0.01g 1.47 ± 0.03d 0.50 ± 0.01i 0.44 ± 0.01j 0.15 ± 0.01l 0.71 ± 0.01g 1.58 ± 0.04c 1.66 ± 0.04c nd
C16:0 21.90 ± 0.1d 53.40 ± 0.20b 17.00 ± 1.00f 19.60 ± 0.10e 17.30 ± 0.20f 18.30 ± 0.10e 51.10 ± 0.70b 52.6 ± 0.50b 61.00 ± 1.00a
C16:1 1.70 ± 0.04a 0.61 ± 0.02d 0.31 ± 0.01f 0.57 ± 0.01d nd 0.63 ± 0.03d 1.40 ± 0.01b nd nd
C17:0 0.16 ± 0.01h nd 0.14 ± 0.01i 0.21 ± 0.01g 0.19 ± 0.01g nd 3.19 ± 0.05c 5.4 ± 0.20a nd
C18:0 4.40 ± 0.01de 7.49 ± 0.02b 3.2 ± 0.10h 5.10 ± 0.10c 4.65 ± 0.03cd 2.92 ± 0.02h 7.10 ± 0.30b nd nd
C18:1n9t nd nd nd nd nd nd nd 5.9 ± 0.10c nd
C18:1n9c 52.60 ± 0.10b 19.9 ± 0.10l 31.30 ± 0.50g 20.2 ± 0.20k 6.50 ± 0.10m 26.80 ± 0.30j 32.40 ± 0.30f 30.3 ± 0.10h nd
C18:2n6t 0.22 ± 0.01f nd 1.3 ± 0.10c 1.75 ± 0.02b 0.58 ± 0.01d nd nd nd 37.00 ± 10.00 a
C18:2n6c 13.50 ± 0.10j 12.3 ± 0.10k 40.4 ± 0.30e 44.70 ± 0.20d 25.10 ± 0.20i 48.30 ± 0.20c nd nd nd
C18:3n3 0.96 ± 0.01b nd nd 0.14 ± 0.01d 12.50 ± 0.10a nd nd nd nd
C20:0 0.74 ± 0.02f 1.10 ± 0.01bc 0.80 ± 0.01de 0.77 ± 0.01ef 2.90 ± 0.10a nd nd nd nd
C20:1 0.22 ±0.01h nd 0.75 ± 0.02d 0.67 ± 0.01e 0.43 ± 0.01f nd nd nd nd
C20:2 0.73 ± 0.04d nd 0.85 ± 0.02d 1.10 ± 0.01c 1.50 ± 0.10b nd nd nd nd
C20:4n6 nd nd nd nd 0.44 ± 0.01 nd nd nd nd
C20:5n3 nd nd nd nd nd nd nd nd nd
C21:0 nd nd nd 0.69 ± 0.01a 0.25 ± 0.01b nd nd nd nd
C22:0 0.55 ± 0.01h nd 1.11 ± 0.01c 0.79 ± 0.01f 7.40 ± 0.10a 0.46 ± 0.01h nd nd nd
C22:1 nd 1.8 ± 0.10a 0.24 ± 0.01b 0.29 ± 0.01b 0.27 ± 0.01b nd nd nd nd
C22:2 nd nd nd 0.33 ± 0.01c 0.46 ± 0.01b nd nd nd nd
C23:0 0.19 ± 0.01d 0.42 ± 0.01c nd nd nd nd nd nd
C24:0 0.47 ± 0.01f nd 0.53 ± 0.01f 0.90 ± 0.02d 6.75 ± 0.02a 0.44 ± 0.01f nd nd nd
C24:1 0.07 ± 0.01g nd 0.71 ± 0.02c 0.36 ± 0.01d 4.47 ± 0.05a nd nd nd nd
C22:6n3 0.27 ± 0.01d nd 0.38 ± 0.01c 0.69 ± 0.02b 7.74 ± 0.01a nd nd nd nd
SFAs 29.70 ± 0.10gh 65.40 ± 0.20b 23.70 ± 0.40i 29.20 ± 0.01h 39.90 ± 0.20ef 24.40 ± 0.05i 66.20 ± 0.30a 63.80 ± 0.20c 63.00 ± 1.00cd
MUFAs 54.60 ± 0.10ab 22.40 ± 0.10i 33.00 ± 1.00g 22.10 ± 0.20i 11.70 ± 0.10j 27.30 ± 0.20h 33.80 ± 0.30g 36.20 ± 0.20ef nd
PUFAs 15.73 ± 0.01i 12.30 ± 0.10j 43.00 ± 0.20d 48.70 ± 0.20c 48.40 ± 0.20c 48.30 ± 0.20c nd nd 37.00 ± 1.00f
Species G. gargal G. sordulenta H. dusenii L. nuda L. perlatum P. ostreatus R. botrytis R. patagonica
C8:0 nd nd 0.25 ± 0.01c Nd nd nd nd nd
C10:0 nd nd Nd nd nd 0.40 ± 0.02 nd nd
C11:0 nd nd Nd nd nd 0.84 ± 0.01b nd 0.17 ± 0.01c
C12:0 nd 0.23 ± 0.01b 0.11 ± 0.01c nd nd 0.37 ± 0.01a nd nd
C13:0 nd 0.20 ± 0.01bc 0.15 ± 0.01cd nd nd 0.41 ± 0.02a nd nd
C14:0 nd 1.20 ± 0.04bc 0.36 ± 0.01f 0.36 ± 0.01f 0.47 ± 0.01de 0.77 ± 0.02cd nd 0.17 ± 0.01i
C15:0 nd 3.23 ± 0.03b 1.12 ± 0.01e 0.30 ± 0.01k nd 5.40 ± 0.10a 0.86 ± 0.01f 0.60 ± 0.01h
C16:0 20.00 ± 1.00e 21.33 ± 0.03d 27.30 ± 0.1c 15.40 ± 0.20g 17.00 ± 1.00f 53.00 ± 1.00b 9.67 ± 0.02i 13.90 ± 0.10h
C16:1 0.63 ± 0.01d nd Nd 0.74 ± 0.02c nd nd nd 0.43 ± 0.01e
C17:0 nd 1.46 ± 0.04d 0.49 ± 0.02f nd nd 4.20 ± 0.20b 1.50 ± 0.02d 0.77 ± 0.01e
C17:1 nd nd Nd nd nd nd 0.30 ± 0.01a 0.29 ± 0.01a
C18:0 8.90 ± 0.10a 3.94 ± 0.05fg 9.32 ± 0.03a 2.05 ± 0.05i 3.19 ± 0.05h nd 4.01 ± 0.01ef 3.70 ± 0.10g
C18:1n9t nd nd Nd nd 11.50 ± 0.10a 7.43 ± 0.02b nd nd
C18:1n9c 58.20 ± 0.20a 28.90 ± 0.10i 46.80 ± 0.03c 25.50 ± 0.10j nd 27.00 ± 1.00j 42.67 ± 0.01d 37.60 ± 0.10e
C18:2n6t nd 0.39 ± 0.02e Nd nd nd nd 0.19 ± 0.01g nd
C18:2n6c 11.10 ± 0.30l 31.45 ± 0.01h 1.53 ± 0.04m 54.30 ± 0.10b 68.00 ± 1.00a nd 35.04 ± 0.01g 38.14 ± 0.02f
C18:3n3 0.50 ± 0.02c nd Nd nd nd nd nd nd
C20:0 nd 2.92 ± 0.01a 1.78 ± 0.01b nd nd nd 0.89 ± 0.01cd nd
C20:1 nd 1.50 ± 0.03b 3.48 ± 0.04a nd nd nd 0.33 ± 0.01g 0.88 ± 0.04c
C20:2 nd nd 1.76 ± 0.01a nd nd nd nd nd
C20:4n6 nd nd Nd nd nd nd nd nd
C20:5n3 nd nd Nd nd nd nd 0.29 ± 0.01 nd
C21:0 nd nd Nd nd nd nd nd nd
C22:0 0.33 ± 0.01i 0.97 ± 0.01d 0.73 ± 0.01g 0.55 ± 0.01h nd nd 1.56 ± 0.01b 0.95 ± 0.02e
C22:1 nd nd Nd nd nd nd 0.48 ± 0.01ab nd
C22:2 nd 1.15 ± 0.04a Nd nd nd nd 0.25 ± 0.01d nd
C23:0 nd nd 0.28 ± 0.01d nd nd nd 0.78 ± 0.01b 1.15 ± 0.01a
C24:0 0.51 ± 0.02f 0.99 ± 0.01cd 1.62 ± 0.01b 0.50 ± 0.02f nd nd 0.71 ± 0.02e 1.03 ± 0.02c
C24:1 nd nd 2.32 ± 0.01b 0.33 ± 0.01d nd nd 0.14 ± 0.01f 0.18 ± 0.01e
C22:6n3 0.12 ± 0.01f 0.14 ± 0.01e 0.65 ± 0.01b nd nd nd 0.34 ± 0.01c 0.08 ± 0.02g
SFA 29.40 ± 0.40h 36.47 ± 0.03fg 43.47 ± 0.04de 19.10 ± 0.20k 20.66 ± 1.00 j 66.00 ± 1.00b 19.98 ± 0.01j 22.42 ± 0.02i
MUFA 58.90 ± 0.20a 30.40 ± 0.10h 52.60 ± 0.01bc 26.60 ± 0.10h 11.50 ± 0.10j 34.00 ± 1.00f 43.91 ± 0.01cd 39.37 ± 0.01de
PUFA 11.70 ± 0.30k 33.10 ± 0.10h 3.93 ± 0.04l 54.30 ± 0.10b 68.00 ± 1.00a nd 36.11 ± 0.02g 38.22 ± 0.02e
Open in a new tab

