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Article

Content of Biogenic Amines and Physical Properties of Lacto-Fermented Button Mushrooms

by
Ewa Jabłońska-Ryś
1,*,
Aneta Sławińska
1,
Katarzyna Skrzypczak
1,
Dariusz Kowalczyk
2 and
Joanna Stadnik
3
1
Department of Plant Food Technology and Gastronomy, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
2
Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
3
Department of Animal Food Technology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(18), 8957; https://doi.org/10.3390/app12188957
Submission received: 10 August 2022 / Revised: 31 August 2022 / Accepted: 3 September 2022 / Published: 6 September 2022
(This article belongs to the Special Issue Fermentation Technology in Food Production)
Browse Figure
Versions Notes

Abstract

:
The aim of the study was to assess the content of biogenic amines and physical properties of fruiting bodies of white and brown button mushrooms subjected to the process of controlled lactic acid fermentation. Lactiplantibacillus plantarum 299v with documented probiotic properties and L. plantarum EK3, i.e., an isolate obtained from spontaneously fermented button mushrooms, were used as starter strains. Fresh, blanched, fermented, and refrigerated fruiting bodies were analysed. The mushroom samples were found to contain three amines: spermidine, putrescine, and tyramine in amounts that do not pose a threat to consumer health. The highest content of spermidine was found in the fruiting bodies of unprocessed brown and white mushrooms (367.22 ± 14.19 and 266.47 ± 13.38 mg/kg, respectively). Putrescine and tyramine were found only in the fermented mushrooms. Putrescine ranged from 0.58 ± 0.25 to 10.11 ± 0.5 mg/kg, while tyramine ranged from 1.44 ± 0.25 to 69.04 ± 1.39 mg/kg. Histamine, which is the most toxic biogenic amine, was not detected in any of the samples. The technological process caused substantial changes in all colour parameters. The blanching process resulted in a decrease in the value of parameter L* and an increase in the value of parameters a* and b*. The process of lactic acid fermentation increased the brightness parameter. It also caused a substantial increase in the yellowness parameter and reduced the redness of the fermented mushrooms. Blanching exerted a significant effect on the texture of the mushroom fruiting bodies, contributing to an increase in the puncture force value from 2.78 ± 0.22 to 4.90 ± 0.43 N and from 3.21 ± 0.23 to 5.59 ± 0.3 N in the case of the white and brown mushrooms, respectively. During the refrigerated storage, the firmness of the fermented mushrooms did not change.

1. Introduction

Fermented mushrooms are known and highly valued in many countries of Eastern Europe, Asia, and Africa [1,2,3,4]. Fruiting bodies of both wild and cultivated mushrooms are subjected to the fermentation process. The button mushroom is the most popular cultivated fungal species in Poland and one of the most commonly cultivated edible mushrooms in the world [5]. China is the leader in the global production of mushrooms, with the production estimated at 2314 million kg in 2019 [6]. Currently, approximately 60 species of Agaricus mushrooms can be found in Europe, but the most popular species is the button mushroom. There are two varieties available on the world market: the white button mushroom and the brown button mushroom. The latter differs from the classic white button mushroom not only in the colour, but also in the aroma and taste. With its organoleptic properties, it is gaining increasing popularity [7,8,9].
Mushrooms are available on the market as either fresh or processed (mainly vinegar-pickled) products [5]. Fermented mushrooms, which can be an alternative to pickled products, are currently impossible to buy. Nevertheless, they have been the subject of several research studies focused mainly on the optimisation of the technological process and, in particular, the assessment of the impact of starter cultures and the addition of sugar as a substrate for lactic bacteria (LAB) on the course of the fermentation process [10,11,12,13,14]. The effect of lactic acid fermentation on antioxidant properties, total content of phenolic compounds [15,16], and changes in the content of free sugars and organic acids [17] have been investigated as well [17]. The final products were subjected to sensory evaluation, and the high scores achieved suggest that fermented mushrooms may be accepted by potential consumers [16,17]. The most important features in the assessment of food product quality are, e.g., its physical properties, such as the colour and texture. Both these parameters change considerably during the food production process, mainly under the influence of high temperature and substrate pH [18].
Mushrooms are highly valued not only for their organoleptic qualities, but also for their nutritional value, content of bioactive compounds, and healing properties [5,19,20]. Fermentation is a preservation method that helps to retain the valuable properties of the raw material and often increases its nutritional value and the bioavailability of biologically active compounds [21,22]. The fermentation process also improves the health safety of food through the elimination or substantial reduction of the level of anti-nutritional factors and toxins [3,21,22,23,24]. However, the lactic acid fermentation process may increase the content of biogenic amines (BAs) in the fermented product. These nitrogenous compounds are generated through decarboxylation of amino acids or amination and transamination of aldehydes and ketones. They serve important functions in living cells, but large amounts of BAs (mainly histamine) supplied with food may be toxic. Biogenic amines are also precursors of carcinogenic N-nitroso compounds [25,26,27]. In food, amines are produced by bacterial enzymes (decarboxylases) converting amino acids into biogenic amines. Products with high protein content (a source of amino acids—BA precursors) as well as perishable and fermented products (presence of microorganisms and, more precisely, their enzymes—decarboxylases) are characterised by high content of BAs [27,28,29]. Edible mushrooms contain on average from 20 to even 40% of protein in dry matter.
The high protein content combined with the low dry matter level and high metabolic activity largely contribute to the low stability and rapid deterioration of mushroom fruiting bodies [5,19,30]. The content of BAs in the fruiting bodies of edible mushrooms varies considerably. The large variation in the content of these compounds is associated with many factors, e.g., the stage of maturity, storage conditions, or morphological part of the mushroom [31,32,33,34].
Fermented foods, in particular products obtained in the spontaneous fermentation process, are exposed to the generation of BAs. Some lactic acid bacteria (LAB) are able to convert amino acids into BAs through decarboxylase activity during the fermentation of various foodstuffs [23,35,36,37,38]. LAB strains used as starter cultures [36] may have this ability; hence, it is important to assess their properties in this respect.
To the best of our knowledge, there are currently no data on the content of biogenic amines in fermented mushrooms. The aim of the study was to determine the BA content and assess the physical properties of white and brown mushroom fruiting bodies subjected to the process of controlled lactic fermentation at the different stages of the technological process.

