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Article

Volatile Profiling of Pleurotus eryngii and Pleurotus ostreatus Mushrooms Cultivated on Agricultural and Agro-Industrial By-Products

by
Dimitra Tagkouli
1,
Georgios Bekiaris
2,
Stella Pantazi
1,
Maria Eleni Anastasopoulou
1,
Georgios Koutrotsios
2,
Athanasios Mallouchos
3,
Georgios I. Zervakis
2 and
Nick Kalogeropoulos
1,*
1
Department of Dietetics-Nutrition, School of Health Science and Education, Harokopio University of Athens, El. Venizelou 70, Kallithea, 176 76 Athens, Greece
2
Laboratory of General and Agricultural Microbiology, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece
3
Department of Food Science and Human Nutrition, Agricultural University of Athens, Iera Odos 75, 11855 Athens, Greece
*
Author to whom correspondence should be addressed.
Foods 2021, 10(6), 1287; https://doi.org/10.3390/foods10061287
Submission received: 22 April 2021 / Revised: 1 June 2021 / Accepted: 2 June 2021 / Published: 4 June 2021
(This article belongs to the Special Issue Assessment of Food Quality and Authenticity Using Volatile Compounds)
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Abstract

:
The influence of genetic (species, strain) and environmental (substrate) factors on the volatile profiles of eight strains of Pleurotus eryngii and P. ostreatus mushrooms cultivated on wheat straw or substrates enriched with winery or olive oil by products was investigated by headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry (HS-SPME-GC-MS). Selected samples were additionally roasted. More than 50 compounds were determined in fresh mushroom samples, with P. ostreatus presenting higher concentrations but a lower number of volatile compounds compared to P. eryngii. Roasting resulted in partial elimination of volatiles and the formation of pyrazines, Strecker aldehydes and sulfur compounds. Principal component analysis on the data obtained succeeded to discriminate among raw and cooked mushrooms as well as among Pleurotus species and strains, but not among different cultivation substrates. Ketones, alcohols and toluene were mainly responsible for discriminating among P. ostreatus strains while aldehydes and fatty acid methyl esters contributed more at separating P. eryngii strains.

Graphical Abstract

1. Introduction

Mushrooms have been considered a delicacy for centuries, due to their distinct texture, aroma and exceptional flavor, while pertinent research evidenced unique nutritional and health-promoting benefits [1,2,3]. Mushrooms’ popularity steadily increased during the last decades, leading to a 30-fold increment of the world production of edible mushrooms, with Lentinus edodes and Pleurotus (“oyster”) spp. accounting for over 40% of the respective total supply [4]. Pleurotus (oyster) mushrooms are low energy, low fat, low sodium and cholesterol-free food items, being at the same time rich in proteins, minerals, functional polysaccharides like chitin and β-glucans, and water-soluble vitamins. In addition, they contain health-promoting bioactive microconstituents like ergosterol (provitamin D2), phenolic acids, the antioxidant amino acid ergothionein and lovastatin [5,6]. Currently, several species of Pleurotus are produced worldwide (e.g., P. ostreatus, P. pulmonarius, P. eryngii, P. djamor and P. citrinopileatus), by exploiting a wide range of lignocellulosic residues as substrates [7]. Of particular interest is their cultivation on olive mills and wineries by-products (i.e., materials that are difficult to manage due to their high content in organic compounds, notably lipids and polyphenolics), which is in line with the concepts of waste biodegradation and valorization [5,8].
Volatile compounds emitted by fungi are not only associated with key-functions related to growth physiology and mycelium interactions [9,10], but they also add to the quality of edible mushrooms [11,12]. They are additionally formed as a result of post-harvest processing, especially after thermal treatment [13,14]. The characteristic odor of mushrooms is the combined result of several groups of compounds, such as alcohols, aldehydes, ketones, acids, hydrocarbons, esters, and heterocyclic, aromatic and sulfur compounds [12,15,16,17]; their relative abundance may vary among species, strains, stage of growth and part of mushroom examined (i.e., cap, gills or stipe) [17,18,19,20].
More than 110 volatile compounds have been identified so far in mushrooms; among them, eight carbon (C8) compounds account for 44–97% of volatiles fraction, with 1-octen-3-ol, 3-octanol, 3-octanone, 1-octanol and 1-octen-3-one being detected in most cases [2,15,21,22]. In addition, of those identified only 3% are odor-active and can contribute to the aroma or flavor of foods [12,23].
Common laboratory methods for the isolation of aroma compounds include supercritical extraction, simultaneous distillation-extraction, dynamic headspace, and headspace solid phase microextraction (HS-SPME); the latter is an easy, rapid, relatively simple technique that allows the isolation and concentration of volatile analytes in a solvent free, environmentally friendly, manner [2,21,22,24]. Coupled with gas chromatography–mass spectrometry (GC-MS), HS-SPME is considered a powerful tool with high reproducibility and sensitivity [21,24,25,26,27].
In the present study, we investigated the influence of genetic (species, strain) and environmental (substrate) factors on the profile of volatile compounds produced by eight P. ostreatus and P. eryngii strains (four per species), which were cultivated on substrates composed of various agricultural and agro industrial by-products. The main objective was to verify whether a discrimination based on volatile aroma compounds was possible among species, strains and/or substrates. Volatiles were extracted from fresh fruit bodies with HS-SPME and analyzed by GC-MS. The same analytical scheme was applied to selected samples to assess the influence of cooking (roasting) on volatiles’ profiles.

2. Materials and Methods

2.1. Standards

Internal standard 4-methyl-1-pentanol was purchased from Sigma-Aldrich (Merck, Darmstadt, Germany), C8-C40 alkanes calibration standard for calculation of linear retention indices (RI) and a standard mixture of 37 fatty acid methyl esters (FAME) were obtained from Supelco (Supelco Inc., Bellefonte, PA, USA).

2.2. Biological Material and Mushroom Cultivation Substrates

The following Pleurotus eryngii and P. ostreatus strains were used for the purposes of this study: CS1, CS2, CS3 and LGAM106 for the former, and CS4, CS5, CS6 and LGAM3002 for the latter species. All strains are maintained in the Culture Collection of the Agricultural University of Athens (Laboratory of General and Agricultural Microbiology, Athens, Greece). Mushrooms were cultivated on three substrates consisting of (i) wheat straw (WS, as control), (ii) wheat straw in 1:1 w/w ratio with grape marc (GM), and (iii) olive leaves in 3:1 w/w ratio with two-phase olive mill wastes (OL). WS were obtained from the Thessaly region (central Greece), GM from a winery in the Nemea area (northeast Peloponnese, Greece) and OL from an olive-oil mill in Kalamata (southwest Peloponnese, Greece). Spawn and substrate preparation methodologies as well as mushroom cultivation conditions were as previously described [5,28].

2.3. Extraction of Aroma Volatile Compounds

Aroma volatile compounds were isolated by head space solid phase microextraction (HS-SPME) and identified and quantitated by GC-MS. For this purpose, immediately after harvest, approximately 50 g of fresh mushroom samples from each treatment (in triplicates) were wrapped in aluminum foil, sealed in plastic bags and kept at −40 °C until analysis, which was conducted within one week. Prior to analysis, samples were thawed, finely chopped and approximately 1 g was weighed into 15 mL screw capped glass vials (Supelco, Bellefonte, PA, USA), followed by the addition of 4 mL of saturated aqueous NaCl solution to inhibit enzymatic degradation and boost the release of volatiles [17,29] and 50 μL of internal standard (4-methyl-1-pentanol) methanolic solution (μg/mL). A magnetic stir bar was immersed in each vial, which was sealed with PTFE-faced/silicone septum (Supelco, Bellefonte, PA, USA). Sealed SPME vials were kept in a water bath at 40 °C, under magnetic stirring (250 rpm, Phoenix Instrument RSM-10 HS/HP, Garbsen, Germany) for 5 min to equilibrate. Then the SPME assembly was inserted, and fiber was exposed in the headspace and left to incubate for 40 min under continuous stirring. The volatiles were extracted with 50/30 μm divinylbenzene/carboxen/polydimethylsiloxane (DVB/CAR/PDMS) StableFlex fibers (Supelco Inc., Bellefonte, PA, USA), reported exhibiting good selectivity and high efficiency for the extraction of volatiles from wild and cultivated mushrooms [15,17,27,30,31,32]. They are additionally more selective for the identification of aldehydes such as methional and phenylacetaldehyde, considered important for mushroom flavor [32].