Regarding the favorable effect of fatty acids on human health, oleic acid, a monounsaturated fatty acid ω-9 series, also present in vegetable oils, is known for its efficiency in reducing cholesterol levels, preventing cardiovascular diseases [52,53].

Within polyunsaturated fatty acids, ω-3 and ω-6 are the most abundant in mammals. Its precursors, α-linolenic acid (ALA) and linoleic acid (LA), are considered essential fatty acids, as the body requires them for normal operation but which cannot be synthesized endogenously [54]. Within the series of omega-3, the most important in the human diet are eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), both difficult to synthesize endogenously and with important functions in the human body. DHA is a structural fatty acid, since it forms part of cell membranes and is also important for visual (it makes up 20% of all fatty acids present in the retina) and neuronal development during gestation and early childhood [55,56]. In our study, C. hariotii showed high amounts of DHA (7.74%). Interestingly, some ethnomycological reports [57,58] showed that in the Selknam, Ahonikenk, and Kawesqar native Patagonian populations, after giving birth and while the quarantine lasted, the mothers lived exclusively on Cyttaria fungus (C. darwinii and C. hariotii). In the omega-6 series one has to pay special attention to γ-linolenic acid (GLA) and arachidonic acid (AA), important for prostaglandin production and anti-inflammatory activity [55]. From all the above, the importance of supplementing a diet with fatty acids, which are clearly present in edible mushrooms, can be deduced, since their current intake is insufficient.

The ergosterol content (Table 4) ranged from 0.40 mg/100 g in C. hariotii to 123.57 mg/100 g dw in G. gargal. In other studies of edible and medicinal mushrooms, similar differences have been reported, ranging from traces for Armilaria mellea, to values of 25.71 mg/100 g dw for Laetiporus sulphureus or 445.32 mg/100 g dw for Macrolepiota procera. The differences in ergosterol and other nutritional and bioactive compounds depend on the species, stage of development, tissues, nutrient substrate, and microclimate [26,59]. Vieira Junior et al. [39] showed that ergosterol biosynthesis and its bioconversion into ergocalciferol were also affected by the cultivation process in Agaricus subrufescens production, showing differences between field culture and controlled conditions. Ergosterol is metabolized into a prohormone—vitamin D. Its action is related with bone mineral metabolism and with the balance of phosphorus and calcium, related to various mechanisms such as secretion and effect of insulin, regulation of the renin–angiotensin–aldosterone system, endothelial function, cell cycle control and apoptosis, immunological self-tolerance, and immune response against infections, among other effects [60]. For these reason, edible mushrooms are promising sources of vitamin D, and thus able to improve food supplements for human consumption.

Table 4.