2. Materials and Methods

2.1. Chemicals, Reagents, and Standards

BA standards (spermidine—SPD, putrescine—PUT, tyramine—TYR, cadaverine—CAD, histamine—HIS, spermine—SPM, and agmatine—AGM), Na+/K+ citric buffer and ninhydrin were supplied by Ingos, Prague, the Czech Republic. Trichloroacetic acid (TCA) used for the preparation of samples was obtained from Merck, Darmstadt, Germany.

2.2. Raw Materials

Fruiting bodies of white and brown button mushrooms Agaricus bisporus were the study material. The mushrooms were grown on a fermented and pasteurised substrate based on straw, chicken manure, and gypsum with peat casing. They were purchased from producers and intended for further processing immediately after harvest (maximum after 4 h). Two strains of LAB used in a previous study [17]—Lactiplantibacillus plantarum 299v with documented probiotic properties (Probi AB, Lund, Sweden) and L. plantarum EK3, i.e., one of the isolates obtained from fermented button mushrooms in previous research [39]—were the starter cultures. The bacteria were propagated twice in MRS broth (Biocorp, Warsaw, Poland) and incubated (TK-2, Cabrolab, Warsaw, Poland) overnight at 30 °C. After centrifugation (MPW 350-R, MPW, Warsaw, Poland) at 1400× g for 10 min, microbial cells were harvested and washed twice in sterile 0.9% NaCl (P.O.Ch., Gliwice, Poland) before inoculation.

2.3. Preparation of Fermented Mushrooms

The fermentation procedure was based on a previous study [16], with some modifications. Fruiting bodies in the “closed cap” maturity stage with a diameter of 3.0–3.5 cm and stipes trimmed short were chosen for the fermentation process. The mushrooms were cleaned thoroughly to remove substratum debris, washed, and blanched in boiling water for 2 min. After cooling, 2% (w/w) NaCl and 1% (w/w) sucrose were added. The mushrooms were divided into portions of 380 g each and placed in 500 mL glass jars. Next, 120 mL of a solution containing 2% NaCl and 1% sucrose were added. Then, the starter cultures (probiotic L. plantarum 299v or L. plantarum EK3) were added at 107 CFU/g to the materials subjected to the fermentation process and the jars were closed. Lactic fermentation proceeded for 7 days at 21–22 °C; next, the fermented mushrooms were stored at 5 °C for 5 weeks for maturation.
Fresh and blanched samples, as well as mushrooms fermented for 7 days and stored for 5 weeks, were analysed. The samples were stored at −80 °C until the determination of biogenic amines, and the other analyses were performed on an ongoing basis.

2.4. Microbiological Analysis

The number of LAB in the brine during fermentation was measured according to PN-ISO 15214:2002 [40]. The counts were expressed as the log of colony-forming units (CFU) per millilitre of the sample. All measurements were performed in triplicate and expressed as a mean ± standard deviation (SD).