2.4. Gas Chromatography-Mass Spectrometry Analysis

An Agilent GC 6890N gas chromatograph (Waldron, Germany) coupled with HP5973 Mass Selective detector (electron impact 70 eV) and split—splitless injector, with a specific 0.75 mm i.d. liner provided by Supelco (Bellefonte, PA, USA) was used for volatiles profiling. Following incubation, the SPME assembly was removed from the vial and inserted into the GC injection port, where it remained for 20 min at 220 °C to desorb volatiles. The separation was achieved in a J&W 122-7032 DB-WAX column (30 m, 0.25 mm i.d., 0.25 μm film thickness). High purity helium was the carrier gas at a constant flow of 1.0 mL/min. GC operated in 1:1 split mode and mass detector operated at full scan mode covering 33–350 m/z mass range. The injector and transfer line temperatures were kept at 220 °C. The oven temperature program was: initial temperature 35 °C for 2 min, followed by a ramp of 20 °C /min to 100 °C, and finally 5 °C /min to 240 °C. The MS data were obtained by the mass detector operating at full scan in the range of m/z 35–350.

2.5. Identification and Semi-Quantification of Volatile Compounds

The identification of chromatographic peaks was performed by comparing the mass spectrum of each compound with the Wiley 275 (Wiley, New York, NY, USA) and NIST 98 (NIST MS search v6.1d) mass spectral databases. Further confirmation was performed by calculating the Kovats linear retention indices (RIs), using n-alkanes (C8–C40) standard (Supelco, Bellefonte, PA, USA) as external reference [33] and comparing the values obtained with those reported in the literature [34]. Among the compounds detected, only those exhibiting mass spectra matching qualities higher than 90% and their calculated RI did not differ by more than ±15 from the values available in public domain databases were included in the respective Table 1, Tables S1 and S2. For the aroma description of volatiles, “The Good Scents Company Information System” database was used [35]. Semi-quantification was performed based on the peak area and amount (μg) of the internal standard.

2.6. Cooking of Mushroom Samples

Cooking (roasting) of mushrooms was carried out in a domestic oven. For this purpose, approximately 100 g of fresh P. ostreatus LGAM3002 and P. eryngii CS3, cultivated on WS, were weighed, placed in clean Pyrex dishes and roasted at 180 °C for 10 min without aeration. The Pyrex dish was subsequently removed from the oven, covered with aluminum foil and allowed to cool for 5 min. Mushrooms were weighed before and after cooking to estimate water loss. Cooking procedure was conducted in triplicate. The pre-treatment and analysis of roasted samples was the same as that applied for the fresh ones.

2.7. Total Lipids Content

Mushrooms lipid content was measured in freeze-dried, pulverized samples by the colorimetric sulfo-phospho-vanillin reaction, employing commercial sunflower oil as lipid standard [36,37].

2.8. Statistical Analysis

Analyses were performed in triplicate and data are presented as mean ± standard deviation. Differences between means were established by one way analysis of variance (ANOVA) and Duncan’s t-test (p < 0.05) with the SPSS software (SPSS for Windows, version 21.0, SPSS Inc., Chicago, IL, USA). Principal component analysis (PCA) was performed on the entire volatile compounds profile set, as well as on the volatile compounds’ classes, to attain an overview of possible associations between volatiles and species/strains, raw and roasted mushroom samples and/or different cultivation substrates. Mean centering was only applied on the respective data sets. R-studio 1.0.136/R3.3.3 loaded with the “ade4” [38] and “adegraphics” [39] packages, were used for PCA.

3. Results and Discussion

3.1. Total Volatiles Contents

Overall, according to the criteria set at paragraph 2.5, more than 80 compounds were identified in mushrooms of the present study, with 24 of them detected only in roasted samples (Table 1). Fresh P. ostreatus mushrooms contained a lower number of volatile compounds compared to fresh P. eryngii ones (36 vs. 56 compounds). In accordance with our observation, Yin et al. (2019) [40] reported that P. ostreatus had the lower number of volatile compounds among six Pleurotus species. However, one should not overlook that the concentrations of volatile compounds alone are not a sufficient base for studying the aroma profile of mushrooms, as different volatile compounds may present significantly different odor thresholds [30].
Nevertheless, concentrations of the volatiles (i.e., compounds included in Table 2 and Table 3) were higher in P. ostreatus compared to P. eryngii (1684 ± 591 vs. 965.4 ± 321.5 μg/g f.w), in agreement with the data reported by Jung et al. (2019) [2]. The compounds detected in fresh samples are classified as aldehydes, alcohols, ketones, alkanes, fatty acid methyl esters (FAME) and terpenes. Moreover, the heterocyclic 2-pentyl-furan and the aromatic hydrocarbons toluene and ethylbenzene were also detected. Regarding the strains studied, P. eryngii LGAM106 and P. ostreatus CS5, CS6 and LGAM3002 presented the higher total volatiles content. In most cases, cultivation on GM and/or OL resulted in enhanced volatiles production however this pattern was not consistent (Figure 1).

3.2. Aldehydes

Fifteen aliphatic and aromatic aldehydes were identified in fresh Pleurotus samples, 12 of them in P. ostreatus and 14 in P. eryngii (Tables S1 and S2). Aliphatic aldehydes are biochemically derived from fatty acids, whereas the aromatic ones derive from amino acids [41]. Aldehydes confer a fresh, floral grassy and fatty aroma [17,29], and are characterised by low odor thresholds, i.e., they can be perceived even in small concentrations [40]. As a general trend, three out of four P. eryngii strains contained more volatile aldehydes than P. ostreatus strains, while this was also the case for mushrooms cultivated on WS and/or GM (Figure 1). Hexanal was the predominant aldehyde in both species (in accordance to the findings of a recent study [2]), followed by 2-octenal, n-octanal and 2-heptenal. P. eryngii contained three times more benzaldehyde than P. ostreatus (17.72 ± 11.17 vs. 5.58 ± 2.96 μg/g f.w.). According to Mau et al. (1998) [41], benzaldehyde was the major volatile compound in fruitbodies of P. eryngii. This aromatic aldehyde derives from the catabolism or oxidative degradation of phenylalanine [29,42,43] which is present in the Pleurotus mushrooms studied [44]. Benzaldehyde together with phenylacetaldehyde and short-chain aldehydes (pentanal, hexanal, octanal, nonanal, trans-2-heptenal) detected in the mushrooms studied (Table 1), are oxidative degradation products of oleic and linoleic acids; according to a recent report, they are among the major contributors of edible oil flavors during ambient storage [45]. Heptanal, 2-hexenal, phenylacetaldehyde, 2,4-nonadienal, and 2,4 decadienals were also present in the volatiles of both mushroom species, at slightly higher concentrations in P. eryngii; finally, nonanal, undecenal and 3-dodecenal were detected only in P. eryngii, while 2-phenyl-2-butenal was recorded only in P. ostreatus. The aldehydes identified in this study have been previously reported in several mushroom species [2,17,29,40].

3.3. Alcohols

Seven aliphatic and one aromatic alcohols were identified in fresh Pleurotus samples, (Tables S1 and S2; Figures S1 and S2), their overall concentration being almost double in P. ostreatus compared to P. eryngii (1200 ± 458 vs. 666.9 ± 252.3 μg/g f.w.). In all strains studied, 1-octen-3-ol, predominated, i.e., 650.7 ± 212.4 and 622.0 ± 225.2 μg/g f.w. in P. ostreatus and P. eryngii, respectively. 1-Octen-3-ol, the so called “mushroom alcohol” [46], is a key odor compound deriving from linoleic acid through oxygenation and subsequent cleavage of the respective hydroperoxide [47]. It is responsible for the earthy, green, oily, fungal aroma of mushrooms, identified as a major aroma compound in many mushroom species [2,17,40,46]. In addition, 3-octanol, 2-octen-1-ol, 1-octanol, 2-ethyl-1-hexanol, and hexanol were also detected in both species, while phenylethyl alcohol was found only in P. eryngii. Alcohols provide aromas, similar to those of aldehydes. Unsaturated alcohols have a lower odor threshold than the saturated ones, therefore they affect to a greater extent the overall aroma [40].