Ergosterol content expressed in mg/100 g dw. For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Species Ergosterol
A. vitellinus 21.50 ± 0.40defg
C. magellanicus 38.00 ± 9.00de
C. xiphidipus 34.00 ± 9.00def
C. aegerita 72.00 ± 10.00b
C. hariotii 0.40 ± 0.10g
F. antarctica 16.00 ± 1.00efg
F. endoxantha 45.00 ± 1.00cd
F. pumiliae 71.00 ± 14.00b
F. velutipes 32.00 ± 2.00defg
G. gargal 123.57 ± 12.00a
G. sordulenta 29.00 ± 9.00def
H. dusenii 16.00 ± 1.00efg
L. nuda 13.00 ± 0.40efg
L. perlatum 31.00 ± 1.00def
P. ostreatus 32.00 ± 2.00defg
R. botrytis 68.50 ± 0.30bc
R. patagonica 13.00 ± 1.00fg
Open in a new tab

Regarding phenolic compounds (Table 5), four phenolic acids (gallic, p-hydroxybenzoic, protocatechuic, and p-coumaric) and two related compounds (3-(3,4-dihydroxyphenyl)-lactic acid and gallic acid monohydrate) were identified and quantified. All the studied species presented gallic acid between 0.80 (for C. hariotii, consistent with previous reports [25]) and 7.36 mg/g dw (C. xiphidipus). The p-hydroxybenzoic acid was present in C. magellanicus, C. xiphidipus, C. aegerita, F. endoxantha, F. pumiliae, L. nuda, L. perlatum, and P. ostreatus, with values of 0.55 mg/g dw for F. pumiliae and 40.33 mg/g dw for L. perlatum. Protocatechuic acid was present in C. magellanicus, C. xiphidipus, C. aegerita, F. antarctica, F. endoxantha, F. pumiliae, G. gargal, R. botrytis, and R. patagonica, with the highest values for F. endoxantha (7.65 mg/g dw) and R. patagonica (5.30 mg/g dw). In addition, p-coumaric acid was registered only in C. aegerita, L. nuda, and L. perlatum. In comparison with the other species, L. perlatum presented a significantly higher value of total phenolic acids (51.40 mg/g dw), attributable to the proportion of p-hydroxybenzoic acid. In the study of Toledo et al. [25], L. nuda did not present phenolic compounds; however, in concordance with Barros et al. [61], in this study, L. nuda presented p-coumaric, gallic, and p-hydroxybenzoic acids.

Table 5.

Phenol content expressed in mg/g. For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Species p-Coumaric Acid Gallic Acid p-Hidroxibenzoic
Acid		 Protocatechuic
Acid		 3-(3,4-Dihydroxyphenyl)-lactic Acid Galic Acid Monohidrate Total
Phenols
A. vitellinus nd 1.94 + 0.05h Nd nd nd nd 1.94 + 0.05i
C. magellanicus nd 5.79 + 0.23c 1.34 + 0.02e 0.85 + 0.01e nd nd 7.90 + 0.20d
C. xiphidipus nd 7.36 + 0.07a 1.60 + 0.10d 1.16 + 0.02d nd nd 10.20 + 0.10c
C. aegerita 0.83 + 0.01b 4.91 + 0.04d 4.10 + 0.10c 0.69 + 0.01f nd 1.19 + 0.04 11.70 + 0.10b
C. hariotii nd 0.80 + 0.01j Nd nd nd nd 0.80 + 0.01l
F. antarctica nd 1.00 + 0.05j Nd 0.15 + 0.01h 0.10 + 0.01c nd 1.30 + 0.10k
F. endoxantha nd 2.03 + 0.04h 5.90 + 0.10b 7.65 + 0.04a 1.75 + 0.02a nd 11.40 + 0.10b
F. pumiliae nd 1.43 + 0.01i 0.55 + 0.02g 0.69 + 0.01f 1.01 + 0.02b nd 3.12 + 0.02h
F. velutipes nd 2.84 + 0.04g Nd nd nd nd 2.84 + 0.04h
G. gargal nd 3.58 + 0.03f Nd 0.56 + 0.02g nd nd 4.20 + 0.10g
G. sordulenta nd 1.74 + 0.11hi nd nd nd nd 1.70 + 0.10ij
H. dusenii nd 4.40 + 0.15e nd nd nd nd 4.40 + 0.12fg
L. nuda 0.22 + 0.01c 3.61 + 0.05f 0.87 + 0.02f nd nd nd 4.70 + 0.10f
L. perlatum 4.32 + 0.04a 6.75 + 0.13b 40.30 + 0.30a nd nd nd 51.40 + 0.20a
P. ostreatus nd 0.80 + 0.03j 0.56 + 0.02g nd nd 1.40 + 0.10jk
R. botrytis nd 3.84 + 0.12f nd 2.90 + 0.10c nd nd 6.80 + 0.20e
R. patagonica nd 2.54 + 0.04g nd 5.30 + 0.07b nd nd 7.80 + 0.10d
Open in a new tab

Table 6 shows the in vitro antioxidant activity of the studied species. Ramaria patagonica (156 µg/mL), R. botrytis (167 µg/mL), G. sordulenta (299 µg/mL), and A. vitellinus (551 µg/mL) presented the best results in the TBARS assays; meanwhile, L. perlatum (90 µg/mL), L. nuda (93 µg/mL), A. vitellinus (113 µg/mL), and G. sordulenta (155 µg/mL) presented the best results in OxHLIA, all with IC50 values ≤ 1000 µg/mL. The result of the antioxidant activity in OxHLIA for L. perlatum is in concordance with its highest total levels of phenolic compounds. That the antioxidant activity of mushrooms correlates with the phenolic compounds content has already been reported [62]. Fistulina antarctica comparatively presented the lowest antioxidant activity (IC50 of 2627 µg/mL for TBARS and of 1066 µg/mL for OxHLIA), in concordance with Toledo et al. [25]. Lepista nuda showed lower values (711 µg/mL) for the TBARS assay compared to those reported by other authors, with IC50 values of 5800 µg/mL [11] and 6100 µg/mL [25]. The high antioxidant activity of Ramaria is in agreement with the literature; for example, for R. flava, R. botrytis, and R. subaurantiaca with DPPH assays by Jacinto-Azevedo et al. [14], and for R. patagonica with different assays by Toledo et al. [25]. The antioxidant activity by DPPH or reducing the power test was also evaluated applying different extracting methodologies in Grifola samples; for example, Brujin et al. [63,64], using different solvents or heat treatments in Grifola gargal, and Postemsky et al. [65], using wheat grain biotransformed with mycelium of G. gargal and G. sordulenta. Among the three edible Rusulla species, R. integra ethanolic extract showed the best antihemolytic activity, with an IC50 value of 139 ± 3 μg/mL, also for a 60 min Δt [25]. This is the first study on the anti-hemolytic capacity of wild edible species.

Table 6.