2.5. Determination of pH

The pH value during fermentation was measured in the brine using a digital pH meter (Seven Compact S210, Mettler Toledo, Greifensee, Switzerland). All measurements were performed in triplicate and expressed as a mean ± standard deviation (SD).

2.6. Determination of Biogenic Amines

Biogenic amines (BAs) were extracted from the mushroom samples with the method proposed by Rabie et al. [41], with some modifications. Three grams of a sample (fresh, blanched, and fermented mushrooms) were homogenized with 10 mL of 10% (w/v) trichloroacetic acid (TCA) in a homogenizer (IKAT10 basic ULTRA-TURRAX, Staufen, Germany) and shaken for 1 h in an orbital shaker (DragonLab, SK-330-Pro, Beijing, China). The samples were centrifuged at 1957× g for 15 min at 4 °C (MPW-350R, Warsaw, Poland). Supernatants were kept at −20 °C for 1 h and centrifuged again in the same conditions. Purified extracts were filtered through a 0.22 μm membrane filter (Alfachem, Poznań, Poland) and stored at 4 °C until analysis (maximally a few hours).
The analysis of BAs was performed using an AAA500 amino acid analyser (Ingos, Prague, Czech Republic) equipped with an Ostion LG AAA8 ion-exchange column (3.6 × 100.8 μm). Separation was performed by stepwise gradient elution using Na+/K+ citric buffers. Detection was carried out with the use of spectrophotometry at 570 nm after postcolumn derivatization with ninhydrin. The operating parameters were as follows: column temperature of 75 °C, eluent flow rate of 0.30 mL/min, reagent flow rate 0.20 of mL/min, reactor temperature of 120 °C, and sample volume of 100 mL [42]. The determination of BAs was confirmed by comparison of the retention times of biogenic amine standards with those of the components present in the samples. The determination of the BA concentrations was performed in triplicate and the values were expressed as mg/kg of mushroom samples.

2.7. Colour Analysis

The L* (whiteness or darkness), a* (greenness or redness), b* (blueness or yellowness) colour parameters of the mushrooms were determined using a 3Color K9000Neo spectrophotometer (3Color, Narama, Poland). The measurements were performed using a D65 light source and a standard colorimetric observer with a 10° field of view. The colorimeter was calibrated with respect to the white and black pattern. The measurements were carried out on the top layer of the mushroom caps. The colour analysis was performed in 15 replicates.

2.8. Texture Analysis

The firmness of the mushroom caps was determined with a penetration test, using a TA-XT2i texture analyser (Stable Micro Systems, Godalming, UK) equipped with a cylindrical probe of 2 mm diameter. The test speed and penetration were 1 mm/s and 5 mm, respectively. Firmness was determined from the force versus time curves as the maximum force (in N). The experiment was carried out in eight replicates.

2.9. Statistical Analysis

Statistical analysis was performed using the STATISTICA 13.1 program (StatSoft, Cracow, Poland), applying Tukey’s HSD test in the analysis of variance (ANOVA) to estimate the significance of the differences between the mean values at p < 0.05.

3. Results and Discussion

3.1. Changes in the pH Value and the Number of LAB during Mushroom Fermentation

The use of starter cultures is recommended in the process of lactic fermentation of the fruiting bodies of edible mushrooms. Most studies in this field were based on the use of L. plantarum strains as starter cultures [1]. The probiotic L. plantarum 299v strain and the L. plantarum EK3 isolate were used in the present study. The number of LAB introduced with the starter cultures was 7.08 ± 0.03 and 7.01 ± 0.05 log CFU/mL in the L. plantarum 299v and L. plantarum EK3 fermentation variants, respectively, in the white mushroom samples, and 7.11 ± 0.04 and 7.05 ± 0.03 log CFU/mL of L. plantarum 299v and L. plantarum EK3, respectively, in the brown mushroom samples (Figure 1a).
The highest number of LAB was recorded after the one-week fermentation time, i.e., 7.95 ± 0.05 and 8.63 ± 0.04 log CFU/mL in the L. plantarum 299v and L. plantarum EK3 variants, respectively, in the white mushroom samples, and 8.14 ± 0.05 and 8.53 ± 0.04 log CFU/mL, respectively, in the L. plantarum 299v and L. plantarum EK3 variants in the case of the brown mushroom samples. During the refrigerated storage period, the number of LAB systematically decreased and was within the range of 7.10–7.80 log CFU/mL on day 42 of the experiment. It was higher in the samples fermented with the EK3 isolate in both raw materials. As reported by Jabłońska-Ryś et al. [17], the probiotic 299v LAB population in the fermented white button mushrooms increased rapidly and reached a maximum on day 4 of the experiment, while the EK3 isolate reached the maximum count on day 2.
The pH value is an important indicator of the fermentation progress. As shown in Figure 1b, the initial pH value in all the experimental combinations was in a similar range of 6.72–6.78. During the first days of fermentation, the pH declined sharply and its value stabilised at a value below 4 (≤3.75) on day 7 of the experiment, which evidenced a correct course of the process. Similar values were recorded during the consecutive days of refrigerated storage of the samples. Slightly lower pH values in the final product were recorded in the white and brown button mushrooms fermented with the EK3 isolate (3.58 ± 0.05 and 3.53 ± 0.03, respectively) than in the 299v strain variant (3.65 ± 0.05 and 3.69 ± 0.04, respectively). This correlated with the amount of LAB present in the fermented product. Similar pH values were reported in previous studies on A. bisporus [15,16,17].
A low pH value indicates the production of large amounts of lactic acid in the lactic fermentation process, which has a considerable effect on the organoleptic characteristics and primarily determines the storability of fermented products.