3.4. Ketones

Ketones are products of fatty acids metabolism [42,48]. In the present study seven aliphatic and one aromatic ketones were recorded in P. eryngii mushrooms but only four (3-octanone, 1-octen-3-one, 2,3-octanedione and 2-undecanone) in P. ostreatus strains; however, the latter contained a higher amount of ketones (266.9 ± 101.9 μg/g f.w. in P. ostreatus vs. 68.59 ± 20.60 μg/g f.w. in P. eryngii) (Table 2). Nonetheless, no clear and consistent distribution pattern is observed when the cultivation substrates are taken into account (Figure 1). Among the ketones detected, 3-octanone is predominant in both species at concentrations of 51.01 ± 15.44 and 249.9 ± 98.8 μg/g f.w. in P. eryngii and P. ostreatus, followed by 1-octen-3-one, 2-undecanone and 2,3-octanedione in lower concentrations, while acetophenone, 2-octanone, 6-methyl-5-hepten-2-one, and 3-octen-2-one were detected only in P. eryngii strains (Tables S1 and S2). Regarding their aromas, 3-octanone is described having a sweet, fruity, musty and lavender aroma [21], while 1-octen-3-one represents the dried-mushroom flavor imparting wet ground smell [40,49]. They both possess low odor detection thresholds, and are considered important contributors to the aroma of mushrooms [21,40]. The ketones detected in the present study have been reported among volatiles of various edible mushroom species [2,18,20,29,40,50,51].

3.5. Fatty Acid Methyl Esters (FAME)

FAME originate from fatty acids metabolism [42,48] and impart fatty and fruity aromas, with very low odor thresholds [17]. In the present study, seven FAME were identified in P. eryngii, and six in P. ostreatus, their total concentrations being 65.79 ± 40.31 vs. 13.91 ± 8.49 μg/g f.w., in line with their respective lipids content (7.29 ± 0.4 vs. 3.73 ± 0.2 mg/g f.w.). Methyl palmitate was the predominant FAME in both species (31.44 ± 20.62 vs. 6.02 ± 3.11 μg/g f.w. in P. eryngii and P. ostreatus) followed by methyl linoleate and methyl oleate (Tables S1 and S2). Methyl pentadecanoate, methyl laurate and methyl myristate were also detected at lower concentrations, while methyl stearate was found only in P. eryngii samples. There is a clear difference regarding the levels of FAME among the species studied since volatiles of P. eryngii strains contain more FAME than P. ostreatus (Figure 1). Regarding the influence of cultivation substrates, volatiles of P. eryngii mushrooms from OL and GM contained more FAME, whereas no clear pattern was evident in P. ostreatus (Figure 1). The FAME identified in this study have been reported in various Pleurotus spp. [51,52], Morchella importuna [17], Agaricus bisporus [27], and eleven wild edible mushrooms [31].

3.6. Alkanes

Alkanes confer woody, terpene and waxy aromas to mushrooms [17]. Thirteen alkanes were detected in volatiles of P. eryngii and five in P. ostreatus mushrooms, the most abundant being undecane (15.15 ± 4.26 vs. 18.03 ± 8.01 μg/g f.w.) (Tables S1 and S2). No specific trend regarding their distribution among species, strains or cultivation substrates was observed. The alkanes detected in the present study have been also identified in the volatiles of various mushroom species [17,19,27,40,50,52,53,54].

3.7. Terpenes

Three terpenes were identified in P. eryngii, but only one in P. ostreatus strains. The monoterpene limonene was present in three out of four P. ostreatus strains, at concentrations ranging from 0.09 ± 0.02 to 2.59 ± 1.27 μg/g f.w. in P. ostreatus and 0.34–0.45 μg/g f.w. in P. eryngii CS1 grown on GM and OL (Tables S1 and S2). Limonene has been reported in P. eryngii and P. cystidiosus [52] and other edible mushrooms, like Tricholoma matsutake [18,55], A. bisporus [19], various species growing in the wild [20], several truffles [53] and L. edodes [54]. The isoprenoid hydrocarbons pristane (2,6,10,14-tetramethylpentadecane) and phytane (2,6,10,14-tetramethylhexadecane) were detected in P. eryngii CS3 and LGAM106, cultivated on GM and OL at 3.92–15.46 μg/g f.w. (Table S1). Phytane has been also detected in hot water extract of tiger milk mushroom (Lignosus rhinocerus) [56], while no literature data concerning pristane in edible mushrooms were found. Terpenes confer a pleasant camphoric aroma as well as exotic fruit notes (e.g., immature mango fruit) [53].

3.8. Other Compounds—Toluene

The aromatic hydrocarbons toluene and ethylbenzene as well as the heterocyclic 2-pentylfuran, not belonging to the groups mentioned above, are discussed separately. Toluene was present in all strains of both species at 17.05 ± 8.11 vs. 104.5 ± 38.8 μg/g f.w. in P. eryngii and P. ostreatus, respectively. Toluene derives from unsaturated fatty acids and has been reported in wild edible species [15], freeze-dried truffle (Tuber aestivum) [57], and other food items like cooked beef [58,59] and fresh Mediterranean fish and shellfish [60]. Toluene exhibited a distinct distribution among Pleurotus volatiles, its concentrations being 3–13 times lower in P. eryngii when compared to P. ostreatus (Figure 1, Tables S1 and S2). Ethylbenzene was detected at low concentrations only in P. eryngii. It has been reported in food items like cooked beef [58] and fermented cucumbers [61] but—to the best of our knowledge—not in edible mushrooms. The heterocyclic compound 2-pentylfuran is formed by the autoxidation of linoleic acid [62]; its odor is described as green, earthy and meaty [17,40]. It was detected at low concentrations in P. eryngii and P. ostreatus (0.17–0.94 μg/g f.w.), and it did not exhibit any specific distribution pattern. It was identified in Pleurotus [40] and other edible mushrooms [2,15,17,50].

3.9. Eight-Carbon Compounds

Eight-carbon volatile compounds are major contributors to the characteristic flavor of many mushrooms [2,17,21,40,49]. They are oxidation products of linoleic acid via a 10-hydroperoxide intermediate [21,23,40] which represents 60.6–80.6% of fatty acids in P. eryngii and P. ostreatus [3,7]. They are classified as oxylipins and are involved in a wide range of biological processes [21]. Eight-carbon compounds predominated among the volatiles of all Pleurotus strains studied, comprising 78–83% and 84–91% of total volatiles in P. eryngii and P. ostreatus, following similar distributions with the total volatiles presented in Figure 1. Their concentrations were 776.5 ± 282.0 μg/g f.w. in P. eryngii and almost doubled in P. ostreatus (1498 ± 551 μg/g f.w.) (Table 2). In addition, 1-octen-3-ol predominated in all P. eryngii and in three out of four P. ostreatus strains, comprising 88–95% and 47–53% of eight-carbon compounds, respectively. Differences were observed among the Pleurotus strains studied: (a) three of the eight-carbon compounds detected in P. eryngii were absent from P. ostreatus, and (b) in three out of four P. eryngii strains, the second more abundant eight-carbon compound was 3-octanone followed by 2-octenal, while in three out of four P. ostreatus strains it was 3-octanol, followed by 3-octanone (Table 2).