Antioxidant activity of the mushroom extracts measured by inhibition of lipid peroxidation (TBARS) and the oxidative hemolysis inhibition assay (OxHLIA). IC50 values were expressed in µg/mL. na: no activity (Δt values less than 60 min were obtained). For each mushroom sample, means within a column with different letters differ significantly (p < 0.05).

Species TBARS OxHLIA
A. vitellinus 551.00 ± 9.00hi 113.00 ± 7.00i
C. magellanicus 688.00 ± 268.00hi Na
C. xiphidipus 1206.00 ± 200.00def 672.00 ± 9.00b
C. aegerita 2426.00 ± 50.00ab 202.00 ± 14.00g
C. hariotii 1468.00 ± 82.00cde Na
F. antarctica 2627.00 ± 189.00a 1066.00 ± 81.00a
F. endoxantha 1132.00 ± 8.00ef 335.00 ± 8.00de
F. pumiliae 1019.00 ± 20.00fg 285.00 ± 13.00ef
F. velutipes 1543.00 ± 100.00bcd 426.00 ± 53.00c
G. gargal 633.00 ± 15.00h 376.00 ± 17.00cd
G. sordulenta 299.00 ± 31.00ij 155.00 ± 7.00h
H. dusenii 610.00 ± 17.00h 220.00 ± 11.00g
L. nuda 711.00 ± 185.00gh 93.00 ± 6.00i
L. perlatum 1217.00 ± 564.00def 90.00 ± 4.00i
P. ostreatus 2052.00 ± 276.00abc Na
R. botrytis 167.00 ± 14.00j 249.00 ± 12.00fg
R. patagonica 156.00 ± 12.00j Na
Control/Trolox 18.40 ± 0.10k 21.80 ± 0.30j
Open in a new tab

All extracts were tested against ten bacteria and fungi considered food contaminants (Table 7). Each mushroom species showed different intensities of positive antimicrobial activity against the tested microorganisms. The antibacterial effects were more effective against Salmonella enterocolitica, Yersinia enterocolitica (Gram-negative bacteria), and Staphylococcus aureus (Gram-positive bacteria). The antifungal effect was more effective in Aspergillus brasiliensis. Among these active extracts, those produced by A. vitellinus (MIC 1.25 mg/mL) F. velutipes (MIC 2.5 mg/mL), G. gargal (MIC 2.5 mg/mL), P. ostreatus (MIC 2.5 mg/mL), and R. botrytis (MIC 1.25 mg/mL) exhibited a good inhibitory activity against Yersinia enterocolitica; and the extracts from G. sordulenta and R. botrytis (MIC 0.3 mg/mL) against Staphylococcus aureus. The Gram-negative bacteria, Enterobacter cloacae, Escherichia coli, and Pseudomonas aeruginosa, and the Gram-positive bacteria Bacillus cereus and Listeria monocytogenes were less sensitive to the extracts used. C. hariotii showed no activity against the analyzed bacteria. None of the extracts presented bactericidal and fungicidal activity.

Table 7.

Antimicrobial activity of all the extracts against selected food-contaminating bacteria and fungi. The maximum concentration used was 10 mg/mL. MIC: Minimum inhibitory concentration; MBC: Minimum bactericidal concentration; MFC: Minimum fungicidal concentration; n.t. not tested.

Positive Control
AV CM CX CA CH Streptomicin
1 mg/mL 		Methicilin
1 mg/mL 		Ampicillin
10 mg/mL
Antibacterial Activity MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC
Gram-negative bacteria
Enterobacter cloacae 10 >10 10 >10 10 >10 10 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Escherichia coli 5 >10 10 >10 10 >10 10 >10 >10 >10 0.01 0.01 n.t. n.t. 0.15 0.15
Pseudomonas aeruginosa >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 0.06 0.06 n.t. n.t. 0.63 0.63
Salmonella enterocolitica 2.5 >10 5 >10 5 >10 5 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Yersinia enterocolitica 1.25 >10 >10 >10 10 >10 >10 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Gram-positive bacteria
Bacillus cereus 10 >10 10 >10 10 >10 >10 >10 10 >10 0.007 0.007 n.t. n.t. n.t. n.t.
Listeria monocytogenes 10 >10 10 >10 >10 >10 >10 >10 >10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Staphylococcus aureus 1.25 >10 5 >10 0.6 >10 1.25 >10 10 >10 0.007 0.007 0.007 0.007 0.15 0.15
Ketaconazole
1mg/mL
Antifungal Activity MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC
Aspergillus brasiliensis 10 >10 2.5 >10 2.5 >10 2.5 >10 5 >10 0.06 0.125
Aspergillus fumigatus 0.07 0.15 0.07 0.15 0.07 0.15 >10 >10 >10 >10 0.5 1
Positive Control
FA FE FP FV GG GS Streptomicin
1 mg/mL 		Methicilin
1 mg/mL 		Ampicillin
10 mg/mL
Antibacterial Activity MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC
Gram-negative bacteria
Enterobacter cloacae 10 >10 >10 >10 10 >10 >10 >10 10 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Escherichia coli 10 >10 >10 >10 10 >10 >10 >10 >10 >10 10 >10 0.01 0.01 n.t. n.t. 0.15 0.15
Pseudomonas aeruginosa >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 0.06 0.06 n.t. n.t. 0.63 0.63
Salmonella enterocolitica 5 >10 10 >10 5 >10 5 >10 10 >10 5 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Yersinia enterocolitica 10 >10 10 >10 5 >10 2.5 >10 2.5 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Gram-positive bacteria
Bacillus cereus >10 >10 >10 >10 5 >10 5 >10 10 >10 >10 >10 0.007 0.007 n.t. n.t. n.t. n.t.
Listeria monocytogenes 10 >10 5 >10 10 >10 10 >10 10 >10 >10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Staphylococcus aureus 1.25 >10 0.6 >10 0.6 >10 0.6 >10 10 >10 0.3 >10 0.007 0.007 0.007 0.007 0.15 0.15
Ketaconazole
1 mg/mL
Antifungal Activity MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC
Aspergillus brasiliensis 2.5 >10 5 >10 2.5 >10 1.25 >10 5 >10 5 >10 0.06 0.125
Aspergillus fumigatus >10 >10 0.07 0.15 >10 >10 >10 >10 >10 >10 >10 >10 0.5 1
Positive Control
HD LN LP PO RB RP Streptomicin
1 mg/mL 		Methicilin
1 mg/mL 		Ampicillin
10 mg/mL
Antibacterial Activity MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC MIC MBC
Gram-negative bacteria
Enterobacter cloacae 10 >10 >10 >10 10 >10 >10 >10 10 >10 >10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Escherichia coli 10 >10 10 >10 >10 >10 5 >10 10 >10 10 >10 0.01 0.01 n.t. n.t. 0.15 0.15
Pseudomonas aeruginosa >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 >10 0.06 0.06 n.t. n.t. 0.63 0.63
Salmonella enterocolitica 5 >10 5 >10 10 >10 5 >10 5 >10 5 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Yersinia enterocolitica 5 >10 5 >10 >10 >10 2.5 >10 1.25 >10 5 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Gram-positive bacteria
Bacillus cereus 10 >10 5 >10 5 >10 >10 >10 10 >10 5 >10 0.007 0.007 n.t. n.t. n.t. n.t.
Listeria monocytogenes >10 >10 10 >10 5 >10 10 >10 >10 >10 10 >10 0.007 0.007 n.t. n.t. 0.15 0.15
Staphylococcus aureus 0.6 >10 0.6 >10 2.5 >10 0.6 >10 0.3 >10 2.5 >10 0.007 0.007 0.007 0.007 0.15 0.15
Ketaconazole
1 mg/mL
Antifungal Activity MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC MIC MFC
Aspergillus brasiliensis 1.25 >10 2.5 >10 2.5 >10 2.5 >10 5 >10 5 >10 0.06 0.125
Aspergillus fumigatus 0.07 0.15 >10 >10 >10 >10 >10 >10 >10 >10 0.07 0.15 0.50 1
Open in a new tab