3.2. Changes in the Content of Biogenic Amines during Mushroom Fermentation

Three of the seven analysed BAs were detected in the mushroom samples, i.e., spermidine, putrescine, and tyramine (Table 1). Spermidine was present in all samples, but the fresh mushrooms contained significantly higher content of this compound than the processed samples. The level of SPD in the fruiting bodies of the brown button mushrooms was significantly higher than in the white mushroom samples (367.22 ± 14.19 and 266.47 ± 13.38 mg/kg of mushroom samples, respectively). SPD and PUT are typical fungal polyamines usually occurring most abundantly in comparison with other BAs [31,34]. Spermidine exerts prominent cardioprotective and neuroprotective effects, stimulates anticancer immunosurveillance in rodent models, preserves mitochondrial function, exhibits anti-inflammatory properties, and prevents stem cell senescence. Increased polyamine levels, through enhanced dietary intake, are consistently linked to improved health and reduced overall mortality. In preclinical models, dietary supplementation with spermidine prolongs the life span and the health span [43,44,45]. As shown by the available literature data, fruiting bodies of A. bisporus contain from 43.45 to 4357.5 mg of spermidine per kg of fresh weight [26,31,32]. The BA content is determined by many factors, e.g., the maturity stage, harvesting method, storage conditions and duration, and morphological parts of mushrooms. Dadáková et al. [31] showed that the SPD content systematically increased during the growth and maturation of mushroom fruiting bodies, with its largest amounts in the spore-forming parts, compared to stipes and the other parts of caps. Tissue damage caused by, e.g., mechanical harvesting of fruiting bodies may contribute to an increase in the BA content through an increase in the activity of decarboxylating enzymes. The mushroom fruiting bodies used in the present experiment were harvested by hand after the caps reached a diameter of 3.0–3.5 cm (in the “closed cap” maturity stage) and processed immediately after harvesting.
The blanching process reduced the SPD content significantly to the level of 227.92 ± 16.94 and 296.02 ± 11.43 in the fruiting bodies of the white and brown mushrooms, respectively. Biogenic amines are reported to be heat-stable compounds; however, the thermal water treatment reduces their content to approximately 80%, as these compounds leach into water [46,47]. The fermentation process did not increase the SPD content in the analysed mushroom samples.
It was found that, regardless of the fermentation phase and the duration of the refrigerated storage, the fruiting bodies of the brown mushrooms contained significantly higher amounts of SPD than the white mushrooms. The type of the starter culture used did not differentiate the SPD content in the fermented product. No statistically significant changes in the content of this compound were observed during the refrigerated storage of the fermented mushrooms.
The presence of putrescine was detected only in the fermented samples. In the case of the white button mushrooms, the PUT content differed significantly depending on the type of the starter culture used and the duration of the experiment. The content of this compound in the variant fermented by the probiotic strain ranged from 6.93 ± 0.43 to 10.11 ± 0.5 mg/kg on days 7 and 42 of the experiment, respectively. The EK3 isolate contributed to production of a significantly lower amount of PUT. The putrescine content in this variant ranged from 0.58 ± 0.25 to 2.6 ± 0.0 mg/kg on days 7 and 42 of the experiment, respectively. No PUT was detected in the brown button mushrooms in the initial fermentation period. However, in the following period, the content of this amine ranged from 3.61 ± 0.5 to 4.62 ± 0.5 mg/kg and did not differ significantly depending on the starter culture or the refrigerated storage time. As shown by the available data on the presence of BAs in button mushroom fruiting bodies, the PUT content ranges from 0 to approximately 80 mg/kg [31,32,34,48,49]. As shown by Meng et al. [32], refrigerated storage of A. bisporus fruiting bodies induced the most pronounced changes in the PUT content, in comparison with other BAs. An approximately 10-fold and 40-fold increase in the content of this compound was observed after 7 and 21 days, respectively. Yen [47] found that the storage of Volvariella volvacea mushrooms at room temperature resulted in a higher increase in the PUT content than storage in refrigerated conditions.