3.10. Effect of Cooking on Volatiles’ Profiles

The volatile compounds determined in fresh and roasted mushrooms of P. eryngii strain CS3 and P. ostreatus strain LGAM 3002 cultivated on wheat straw are shown in Table 3. Besides water loss, roasting caused significant alterations in the volatiles’ profiles for both species. Overall, the number of volatile compounds decreased from 35 to 27 in roasted P. eryngii and increased from 35 to 41 in roasted P. ostreatus (Table 3). The percent abundance of volatile alcohols decreased by 65% and 77% in roasted P. eryngii and P. ostreatus, respectively; the same trend was followed by fatty acid methyl esters, which were almost eliminated (they decreased by 95% and 97% in roasted P. eryngii and P. ostreatus, respectively). Similarly, ketones, aldehydes and eight-carbon compounds decreased by 66%, 64% and 65% in P. eryngii and by 85%, 9.0% and 81% in P. ostreatus. Elimination of FAME during the freeze-drying of A. bisporus has been reported by Pei et al. (2016) [27].
In addition, roasting resulted in the formation of nitrogen-containing heterocyclic compounds (17 pyrazines, one pyrrole and one oxazole) and two sulfur compounds, i.e., substances with low odor threshold values, known to enrich food flavor with meat- or roast-like aromas [63]. The predominant compounds in roasted P. eryngii were 1-octen-3-ol (mushroom-like flavor), followed by hexanal (green and woody), toluene (sweet, solventy, woody, roasted coffee) and undecane (gasoline-like). In roasted P. ostreatus 1-octen-3-ol also predominated, followed by 3-octanol (mushroom, buttery), toluene, 3-octanone (mushroom, ketonic, cheesy) and 3-ethyl-2,5-dimethyl pyrazine (hazelnut, nutty). Several aroma compounds detected in fresh and cooked mushrooms originate from the enzymatic and oxidative decomposition of unsaturated fatty acids or from reactions between amino acids and carbonyl compounds, i.e., the Maillard reactions and the Strecker amino acid degradation which leads to the formation of Strecker aldehydes and other flavor-active compounds [48,64,65]. The extent of these transformations depends on the types of compounds involved, temperature, pH and reaction time [65,66,67]. Regarding the influence of temperature, the volatile compounds produced by lipid oxidation (aldehydes, ketones, and aromatic hydrocarbons like hexanal, octanal, benzaldehyde and toluene) are formed at relatively low temperatures, even at room temperature [45]; this provides an explanation for their presence in the fresh mushroom samples (Table 3). By contrast, Maillard and Strecker reactions take place at higher temperatures. Literature data consider temperatures around 120–130 °C as optimal for the formation of Maillard reaction products with favorable sensory characteristics [68] as well as for the formation of compounds with sulfur and nitrogen groups [69,70], e.g., pyrazines, Strecker aldehydes, dimethyldisulfide and pyrrole (detected in the roasted Pleurotus samples; Table 3). It is noteworthy that Pleurotus mushrooms contain significant amounts of Maillard reaction precursors, namely free amino acids, reported to comprise 37.1–41.6% of crude protein [44] and glucans, which comprise 40–50% w/w of the total content on a dry weight basis [71]. In addition, the Strecker aldehydes 2-methylbutanal, 3-methylbutanal, methional, phenylacetaldehyde and benzaldehyde, detected in the roasted samples (Table 3) derive from isoleucine, leucine, methionine and phenylalanine [67,72], i.e., amino acids that are present in the mushrooms studied [44].
Pyrazines are heterocyclic aromatic compounds, formed by the reaction between amines and dicarbonyl compounds through Strecker’s degradation [73,74]. They provide roasted, nutty flavor notes to the aroma of thermally-treated food products, even at very low amounts, because of their very low odor thresholds [75,76]. Strecker aldehydes and/or nitrogen heterocyclic compounds have been repeatedly identified among the volatiles of thermally-dried or heat-extracted samples of Pleurotus [42], Boletus edulis and P. ostreatus [77], A. bisporus [78], Hericium erinaceus [79], Boletus edulis [80], as well as in oils obtained from hydro distillation of Pleurotus mushrooms [51,52]. They were also present in cooked P. ostreatus [81], cooked wild mushrooms [15] and in A. bisporus soup [82]. Interestingly, Strecker aldehydes and/or pyrazines were also detected in freeze-dried M. importuna [17], dried L. edodes [54] fresh and freeze-dried truffles [29,57]. In the present study, six and 17 pyrazines were detected in roasted P. eryngii and P. ostreatus, with 3-ethyl-2,5-dimethyl pyrazine predominating at 8.76 and 21.22 μg/g f.w., followed by 2-ethyl-3,5-dimethylpyrazine, 2,5-dimethylpyrazine, 2-ethylmethylpyrazine and 3,5-diethyl-2-methylpyrazine at concentrations ranging between 2.9–6.0 μg/g f.w. (Table 3). Among the pyrazines determined in roasted Pleurotus mushrooms, 3-ethyl-2,5-dimethylpyrazine is formed from the thermal treatment of alanine [66], methylpyrazine, ethylpyrazine, 2-ethyl-methylpyrazine, and 2,6-diethylpyrazine originate from the thermal treatment of serine and 2,5-dimethylpyrazine, 2,6-dimethylpyrazine, and 2-ethyl-3,5-dimethylpyrazine from the thermal treatment of threonine [74]. Finally, ethyldimethylpyrazines, also detected in the roasted Pleurotus samples, originate from the Strecker degradation of methionine and are considered important flavor contributors in thermally processed foods [65]. Alanine, serine, threonine and methionine are among the amino acids reported in the Pleurotus mushrooms studied [44].
It is noteworthy that due to the absence of thermal treatments, pyrazines, pyrrole, oxazole and sulfur compounds were detected only in the cooked samples (Table 3); hence, the volatile profiles of fresh mushrooms obtained in the present study can be considered as representative, in some degree, of the P. eryngii and P. ostreatus aroma.
The sulfur compounds methional and dimethyl disulfide were detected in the roasted Pleurotus samples (Table 3). Methional is the Strecker aldehyde of methionine and is eventually decomposed to form dimethyl disulfide, which contributes further to the overall flavor development [65,67]. Methional is responsible for the aroma of cooked potatoes [67] and is the key aroma-active compound in cooked T. matsutake mushrooms [55], while both sulfur compounds were reported in A. bisporus soup [82].

3.11. Principal Component Analysis (PCA)

Principal component analysis (PCA) was performed on the entire volatile compounds profile of P. eryngii and P. ostreatus strains, in order to investigate the existence of any groupings or associations (Figure 2). The first two principal components, explaining 98% of the data set variance (i.e., PC1: 75.4% and PC2: 22.6%), allowed a clear discrimination of two Pleurotus species and eight strains studied (Figure 2a,b; ellipses drawn at a confidence level of 0.95).
However, due to the high number of identified compounds, it was impossible to acquire some additional information regarding the volatile compounds that were responsible for the species/strain discrimination through the interpretation of their loadings. Therefore, a PCA was performed on the basis of the volatile compounds’ classes, which revealed a clear separation at species and strain level (Figure 3a,b, respectively). Furthermore, the first two principal components explained an even higher percentage (98%) of the data set variance (i.e., PC1: 95.7% and PC2: 2.9%). Separation is taking place in both axes (PC1 and PC2), with P. eryngii strains mainly placed in the 4th quartile and P. ostreatus strains in the 2nd quartile. The observation of the loadings (i.e., the compound classes) revealed a positive effect of ketones, alcohols and toluene at separating P. ostreatus strains (Figure 3c). On the other hand, aldehydes and fatty acid methyl esters presented a stronger effect on the separation of P. eryngii strains. Both observations are in agreement with the previously determined content in volatile compounds for these particular species/strains.
PCA was also performed on the basis of volatile compounds’ classes for cooked (roasted) and raw (fresh) P. eryngii strain CS3 and P. ostreatus strain LGAM 3002 cultivated on wheat straw, to detect any groupings and to acquire additional information. The PCA allowed a clear discrimination of samples both in terms of species/strains as well as of the roasted/raw treatment (Figure 4a,b). As regards the latter, in particular, separation took place across PC1 (X-axis) with the fresh samples being placed on the negative side of PC1 and the roasted on the positive side. By examining the PCA loadings, it appears that pyrazines, sulfur compounds and toluene exert a significant role at separating the roasted samples. However, PCA was not able to discriminate mushrooms according to the cultivation substrate on the basis of the volatile compounds or compound classes studied (data not shown). This possibly indicates a low effect of the cultivation substrates on the mushrooms content in volatile compounds, contrary to the outcomes of our previous works regarding antioxidant properties and bioactive microconstituents like ergosterol, phenolic and terpenic compounds as well as free amino acids in the same mushroom species [5,44].