In addition, A. vitellinus, C. magellanicus, C. xiphidipus, F. endoxantha, H. dusenii, and R. patagonica had fungistatic effects (MIC 0.15 mg/mL) against A. brasiliensis and A. fumigatus.

All these results must be considered taking into account the already established fact that the chemical composition of mushrooms could vary with the genetic structure and strains within the same species. Our ranks also considered dehydrated, complete fruiting bodies, in the mature stage, with no stratification by site conditions nor post-harvest treatments. Maturation stage at harvest, a specific part of the mushroom analyzed (stem, cup, lamellae), and environmental variables, such as soil composition, as well as the postharvest preservation method (freeze dry, oven-dry, cooled, fresh) and cooking process may affect their chemical composition [3].

4. Conclusions

This study highlights the value of the native and endemic mushrooms of the Patagonian forest, regarding, for example, their antioxidant qualities, as in the case of Ramaria spp., or their energetic value, as in the case of G. gargal and C. hariotti. Species such as C. aegerita, F. velutipes, L. nuda, and P. ostreatus demonstrated the importance of edible mushroom with a cosmopolitan distribution growing in native forests, resulting in an invaluable source of food with high protein values, low contents of fat, along with other bioactive compounds with remarkable antioxidant and antimicrobial activity. The data provided by this study, along with previous ones, will strengthen and support the inclusion of new species of wild edible fungi in the Argentine food code. In this way, we expect to revalue these resources as non-timber forest products from Patagonia, promoting multiple and sustainable uses of native forests.

Acknowledgments

Maximiliano Rugolo and Carolina Barroetaveña thank the National Scientific and Technical Research Council (CONICET) and Andean Patagonian Forest Research and Extension Center (CIEFAP) for funding the postdoctoral travel fellowship; and the National Parks of Argentina for the authorization to collect and transport the fungal material. Authors thank Viviana Salazar Vidal and Gabriela Gonzalez kindly permitted to use their photographs. The authors are grateful to the Foundation for Science and Technology (FCT, Portugal) for financial support by national funds FCT/MCTES (PIDDAC) to CIMO (UIDB/00690/2020 and UIDP/00690/2020) and SusTEC (LA/P/0007/2021). M.I. Dias and L. Barros are grateful for national funding from FCT; P.I., through the institutional scientific employment program contract. M. Añibarro-Ortega thanks FCT for his PhD studentship (2020.06297.BD). C. Caleja is thankful for her contract through the project Healthy-PETFOOD (POCI-01-0247-FEDER-047073).

Author Contributions

Conceptualization, C.B. and L.B.; methodology, M.R., R.M.S., M.I.D., T.C.S.P.P., M.A.-O. and C.C., experimental work, M.R., R.M.S., M.I.D., T.C.S.P.P., M.A.-O. and C.C., modelling and data analysis, M.R., M.I.D., T.C.S.P.P., M.A.-O. and C.C.; writing—original draft preparation, M.R., R.M.S., M.I.D., T.C.S.P.P., M.A.-O. and C.C.; writing—review and editing, L.B. and C.B.; supervision, C.C. and L.B. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Conflicts of Interest

The authors declare they have no conflict of interest.

Funding Statement

This work was supported by National Funds from Foundation for Science and Technology (FCT, Portugal) through project UIDB/00690/2020 and UIDP/00690/2020; and by National Scientific and Technical Research Council (CONICET, Argentina) through project PIP 11220170100982C and and Ministry of Science, Technology and Productive Innovation (PICT-2018-03234).