4. Conclusions

The aroma of Pleurotus mushrooms is formed by several classes of compounds namely alcohols, aldehydes, ketones, FAME, alkanes and terpenes. Fifty volatile compounds were identified in P. eryngii strains, while only 31 in P. ostreatus. However, in most cases, P. ostreatus presented a higher content in volatile alcohols, ketones and toluene compared to P. eryngii, whereas the opposite was established for aldehydes and FAME. Roasting of mushrooms caused partial elimination of existing volatiles and the formation of Maillard reaction and Strecker degradation products, mainly pyrazines, which contribute to the distinctive cooked-mushrooms aroma. Unsaturated alcohols and ketones containing eight carbon atoms predominated among the volatiles of both raw and cooked mushrooms. Principal component analysis performed on the aroma profiles data obtained succeeded in discriminating among Pleurotus species/strains and roasted/fresh samples, but not among mushrooms deriving from different cultivation substrates. The findings from the present work are interesting considering that previous studies on the same mushrooms revealed an influence of substrates on the antioxidant activity, β-glucans content and the levels of bioactive microconstituents like ergosterol, phenolic and terpenic acids, and free amino acids [5,45]. The extent to which the mushrooms organoleptic properties are affected by the choice of species/strains or the type of substrate needs to be further investigated by including the determination of additional compounds and/or sensory evaluation.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/foods10061287/s1, Table S1: Volatile compounds (μg/g f.w. equivalents of 4-methyl-2-pentanol) in the Pleurotus eryngii mushrooms cultivated on different substrates, Table S2: Volatile compounds (μg/g f.w. equivalents of 4-methyl-2-pentanol) in Pleurotus ostreatus mushrooms cultivated on different substrates (WS, GM and OL), Figure S1: Indicative GC/MS chromatogram of volatiles extracted by SPME from P. eryngii CS1 mushrooms cultivated on WS, Figure S2: Indicative GC/MS chromatogram of volatiles extracted by SPME from P. ostreatus CS4 mushrooms cultivated on GM.

Author Contributions

Conceptualization, N.K., A.M. and G.I.Z.; implementation of experiments, D.T., N.K., G.B., G.K., S.P. and M.E.A.; validation, D.T., G.B., G.I.Z., A.M. and N.K.; data analysis, D.T. and G.B.; writing—original draft preparation, D.T., G.B. and N.K.; writing—final draft preparation, D.T., N.K., G.B and G.I.Z.; review and editing, D.T., G.B., S.P., M.E.A., A.M., G.I.Z. and N.K.; supervision, N.K.; project administration, N.K. and G.I.Z.; funding acquisition, N.K. and G.I.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research has been co-financed by the European Union and Greek national funds (European Social Fund—ESF) through the Operational Program Competitiveness, Entrepreneurship and Innovation, under the call RESEARCH-CREATE-INNOVATE (project code: T1EDK-02560).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

There are no Data Availability Statements from the present study.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

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Foods 10 01287 g001a 550Foods 10 01287 g001b 550
Figure 1. Main volatile classes (μg/g f.w. equivalents of 4-methyl-2-pentanol) in eight strains of P. eryngii and P. ostreatus grown on three cultivation substrates. (A) Eight carbon atoms compounds, (B) aldehydes, (C) alcohols, (D) FAME, (E) ketones, (F) toluene. Abbreviations f.w.; fresh weight, n.d.: not detected, CS: commercial strains; LGAM: Laboratory of General and Agricultural Microbiology (Agricultural University of Athens, Greece); FAME: fatty acid methyl esters; WS: wheat straw; GM: wheat straw with grape marc (1:1 w/w); OL: olive leaves with olive mill wastes (3:1 w/w).
Figure 1. Main volatile classes (μg/g f.w. equivalents of 4-methyl-2-pentanol) in eight strains of P. eryngii and P. ostreatus grown on three cultivation substrates. (A) Eight carbon atoms compounds, (B) aldehydes, (C) alcohols, (D) FAME, (E) ketones, (F) toluene. Abbreviations f.w.; fresh weight, n.d.: not detected, CS: commercial strains; LGAM: Laboratory of General and Agricultural Microbiology (Agricultural University of Athens, Greece); FAME: fatty acid methyl esters; WS: wheat straw; GM: wheat straw with grape marc (1:1 w/w); OL: olive leaves with olive mill wastes (3:1 w/w).
Foods 10 01287 g001aFoods 10 01287 g001b
Foods 10 01287 g002 550
Figure 2. Score plot of principal component analysis and discrimination on the basis of the volatile compounds detected of Pleurotus mushrooms at (a) species and (b) strain level (Pos: P. ostreatus; Per: P. eryngii).
Figure 2. Score plot of principal component analysis and discrimination on the basis of the volatile compounds detected of Pleurotus mushrooms at (a) species and (b) strain level (Pos: P. ostreatus; Per: P. eryngii).
Foods 10 01287 g002
Foods 10 01287 g003 550
Figure 3. Score plot of principal component analysis and discrimination on the basis of classes of volatile compounds detected in Pleurotus mushrooms at (a) species and (b) strain level, as well as their (c) loadings. (Pos: P. ostreatus; Per: P. eryngii).
Figure 3. Score plot of principal component analysis and discrimination on the basis of classes of volatile compounds detected in Pleurotus mushrooms at (a) species and (b) strain level, as well as their (c) loadings. (Pos: P. ostreatus; Per: P. eryngii).
Foods 10 01287 g003
Foods 10 01287 g004 550
Figure 4. Score plot of principal component analysis and discrimination on the basis of classes of volatile compounds detected in fresh vs. roasted Pleurotus mushrooms at (a) species/strain level (P. ostreatus vs. P. eryngii) and (b) treatment (fresh vs. roasted) level, as well as their (c) loadings (Pos: P. ostreatus; Per: P. eryngii).
Figure 4. Score plot of principal component analysis and discrimination on the basis of classes of volatile compounds detected in fresh vs. roasted Pleurotus mushrooms at (a) species/strain level (P. ostreatus vs. P. eryngii) and (b) treatment (fresh vs. roasted) level, as well as their (c) loadings (Pos: P. ostreatus; Per: P. eryngii).
Foods 10 01287 g004
Table
Table 1. Names, classes, retention times (Rt) and retention indices (RIs) of volatile compounds identified by gas chromatography–mass spectrometry (GC-MS).
Table 1. Names, classes, retention times (Rt) and retention indices (RIs) of volatile compounds identified by gas chromatography–mass spectrometry (GC-MS).
NoClass of CompoundCompound NameRt (min)RIOdor Description
1Aldehyde2-methylbutanal *3.24908Musty, chocolate, nutty, furfural and isovaleraldehyde-like with malty and fermented nuances
2Aldehyde3-methylbutanal *3.29913Ethereal, aldehydic, chocolate peach, fatty
3Alkane1,3-octadiene3.75966
4Aldehydepentanal3.89977Diffusive, fermented, bready, fruity with berry nuances
5Aromatic compoundtoluene4.581048Sweet
6sulfur compounddimethyl disulfide *4.821071Sulfurous, vegetable, cabbage, onion
7Aldehydehexanal4.981087Green, fatty, leafy, vegetative, fruity, with a woody nuance
8Alkaneundecane5.111100Herbal, woody
9Aromatic compoundethylbenzene5.401129
10Ketone2-heptanone5.891178Cheese, fruity, ketonic, green banana, with a creamy nuance
11Aldehyden heptanal6.001189Green
12Heterocyclic compound2,4,5-trimethyloxazole *6.071196Nutty, roasted, wasabi, shellfish, mustard, vegetable
13Alkanedodecane6.111200
14Terpenelimonene6.161205Terpene, pine, herbal, peppery
15Aldehydetrans-2-hexenal6.371224Sweet, almond, fruity, green, leafy, apple, plum, vegetable
16Heterocyclic compound2-pentyl-furan6.471233Fruity, green, earthy beany with vegetable like nuances
17Ketone3-octanone6.751259Musty, mushroom, ketonic, moldy and cheesy fermented with a green, vegetative nuance
18Pyrazinemethylpyrazine *6.831267Nutty, cocoa, roasted, green
19Ketone2-octanone7.091291Musty, ketonic, bleu and parmesan cheese-like with earthy and dairy nuances
20Aldehydeoctanal7.141295Aldehydic, waxy, citrus orange with a green peely nuance
21Alkanetridecane7.191300
22Ketone1-octen-3-one7.291308Earthy, metallic, mushroom-like with vegetative nuances of cabbage and broccoli
23Internal standard4-methyl-1-pentanol7.401317
24Ketone2,3-octanedione7.501324Dill, asparagus, cilantro, herbal, aldehydic, earthy, fatty, cortex
25Pyrazine2,5-dimethylpyrazine *7.501324Nutty, peanut, musty, earthy, powdery and slightly roasted with a cocoa powder nuance
26Aldehyde2-heptenal7.601332Green, fatty
27Pyrazine2,6-dimethylpyrazine *7.691339Cocoa, roasted nuts, roast beef, coffee
28Ketone6-methyl-5-hepten-2-one7.721341Fruity, apple, musty, ketonic and creamy with slight cheesy and banana nuances
29Pyrazineethylpyrazine *7.751344Nutty, musty, fermented, coffee, roasted, cocoa and meaty nuances
30Pyrazine2,3-dimethylpyrazine *7.851352Musty, nut skins, cocoa powdery and roasted with potato and coffee nuances
31Alcohol1-hexanol7.891355Pungent, ethereal, fusel oil, fruity and alcoholic, sweet with a green top note
32Alcohol3-octanol8.421396Earthy, mushroom, dairy, musty, creamy, waxy with a slight fermented green minty nuance
33Alkanetetradecane8.471400Mild waxy
34Aldehydenonanal8.481401Waxy, aldehydic, citrus, with a fresh slightly green lemon peel like nuance, and a cucumber fattiness
35Pyrazine2-ethyl-methylpyrazine *8.591408Coffee bean, nutty, grassy, roasted
36Ketone3-octen-2-one8.711416Earthy, oily, ketonic, sweet, with hay and mushroom nuances
37Alkane3-ethyl-2-methyl-1,3-hexadiene8.911429
38Aldehyde2-octenal9.041437Fatty, green, herbal
39Pyrazine2,6-diethylpyrazine *9.121443Nutty, hazelnut
40Alcohol1-octen-3-ol9.271453Earthy, green, oily, vegetative and fungal
41Pyrazine3-ethyl-2,5-dimethylpyrazine *9.301455Potato, cocoa, roasted, nutty
42Sulfur compoundmethional *9.351458Creamy tomato, potato skin and French fry, yeasty, bready, limburger cheese with a savory meaty brothy nuance
43Pyrazine2-ethyl-3,5-dimethylpyrazine *9.521469Peanut, nutty, caramel, coffee, musty, cocoa, pyrazine and roasted
44Pyrazinetetramethylpyrazine *9.531470Nutty, musty and vanilla with dry, brown cocoa nuances
45Pyrazine2-methyl-5-propylpyrazine *9.711482
46Alcohol2-ethyl-1-hexanol9.891494Citrus, fresh, floral, oily, sweet
47Alkanepentadecane9.991500Waxy
48Pyrazine3,5-diethyl-2-methylpyrazine *10.071505Nutty, meaty, vegetable
49Pyrazine2,3,5-Trimethyl-6-ethylpyrazine *10.261516
50Aldehydebenzaldehyde10.561533Almond, fruity, powdery, nutty and benzaldehyde-like
51Pyrazine2,5-dimethyl-3-isobutylpyrazine *10.601535
52Pyrazine2-acetyl-5-methylfuran *10.921554Sweet, musty, nutty with a caramellic nuance
53Alcoholn-octanol11.061562Waxy, green, citrus, aldehydic and floral with a sweet, fatty, coconut nuance
54Alkanehexadecane11.721600
55Ketone2-undecanone11.811605Waxy, fruity, ketonic with fatty pineapple nuances
56Alcohol2-octen-1-ol12.111621Green, vegetable
57Pyrazine2-isoamyl-6-methylpyrazine *12.301631
58Aldehydephenylacetaldehyde12.591646Honey, floral rose, sweet, fermented, chocolate with a slight earthy nuance
59Pyrazinepyrazine,2-butyl-3,5-dimethyl *12.781657Sweet, earthy
60Ketoneacetophenone12.821658Sweet, cherry pit, marzipan and coumarinic, vanilla nuance
61Terpenepristane12.981667
62Pyrazine2,5-dimethyl-3-cis-propenylpyrazine *13.161677
63Alkaneheptadecane13.601700
64Aldehyde2,4-nonadienal13.741707Fatty, melon, waxy, green, leaf, cucumber, tropical fruit
65Aldehydeundecenal14.681756Fresh, fruity, orange peel
66Aldehyde3-dodecen-1-al14.681756Bitter orange, mandarin, coriander
67Aldehyde2,4-decadienal14.921768Acrid, greasy
68Terpenephytane15.031774
69Alkaneoctadecane15.531800
70FAMEmethyl laurate15.651806Waxy, soapy, creamy, coconut, with mushroom nuances
71Aldehyde2,4 decadienal15.811814Fatty, citrus, nutty
72Alkanen-nonadecane17.491900Bland
73Alcoholphenylethyl alcohol17.791916Sweet, floral, fresh and bready with a rosey honey nuance
74Aldehyde2-phenyl-2-butenal18.231939Musty, floral, honey, powdery and cocoa
75Heterocyclic compound2-acetylpyrrole *18.711964Musty, nutty-like with a coumarin nuance
76Alcohol1-dodecanol18.891973Earthy, soapy, waxy, fatty, honey, coconut
77Alkaneeicosane19.412000Waxy
78FAMEmethyl myristate19.642012Fatty, waxy, petal
79Aldehyde5-methyl-2-phenyl-2-hexenal20.642065
80Alkaneheneicosane21.302100
81FAMEmethyl pentadecanoate21.582116
82Alkanedocosane23.102200
83FAMEmethyl palmitate23.462221Oily, waxy, fatty, orris
84Alkanetetracosane26.862400
85FAMEmethyl stearate27.022413Oily, waxy
86FAMEmethyl oleate27.362440Mild, fatty
87FAMEmethyl linoleate28.152503Oily, fatty, woody
Compounds tentatively identified by Wiley 275 and NIST 98 mass spectral libraries; FAME: fatty acid methyl ester; *: identified in roasted samples.
Table