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Boa E. Non-Wood Forest Products. FAO; Rome, Italy: 2004. Wild edible fungi: A global overview of their use and importance to people; pp. 1–147. [Google Scholar]
  • 2.Guedes de Pinho P., Ribeiro B., Gonçalves R.F., Baptista P., Valentão P., Seabra R.M., Andrade P.B. Correlation between the pattern volatiles and the overall aroma of wild edible mushrooms. J. Agric. Food Chem. 2008;56:1704–1712. doi: 10.1021/jf073181y. [DOI] [PubMed] [Google Scholar]
  • 3.Barroetaveña C., Toledo C.V. Wild Plants, Mushrooms and Nuts: Functional Food Properties and Applications, Ferreira, I.C.F.R., Morales Gómez, P., Barros, L., Eds. Wiley-Blackwell; Chichester, UK: 2017. The nutritional benefits of mushrooms; pp. 65–82. [Google Scholar]
  • 4.Manzi P., Gambelli L., Marconi S., Vivanti V., Pizzoferrato L. Nutrients in edible mushrooms: An inter-species comparative study. Food Chem. 1999;65:477–482. doi: 10.1016/S0308-8146(98)00212-X. [DOI] [Google Scholar]
  • 5.Bobek P., Galbavy S. Hypercholesterolemic and anti-atherogenic effect of oyster mushroom (Pleurotus ostreatus) in rabbit. Nahrung. 1999;45:339–342. doi: 10.1002/(SICI)1521-3803(19991001)43:5&#x0003c;339::AID-FOOD339&#x0003e;3.0.CO;2-5. [DOI] [PubMed] [Google Scholar]
  • 6.Kalač P. A review of chemical composition and nutritional value of wild-growing and cultivated mushrooms. J. Sci. Food Agric. 2013;93:209–218. doi: 10.1002/jsfa.5960. [DOI] [PubMed] [Google Scholar]
  • 7.Lindequist U., Niedermeyer T.H., Jülich W.D. The pharmacological potential of mushrooms. Evid-Based Complement. Altern Med. 2005;2:285–299. doi: 10.1093/ecam/neh107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Zaidman B.Z., Yassin M., Mahajna J., Wasser S.P. Medicinal mushroom modulators of molecular targets as cancer therapeutics. Appl. Microbiol. Biotechnol. 2005;67:453–468. doi: 10.1007/s00253-004-1787-z. [DOI] [PubMed] [Google Scholar]
  • 9.Petrova R.D., Reznick A.Z., Wasser S.P., Denchev C.M., Nevo E., Mahajna J. Fungal metabolites modulating NF-kappa B activity: An approach to cancer therapy and chemoprevention (Review) Oncol. Rep. 2008;19:299–308. doi: 10.3892/OR.19.2.299. [DOI] [PubMed] [Google Scholar]
  • 10.Ribeiro B., Valentão P., Baptista P., Seabra R.M., Andrade P.B. Phenolic compounds, organic acids profiles and antioxidative properties of beefsteak fungus (Fistulina hepatica) Food Chem. Toxicol. 2007;45:1805–1813. doi: 10.1016/j.fct.2007.03.015. [DOI] [PubMed] [Google Scholar]
  • 11.Barros L., Venturini B.A., Baptista P., Estevinho L.M., Ferreira I.C.F.R. Chemical composition and biological properties of Portuguese wild mushrooms: A comprehensive study. J. Agric. Food Chem. 2008;56:3856–3862. doi: 10.1021/jf8003114. [DOI] [PubMed] [Google Scholar]
  • 12.Ferreira I.C.F.R., Barros L., Abreu R. Antioxidants in wild mushrooms. Curr. Med. Chem. 2009;16:1543–1560. doi: 10.2174/092986709787909587. [DOI] [PubMed] [Google Scholar]
  • 13.Reis F.S., Martins A., Barros L., Ferreira I.C.F.R. Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: A comparative study between in vivo and in vitro samples. Food Chem. Toxicol. 2012;50:1201–1207. doi: 10.1016/j.fct.2012.02.013. [DOI] [PubMed] [Google Scholar]
  • 14.Jacinto-Azevedo B., Valderrama N., Henríquez K., Aranda M., Aqueveque P. Nutritional value and biological properties of Chilean wild and commercial edible mushrooms. Food Chem. 2021;356:129651. doi: 10.1016/j.foodchem.2021.129651. [DOI] [PubMed] [Google Scholar]
  • 15.Wasser S. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl. Microbiol. Biotechnol. 2002;60:258–274. doi: 10.1007/s00253-002-1076-7. [DOI] [PubMed] [Google Scholar]
  • 16.Barros L., Falcao S., Baptista P., Freire C., Vilas-Boas M., Ferreira I.C.F.R. Antioxidant activity of Agaricus sp. mushrooms by chemical, biochemical and electrochemical assays. Food Chem. 2008;111:61–66. doi: 10.1016/j.foodchem.2008.03.033. [DOI] [Google Scholar]
  • 17.MAyDS . Segundo Inventario Nacional de Bosques Nativos. Ministerio de Ambiente y Desarrollo Sostenible de la Nación; Buenos Aires, Argentina: 2020. [(accessed on 24 May 2022)]. Informe Bosque Andino Patagónico. Available online: https://www.argentina.gob.ar/sites/default/files/informe_region_forestal_bosque_andino_patagonico_segunda_revision_0.rar. [Google Scholar]
  • 18.Gamundí I.J., Horak E. Hongos de los Bosques Andino-Patagónicos. Vázquez Mazzini Editores; Buenos Aires, Argentina: 1993. pp. 1–144. [Google Scholar]
  • 19.Barroetaveña C., Toledo C. Diversity and ecology of edible mushrooms from Patagonia native forests, Argentina. In: Perez-Moreno J., Guerin-Laguette A., Flores Arzú R., Yu F., editors. Mushrooms, Humans and Nature in a Changing World: Perspectives from Ecological, Agricultural and Social Sciences. 1st ed. Springer; Cham, Switzerland: 2020. pp. 297–318. [Google Scholar]
  • 20.Molares S., Toledo C.V., Stecher G., Barroetaveña C. Traditional mycological knowledge and processes of change in Mapuche communities from Patagonia, Argentina: A study on wild edible fungi in Nothofagaceae forests. Mycologia. 2020;112:9–23. doi: 10.1080/00275514.2019.1680219. [DOI] [PubMed] [Google Scholar]
  • 21.Valenzuela-Flores Hongos comestibles silvestres colectados en la X región de Chile. Boletín Micológico. 2003;18:1–14. doi: 10.22370/bolmicol.2003.18.0.374. [DOI] [Google Scholar]
  • 22.Toledo C.V., Barroetaveña C., Rajchenberg M. Phenology and environmental variables associated to the fruiting of wild edible mushrooms from Andean-Patagonia forests in Argentina. Rev. Mex. Biodiv. 2014;85:1093–1103. doi: 10.7550/rmb.40010. [DOI] [Google Scholar]
  • 23.Barroetaveña C., Toledo C.V. Hongos Silvestres Comestibles Novedosos en el Bosque Nativo y en las Plantaciones de Patagonia Andina, Argentina. Cienc. Investig. For. 2016;22:73–88. doi: 10.52904/0718-4646.2016.461. [DOI] [Google Scholar]
  • 24.González G.C., Barroetaveña C., Visnovsky S.B., Rajchenberg M., Pildain M.B. A new species, phylogeny, and a worldwide key of the edible wood decay Fistulina (Agaricales) Mycol. Prog. 2021;20:733–746. doi: 10.1007/s11557-021-01696-7. [DOI] [Google Scholar]
  • 25.Toledo C., Barroetaveña C., Fernandes A., Barros L., Ferreira I. Chemical and antioxidant properties of wild edible mushrooms from native Nothofagus spp. forest, Argentina. Molecules. 2016;21:1201. doi: 10.3390/molecules21091201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Kostić M., Ivanov M., Babić S.S., Petrović J., Soković M., Ćirić A. An up-to-date review on bio-resource therapeutics effective against bacterial species frequently associated with chronic sinusitis and tonsillitis. Curr. Med. Chem. 2020;27:6892–6909. doi: 10.2174/0929867327666200505093143. [DOI] [PubMed] [Google Scholar]
  • 27.Liu Y., Chen D., You Y., Zeng S., Li Y., Tang Q., Han G., Liu A., Feng C., Li C., et al. Nutritional composition of boletus mushrooms from Southwest China and their antihyperglycemic and antioxidant activities. Food Chem. 2016;211:83–91. doi: 10.1016/j.foodchem.2016.05.032. [DOI] [PubMed] [Google Scholar]
  • 28.Barroetaveña C., Pildain M.B. Review: Edible fungi for local development in the Patagonian Andes of Argentina. For. Syst. :2022. in press. [Google Scholar]
  • 29.Pérez-Moreno J., Mortimer P.E., Ku J., Karunarathna S.C., Li H. Global perspectives on the ecological, cultural and socioeconomic relevance of wild edible fungi. Stud. Fungi. 2021;6:408–424. doi: 10.5943/sif/6/1/31. [DOI] [Google Scholar]
  • 30.Rajchenberg M. Bibliotheca Mycologica Band 201, J. Cramer Verlag; Stuttgart, Germany: 2006. Polypores (Basidiomycetes) from the Patagonian Andes Forests of Argentina.300p [Google Scholar]
  • 31.Salgado Salomón M.E., Dresch P., Horak E., Galleguillos F., Barroetaveña C., Peintner U. The enigmatic Cortinarius magellanicus complex occurring in Nothofagaceae forests of the Southern Hemisphere. Fungal Biol. 2018;122:1077–1097. doi: 10.1016/j.funbio.2018.08.009. [DOI] [PubMed] [Google Scholar]
  • 32.Salgado Salomón M.E., Barroetaveña C., Niskanen T., Liimatainen K., Smith M.E., Peintner U. Loose ends in the Cortinarius phylogeny: Five new myxotelamonoid species indicate a high diversity of these ectomycorrhizal fungi with South American Nothofagaceae. Life. 2021;11:420. doi: 10.3390/life11050420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Rajchenberg M., Pildain M.B., de Errasti A., Riquelme C., Becerra J., Torres-Díaz C., Cabrera-Pardo J.R. Species and genera in Aleurodiscus sensu lato as viewed from the Southern Hemisphere. Mycologia. 2021;113:1264–1277. doi: 10.1080/00275514.2021.1940671. [DOI] [PubMed] [Google Scholar]
  • 34.Rugolo M., Barroetaveña C., Barrett M.D., Mata G., Hood I.A., Rajchenberg M., Pildain M.B. Phylogenetic relationships and taxonomy of Grifola (Polyporales) Mycol. Prog. 2022 accepted . [Google Scholar]
  • 35.González G., Barroetaveña C., Visnovsky S.B., Rajchenberg M., Pildain M.B. Diversity of the Genus Ramaria in the Patagonian andes Forests of Argentina. Mycol. Prog. 2022 submitted . [Google Scholar]
  • 36.AOAC . Official Methods of Analysis. 20th ed. Association of Official Analytical Chemists; Arlington, VA, USA: 2016. [Google Scholar]
  • 37.Barros L., Pereira C., Ferreira I.C.F.R. Optimized analysis of organic acids in edible mushrooms from Portugal by ultra fast liquid chromatography and photodiode array detection. Food Anal. Methods. 2013;6:309–316. doi: 10.1007/s12161-012-9443-1. [DOI] [Google Scholar]
  • 38.Pereira E., Barros L., Martins A., Ferreira I.C.F.R. Towards chemical and nutritional inventory of Portuguese wild edible mushrooms in different habitats. Food Chem. 2012;130:394–403. doi: 10.1016/j.foodchem.2011.07.057. [DOI] [Google Scholar]
  • 39.Vieira Junior W.G., Centeio Cardoso R.V., Fernandes A., Ferreira I.C.F.R., Barros L., Pardo-Giménez A., Soares D.M.M., Stevani C.V., Zied D.C. Influence of strains and environmental cultivation conditions on the bioconversion of ergosterol and vitamin D2 in the sun mushroom. J. Sci. Food Agric. 2021;102:1699–1706. doi: 10.1002/jsfa.11510. [DOI] [PubMed] [Google Scholar]
  • 40.Cardoso R.V.C., Carocho M., Fernandes A., Cunha Zied D., Cobos J.D.V., González-Paramás A.M., Ferreira I.C.F.R., Barros L. Influence of calcium silicate on the chemical properties of Pleurotus ostreatus var. florida (Jacq.) P. Kumm. J. Fungi. 2020;6:299. doi: 10.3390/jof6040299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Bessada S.M., Barreira J.C.M., Barros L., Ferreira I.C.F.R., Oliveira M.B.P.P. Phenolic profile and antioxidant activity of Coleostephus myconis (L.) Rchb. f.: An underexploited and highly disseminated species. Ind. Crop. Prod. 2016;89:45–51. doi: 10.1016/j.indcrop.2016.04.065. [DOI] [Google Scholar]
  • 42.Mandim F., Barros L., Calhelha R.C., Abreu R.M.V., Pinela J., Alves M.J., Heleno S., Santos P.F., Ferreira I.C.F.R. Calluna vulgaris (L.) Hull: Chemical characterization, evaluation of its bioactive properties and effect on the vaginal microbiota. Food Funct. 2019;10:78–89. doi: 10.1039/C8FO01910J. [DOI] [PubMed] [Google Scholar]
  • 43.Lockowandt L., Pinela J., Roriz C.L., Pereira C., Abreu R.M., Calhelha R.C., Alves M.J., Barros L., Bredol M., Ferreira I.C. Chemical features and bioactivities of cornflower (Centaurea cyanus L.) capitula: The blue flowers and the unexplored non-edible part. Ind. Crop. Prod. 2018;128:496–503. doi: 10.1016/j.indcrop.2018.11.059. [DOI] [Google Scholar]