Table 2. (a) Classes of volatiles and toluene (μg/g f.w. equivalents of 4-methyl-2-pentanol) in P. eryngii (strains CS1, CS2, CS3 and LGAM106) mushrooms grown on different cultivation substrates (WS, GM and OL). (b) Classes of volatiles and toluene (μg/g f.w. equivalents of 4-methyl-2-pentanol) in P. ostreatus (strains CS4, CS5, CS6 and LGAM3002) mushrooms grown on different cultivation substrates (WS, GM and OL).
Table 2. (a) Classes of volatiles and toluene (μg/g f.w. equivalents of 4-methyl-2-pentanol) in P. eryngii (strains CS1, CS2, CS3 and LGAM106) mushrooms grown on different cultivation substrates (WS, GM and OL). (b) Classes of volatiles and toluene (μg/g f.w. equivalents of 4-methyl-2-pentanol) in P. ostreatus (strains CS4, CS5, CS6 and LGAM3002) mushrooms grown on different cultivation substrates (WS, GM and OL).
(a)
P. eryngii
CS1CS2CS3LGAM106
WSGMOLWSGMOLWSGMOLWSGMOL
Total *980.6 ± 134.3 a946.12 ± 171.9 a1220 ± 463 a527.8 ± 72.6 a611.6 ± 278.3 a446.3 ± 237.1 a805.0 ± 95.8 a967.9 ± 169.2 a1123 ± 274 a1268 ± 104 a1177 ± 83 a1512 ± 173 a
Alkanes8.98 ± 0.41 a17.79 ± 7.75 a17.97 ± 3.12 a16.69 ± 8.44 a13.25 ± 5.19 a20.99 ± 5.65 a16.82 ± 6.04 a29.83 ± 18.63 a26.09 ± 22.91 a9.84 ± 7.36 a51.34 ± 3.98b19.61 ± 6.78 a
Aldehydes198.1 ± 77.0 a160.6 ± 42.0 a115.0 ± 36.9 a69.21 ± 7.87 a57.40 ± 14.45 a45.57 ± 20.95 a158.3 ± 20.3 a155.6 ± 27.0 a98.86 ± 55.55 a196.2 ± 24.9 a131.8 ± 3.1 a111.3 ± 46.2 a
Alcohols611.9 ± 47.1 a590.9 ± 127.3 a896.4 ± 354.1 a353.1 ± 43.1 a449.2 ± 225.3 a325.7 ± 192.5 a508.8 ± 129.8 a598.9 ± 156.1 a790.0 ± 220.5 a904.6 ± 82.4 a798.4 ± 21.2 a1175 ± 114b
FAME56.07 ± 15.55 a58.02 ± 29.42 a79.88 ± 37.08 a22.09 ± 22.89 a25.48 ± 20.26 a13.80 ± 19.52 a39.49 ± 23.78 a91.32 ± 15.86 ab122.7 ± 46.5c40.25 ± 18.34 a128.3 ± 49.9 a118.5 ± 58.7 a
Ketones86.12 ± 9.38 a99.08 ± 30.40 a83.23 ± 35.87 a48.60 ± 15.47 a49.93 ± 26.42 a30.47 ± 14.40 a64.83 ± 1.44 a74.15 ± 17.03 a63.00 ± 14.96 a95.20 ± 14.68 b54.47 ± 1.91 a74.06 ± 17.55 ab
Furans0.56 ± 0.000.53 ± 0.11n.d.0.30 ± 0.08n.d.n.d.0.17 ± 0.020.33 ± 0.05n.d.0.49 ± 0.21n.d.n.d.
Toluene18.25 ± 3.35 a18.04 ± 12.40 a25.88 ± 11.05 a17.29 ± 2.03 a15.84 ± 9.03 a9.78 ± 4.61 a15.45 ± 4.20 a13.86 ± 5.93 a15.71 ± 6.96 a21.37 ± 16.34 a8.87 ± 0.00 a20.02 ± 4.12 a
Terpenesn.d.0.45 ± 0.210.34 ± 0.13n.d.n.d.n.d.n.d.13.72 ± 0.2726.64 ± 6.53n.d.3.99 ± 2.39n.d.
C8 compounds747.1 ± 68.3 a734.9 ± 157.0 a1033 ± 415 a414.7 ± 55.9 a509.2 ± 256.2 a363.5 ± 208.9 a623.3 ± 142.3 a715.1 ± 175.5 a906.6 ± 268.5 a1065 ± 59 ab894.9 ± 16.8 a1311 ± 164 b
(b)
P. ostreatus
CS4CS5CS6LGAM3002
WSGMOLWSGMOLWSGMOLWSGMOL
Total *814.0 ± 45.8 b1403 ± 52 c424.3 ± 45.0 a2232 ± 70 b2327 ± 23 b1986 ± 42 a2118 ± 75 a2159 ± 40 a1545 ± 547 a1436 ± 362 a2035 ± 217 a1728 ± 70 a
Alkanes15.21 ± 0.45 a11.80 ± 0.73 b9.91 ± 1.27 b31.01 ± 0.36 a26.29 ± 1.77 a27.83 ± 11.67 a27.66 ± 8.66 a11.91 ± 1.47 a23.74 ± 18.80 a10.75 ± 0.89 a27.59 ± 1.44 b24.00 ± 3.45 b
Aldehydes68.20 ± 6.27 b131.9 ± 2.1 a17.54 ± 0.33 c104.7 ± 5.8 b127.5 ± 3.2 c88.06 ± 1.26 a73.80 ± 7.47 a63.89 ± 0.73 a66.88 ± 11.21 a84.56 ± 6.57 a82.16 ± 14.05 a57.87 ± 3.45 a
Alcohols504.3 ± 29.8 b1018 ± 84 a263.9 ± 6.7 c1485 ± 20 b1689 ± 3 c1431 ± 3 a1647 ± 11 a1659 ± 19 a1058 ± 369 a1043 ± 303 a1475 ± 177 a1129 ± 21 a
FAME30.47 ± 2.70 a6.92 ± 0.41 b5.19 ± 0.68 b20.50 ± 2.50 a7.41 ± 1.54 b6.27 ± 0.08 b9.91 ± 0.35 a18.62 ± 0.44 b7.35 ± 1.74 a17.44 ± 9.62 a10.85 ± 1.29 a26.05 ± 2.79 a
Ketones130.4 ± 9.7 a168.5 ± 10.0 a68.19 ± 18.20 b391.6 ± 34.2 a351.8 ± 24.9 a331.1 ± 30.1 a244.7 ± 26.2 a294.0 ± 29.1 a298.1 ± 122.7 a228.9 ± 0.2 a309.1 ± 47.3 ab385.9 ± 62 c
Furansn.d.0.94 ± 0.44n.d.0.84 ± 0.64n.d.0.62 ± 0.15n.d.n.d.0.64 ± 0.450.47 ± 0.490.56 ± 0.14n.d.
Toluene65.30 ± 16.30 a65.30 ± 19.37 a59.51 ± 21.04 a194.0 ± 10.4 b123.5 ± 9.2 a98.86 ± 19.51 a114.1 ± 21.6 a110.4 ± 7.3 a90.37 ± 24.33 a99.15 ± 0.13 a126.1 ± 23.3 a104.6 ± 19.3 a
Terpenesn.d.n.d.n.d.3.75 ± 1.77 a2.22 ± 0.70 a1.79 ± 0.39 a0.09 ± 0.04n.d.0.19 ± 0.002.33 ± 0.02 ab4.01 ± 1.41 b0.44 ± 0.12 a
C8 compounds654.6 ± 21.1 b1253 ± 74 c323.0 ± 20.9 a1926 ± 54 b2087 ± 3 c1796 ± 27 a1912 ± 48 a1988 ± 51 a1376 ± 507 a1309 ± 322 a1818 ± 229 a1529 ± 50 a
*: corresponds to the sum of identified compounds listed in Table 1; Lack of letters in common indicates statistically significant differences (Duncan’s t-test. p < 0.05 in comparisons of treatment means between different substrates. Results are averages ± SD of three replicates. Abbreviations f.w.; fresh weight, n.d.; not detected, CS: commercial strains; LGAM: Laboratory of General and Agricultural Microbiology (Agricultural University of Athens, Greece); FAME: fatty acid methyl esters; WS, wheat straw; GM, wheat straw with grape marc (1:1 w/w); OL, olive leaves with olive mill wastes (3:1 w/w).
Table
Table 3. Volatile compounds (μg/g f.w. equivalents of 4-methyl-2-pentanol) in raw and roasted mushrooms of P. eryngii strain CS3 and P. ostreatus strain LGAM3002 cultivated on wheat straw.
Table 3. Volatile compounds (μg/g f.w. equivalents of 4-methyl-2-pentanol) in raw and roasted mushrooms of P. eryngii strain CS3 and P. ostreatus strain LGAM3002 cultivated on wheat straw.
Classes of Compounds RtP. eryngiiP. ostreatus
RawRoastedRawRoasted
Water content (%) 90.57 ± 1.9146.12 ± 2.890.95 ± 2.144.9 ± 3.1
Total lipids (mg/g f.w.) 7.29 ± 0.4--3.73 ± 0.2--
Total volatiles (μg/g f.w.) 924.2 ± 233.3398.1 ± 82.21165 ± 129364.7 ± 22.0
Alkanes undecane5.1125.88 ± 3.7917.07 ± 5.7616.98 ± 7.1012.39 ± 5.02
dodecane6.111.63 ± 0.12n.d.3.66 ± 3.65n.d.
pentadecane9.998.47 ± 0.46n.d.5.74 ± 4.90n.d.
hexadecane11.728.03 ± 1.06n.d.4.72 ± 3.14n.d.
heptadecane13.606.26 ± 0.78n.d.3.83 ± 2.37n.d.
octadecane15.535.61 ± 0.27n.d.3.15 ± 1.82n.d.
nonadecane17.495.42 ± 0.94n.d.1.92 ± 0.95n.d.
eicosane19.414.27 ± 0.39n.d.1.28 ± 0.36n.d.
Alcohols1-hexanol7.892.37 ± 0.24n.d.6.09 ± 5.51n.d.
3-octanol8.429.39 ± 7.276.32 ± 3.04330.6 ± 75.965.42 ± 26.73
1-octen-3-ol9.27491.6 ± 208.5178.3 ± 29.1 *341.4 ± 131.590.19 ± 16.59
2-ethyl-1-hexanol9.891.68 ± 0.340.99 ± 0.443.06 ± 1.44n.d.
1-octanol11.0623.26 ± 14.562.98 ± 1.229.47 ± 6.450.59 ± 0.03
phenylethyl alcohol17.791.83 ± 0.38n.d.n.d.n.d.
Aldehydes 2-methylbutanal3.17n.d.7.70 ± 9.16n.d.n.d.
3-methylbutanal3.29n.d.14.94 ± 2.35n.d.7.10 ± 1.55
pentanal3.89n.d.n.d.n.d.15.73 ± 6.19
hexanal4.9878.91 ± 25.5542.08 ± 27.1717.26 ± 7.815.50 ± 2.03
trans-2-hexenal6.371.59 ± 0.39n.d.0.39 ± 0.19n.d.
octanal7.148.04 ± 2.42n.d.4.89 ± 2.531.68 ± 1.10
2-heptenal7.6028.93 ± 15.73n.d.10.32 ± 1.61n.d.
2-octenal9.0442.12 ± 16.0015.47 ± 17.6614.89 ± 4.341.17 ± 0.14
benzaldehyde10.5615.40 ± 6.168.71 ± 4.573.60 ± 3.214.21 ± 1.62
phenylacetaldehyde12.59n.d.5.61 ± 2.88n.d.12.91 ± 6.05
2,4-nonadienal13.7411.13 ± 7.91n.d.1.53 ± 0.68n.d.
2,4-decadienal (E,E)15.812.92 ± 1.43n.d.1.73 ± 0.26n.d.
2-phenyl-2-butenal17.92n.d.n.d.n.d.1.87 ± 1.15
5-methyl-2-phenyl-2-hexenal20.64n.d.n.d.n.d.1.39 ± 0.79
FAMEmethyl laurate 15.65n.d.n.d.1.96 ± 0.11n.d.
methyl myristate19.643.21 ± 1.86n.d.2.50 ± 1.10n.d.
methyl pentadecanoate21.584.67 ± 3.45n.d.7.83 ± 5.64n.d.
methyl palmitate 23.4634.14 ± 33.472.06 ± 0.4813.29 ± 5.590.77 ± 0.27
methyl stearate27.021.49 ± 0.16n.d.n.d.n.d.
methyl oleate27.3621.11 ± 20.211.32 ± 0.182.31 ± 1.09n.d.
methyl linoleate28.1518.20 ± 15.981.52 ± 0.2210.67 ± 4.050.64 ± 0.25
Ketones2-heptanone5.95n.d.n.d.n.d.15.28 ± 13.38
3-octanone6.7536.80 ± 5.369.53 ± 5.71310.7 ± 125.325.08 ± 12.30
2-octanone7.094.68 ± 2.526.60 ± 2.21n.d.7.31 ± 9.03
2,3-octanedione7.50n.d.n.d.1.21 ± 0.37n.d.
3-octen-2-one8.717.04 ± 6.87n.d.n.d.n.d.
Aromatic compoundstoluene4.5814.22 ± 5.2660.73 ± 11.5090.62 ± 12.0527.20 ± 8.27
Pyrazinesmethylpyrazine6.83n.d.n.d.n.d.0.63 ± 0.18
2,5-dimethylpyrazine7.60n.d.4.33 ± 0.86n.d.5.44 ± 3.39
2,6-dimethylpyrazine7.69n.d.1.92 ± 1.14n.d.3.09 ± 1.94
ethylpyrazine7.75n.d.n.d.n.d.0.79 ± 0.51
2,3-dimethylpyrazine7.85n.d.0.89 ± 0.41n.d.0.78 ± 0.56
2-ethyl-methylpyrazine8.59n.d.3.69 ± 0.43n.d.4.45 ± 2.98
2,6-diethylpyrazine9.12n.d.n.d.n.d.1.76 ± 0.88
3-ethyl-2,5-dimethylpyrazine9.30n.d.8.76 ± 0.31n.d.21.22 ± 5.11
2-ethyl-3,5-dimethylpyrazine9.52n.d.2.85 ± 0.10n.d.6.00 ± 2.36
tetramethylpyrazine9.53n.d.n.d.n.d.0.56 ± 0.06
2-methyl-5-propylpyrazine9.71n.d.n.d.n.d.0.67 ± 0.25
3,5-diethyl-2-methyl pyrazine10.07n.d.n.d.n.d.5.94 ± 1.85
2,3,5-trimethyl-6-ethylpyrazine10.40n.d.n.d.n.d.2.40 ± 0.47
2,5-dimethyl-3-isobutylpyrazine10.60n.d.n.d.n.d.1.81 ± 0.51
2-isoamyl-6-methylpyrazine12.30n.d.n.d.n.d.2.00 ± 0.49
2-butyl-3,5-dimethyl pyrazine12.94n.d.n.d.n.d.4.49 ± 1.23
2,5-dimethyl-3-propenylpyrazine13.27n.d.n.d.n.d.1.15 ± 0.65
Sulfur compoundsdimethyl disulfide4.82n.d.n.d.n.d.2.67 ± 2.19
methional9.35n.d.1.96 ± 0.36n.d.2.59 ± 1.62
Terpeneslimonene6.165.21 ± 0.561.07 ± 0.410.30 ± 0.01n.d.
pristane12.980.18 ± 0.02n.d.4.32 ± 3.47n.d.
phytane15.03n.d.n.d.3.94 ± 1.49n.d.
Other heterocyclic compounds2,4,5-trimethyloxazole6.07n.d.n.d.n.d.1.72 ± 1.48
2-pentyl-furan6.474.43 ± 2.311.50± 0.321.05 ± 0.480.51 ± 0.36
2-acetyl-5-methylfuran10.92n.d.3.00 ± 0.45n.d.n.d.
2-acetylpyrrole18.71n.d.n.d.n.d.1.66 ± 0.56
* Results are presented as averages ± SD of three replicates; n.d.; not detected, CS: commercial strains; LGAM: Laboratory of General and Agricultural Microbiology (Agricultural University of Athens, Greece); FAME: fatty acid methyl esters.
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Tagkouli, D.; Bekiaris, G.; Pantazi, S.; Anastasopoulou, M.E.; Koutrotsios, G.; Mallouchos, A.; Zervakis, G.I.; Kalogeropoulos, N. Volatile Profiling of Pleurotus eryngii and Pleurotus ostreatus Mushrooms Cultivated on Agricultural and Agro-Industrial By-Products. Foods 2021, 10, 1287. https://doi.org/10.3390/foods10061287

AMA Style

Tagkouli D, Bekiaris G, Pantazi S, Anastasopoulou ME, Koutrotsios G, Mallouchos A, Zervakis GI, Kalogeropoulos N. Volatile Profiling of Pleurotus eryngii and Pleurotus ostreatus Mushrooms Cultivated on Agricultural and Agro-Industrial By-Products. Foods. 2021; 10(6):1287. https://doi.org/10.3390/foods10061287

Chicago/Turabian Style

Tagkouli, Dimitra, Georgios Bekiaris, Stella Pantazi, Maria Eleni Anastasopoulou, Georgios Koutrotsios, Athanasios Mallouchos, Georgios I. Zervakis, and Nick Kalogeropoulos. 2021. "Volatile Profiling of Pleurotus eryngii and Pleurotus ostreatus Mushrooms Cultivated on Agricultural and Agro-Industrial By-Products" Foods 10, no. 6: 1287. https://doi.org/10.3390/foods10061287

APA Style

Tagkouli, D., Bekiaris, G., Pantazi, S., Anastasopoulou, M. E., Koutrotsios, G., Mallouchos, A., Zervakis, G. I., & Kalogeropoulos, N. (2021). Volatile Profiling of Pleurotus eryngii and Pleurotus ostreatus Mushrooms Cultivated on Agricultural and Agro-Industrial By-Products. Foods, 10(6), 1287. https://doi.org/10.3390/foods10061287

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