  • 44.Pires T.C.S.P., Dias M.I., Barros L., Alves M.J., Oliveira M.B.P.P., Santos-Buelga C., Ferreira I.C.F.R. Antioxidant and antimicrobial properties of dried Portuguese apple variety (Malus domestica Borkh. Cv Bravo de Esmolfe) Food Chem. 2018;240:701–706. doi: 10.1016/j.foodchem.2017.08.010. [DOI] [PubMed] [Google Scholar]
  • 45.Heleno S.A., Ferreira I.C.F.R., Esteves A.P., Ćirić A., Glamočlija J., Martins A., Soković M., Queiroz M.J.R.P. Antimicrobial and demelanizing activity of Ganoderma lucidum extract, p-hydroxybenzoic and cinnamic acids and their synthetic acetylated glucuronide methyl esters. Food Chem. Toxicol. 2013;58:95–100. doi: 10.1016/j.fct.2013.04.025. [DOI] [PubMed] [Google Scholar]
  • 46.R Studio Team . RStudio: Integrated Development for R. RStudio. PBC; Boston, MA, USA: 2022. [(accessed on 2 July 2022)]. Available online: http://www.rstudio.com/ [Google Scholar]
  • 47.Schmeda-Hirschmann G., Razmilic I., Gutierrez M.I., Loyola J.I. Proximate composition and biological activity of food plants gathered by chilean Amerindians. Econ. Bot. 1999;53:177–187. doi: 10.1007/BF02866496. [DOI] [Google Scholar]
  • 48.Chang S.T., Miles P.G. Mushrooms: Cultivation, Nutritional Value, Medicinal Effect and Environmental Impact. 2nd ed. CRC Press; Boca Raton, FL, USA: 2004. pp. 27–52. [DOI] [Google Scholar]
  • 49.Richards A.B., Krakowka S., Dexter L.B., Schmid H., Wolterbeek A.P.M., Waalkens-Berendsen D.H., Shigoyuki A., Kurimoto M. Trehalose: A review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol. 2002;40:871–898. doi: 10.1016/S0278-6915(02)00011-X. [DOI] [PubMed] [Google Scholar]
  • 50.Reis F.S., Barros L., Martins A., Ferreira I.C. Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: An inter-species comparative study. Food Chem. Toxicol. 2012;50:191–197. doi: 10.1016/j.fct.2011.10.056. [DOI] [PubMed] [Google Scholar]
  • 51.Kölker S. Organic acid disorders. In: Aminoff M.J., Daroff R.B., editors. Encyclopedia of the Neurological Sciences. 2nd ed. Academic Press; London, UK: 2014. pp. 688–693. [Google Scholar]
  • 52.Puiggrós C., Chacón P., Armadans L.I., Clapés J., Planas M. Effects of oleic-rich and omega-3-rich diets on serum lipid pattern and lipid oxidation in mildly hypercholesterolemic patients. Clin. Nutr. 2002;21:79–87. doi: 10.1054/clnu.2001.0511. [DOI] [PubMed] [Google Scholar]
  • 53.Pacheco Y.M., López S., Bermúdez B., Abia R., Villar J., Muriana F.J.G. A meal rich in oleic acid beneficially modulates postprandial sICAM-1 and sVCAM-1 in normotensive and hypertensive hypertriglyceridemic subjects. J. Nutr. Biochem. 2008;19:200–205. doi: 10.1016/j.jnutbio.2007.03.002. [DOI] [PubMed] [Google Scholar]
  • 54.Sande D., Oliveira G.P., Moura M.A.F.E., Martins B.A., Lima M.T.N.S., Takahashi J.A. Edible mushrooms as a ubiquitous source of essential fatty acids. Food Res. Int. 2019;125:108524. doi: 10.1016/j.foodres.2019.108524. [DOI] [PubMed] [Google Scholar]
  • 55.Aires D., Capdevila N., Segundo M.J. Ácidos grasos esenciales su influencia en las diferentes etapas de la vida. Offarm Farm. Y Soc. 2005;24:96–102. [Google Scholar]
  • 56.Lv W., Xu D. Docosahexaenoic acid delivery systems, bioavailability, functionality and applications: A review. Foods. 2022;11:2685. doi: 10.3390/foods11172685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Martínez-Crovetto R. Estudios Etnobotánicos 4: Nombres de plantas y su utilidad, según los indios Onas de Tierra del Fuego. Bonplandia. 1968;3:1–20. doi: 10.30972/etn.032150. [DOI] [Google Scholar]
  • 58.Domínguez Díaz E. Flora de interés etnobotánico usada por los pueblos originarios: Aónikenk, Selk’nam, Kawésqar, Yagan y Haush en la Patagonia Austral. Dominguezia. 2010;26:19–29. [Google Scholar]
  • 59.Jasinghe V.J., Perera C.O. Distribution of ergosterol in different tissues of mushrooms and its effect on the conversion of ergosterol to vitamin D2 by UV irradiation. Food Chem. 2005;92:541–546. doi: 10.1016/j.foodchem.2004.08.022. [DOI] [Google Scholar]
  • 60.Espinosa N.A.Z., Velásquez J.M.A., González V.B., Blanco K.E.J., Maya G.C. Vitamin D: New paradigms. Med. Lab. 2011;17:211–246. [Google Scholar]
  • 61.Barros L., Dueñas M., Ferreira I.C.F.R., Baptista P., Santos-Buelga C. Phenolic acids determination by HPLC-DAD-ESI/MS in sixteen different Portuguese wild mushrooms species. Food Chem. Toxicol. 2009;47:1076–1079. doi: 10.1016/j.fct.2009.01.039. [DOI] [PubMed] [Google Scholar]
  • 62.Barros L., Baptista P., Correia D., Casal S., Oliveira B., Ferreira I.C.F.R. Fatty acid and sugar compositions and nutritional value of five edible mushrooms from Northeast Portugal. Food Chem. 2007;105:140–145. doi: 10.1016/j.foodchem.2007.03.052. [DOI] [Google Scholar]
  • 63.Bruijn J., Loyola C., Aqueveque P., Cañumir J., Cortéz M., France A. Influence of heat treatment on the antioxidant properties of Grifola gargal hydro-alcoholic extracts. Micol. Apl. Int. 2008;20:27–34. [Google Scholar]
  • 64.Bruijn J., Loyola C., Aqueveque P., Cañumir J., Cortéz M., France A. Antioxidant properties of extracts obtained from Grifola gargal mushrooms. Micol. Apl. Int. 2009;21:11–18. [Google Scholar]
  • 65.Postemsky P.D., Curvetto N.R. Enhancement of wheat grain antioxidant activity by Solid-state fermentation with Grifola spp. J. Med. Food. 2014;17:543–549. doi: 10.1089/jmf.2013.0108. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Articles from Foods are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)

RESOURCES