The presence of PUT in fermented samples may indicate the ability of starter cultures to produce this amine. As reported by Karovičová and Kohajdová [50], Lactiplantibacillus spp. present in fermented food have the ability to produce PUT and TYR.
As in the case of PUT, no tyramine was detected in the fresh and blanched mushrooms. Similar results were obtained in an earlier study of the BA content in the fruiting bodies of fresh and processed mushrooms available on the Polish market [34]. As shown by Dadáková et al. [31], A. bisporus fruiting bodies contain small amounts of TYR, i.e., less than 2 mg/kg. In the case of the fermented button mushrooms analysed in the present study, TYR was detected only in the EK3 isolate-fermented samples. During the refrigerated storage, the content of this amine increased significantly from 1.44 ± 0.25 to 28.89 ± 3.93 mg/kg in the white mushroom samples, and from 36.98 ± 3.13 to 69.04 ± 1.39 mg/kg in the brown mushrooms on experimental days 7 and 42, respectively. The significantly higher content of TYR in the fermented brown mushrooms may be associated with the higher content of tyrosine, i.e., an amino acid which is a precursor of this compound. Paulauskiene et al. [51] analysed the chemical composition and nutritional values of white and brown A. bisporus and reported higher amounts of crude protein in the brown mushrooms. As shown by Bernaś [52], the content of amino acids in brown button mushrooms is 43–44% higher than that in white mushrooms. However, the author did not analyse the tyrosine content.
Histamine and tyramine are regarded as the most toxic BAs [28]. No histamine was detected in any of the analysed samples. It is currently the only amine whose content is subject to legal limits. However, the limits on the HIS content have only been established for fish and fish products, in which it should not exceed 100 and 200 mg/kg, respectively [53,54]. There are currently no such regulations for the other amines. The large discrepancy in the sensitivity to the presence of BAs causes difficulties in establishing limits for the content of these compounds in food. In normal conditions, BAs ingested with food are quickly detoxified by intestinal amine oxidases. These enzymes are classified as mono- (MAO) or diamine (DAO) oxidases. However, they may be genetically dysfunctional or BAs can enter the systemic circulation via ingestion of such inhibitors as alcohol or certain antidepressants and exert toxic effects on various organs. This poses a serious threat to human health [36]. As reported by El-Kosi et al. [55], the maximum content of histamine and tyramine in food products should range between 50 and 100 mg/kg and between 100 and 800 mg/kg, respectively. The EFSA (European Food Safety Authority) suggests that the consumption of 50 mg of histamine and 600 mg of tyramine by a healthy subject in one meal has no negative effects on human health. No limits have been proposed for putrescine and cadaverine, as there are no sufficient data available [56]. As reported by Til et al. [57], putrescine and spermidine oral acute toxicity, determined in Wistar rats, was observed at the level of 2000 (PUT) and 600 mg/kg body weight (SPD). The respective no-observed-adverse-effect levels (NOAEL) were 180 and 83 mg/kg body weight. Given these data, mushrooms fermented by L. plantarum 299v and EK3 can be regarded as the safest products in terms of the BA content.

3.3. Changes in Colour and Texture during Mushroom Fermentation

Colour is one of the most important quality traits of food. This feature changes substantially during the lactic acid fermentation process. Changes in the colour parameters induced by the fermentation of the mushroom fruiting bodies are presented in Table 2.
The cap colour parameters of the white and brown mushroom varieties differed significantly. The L*, a*, and b* values in the fresh fruiting bodies were 89.02 ± 2.55, 0.73 ± 0.43, and 12.8 ± 1.38 in the white mushrooms and 58.51 ± 2.85, 9.30 ± 0.55, and 16.21 ± 1.26 in the brown mushroom samples, respectively. As reported by Jaworska [58] based on results obtained by another author, the brightness of white mushrooms usually reaches values in the range of 80–85 or sometimes higher. Brightness (L*) is the most frequently described parameter in the assessment of the colour of A. bisporus fruiting bodies. It is particularly important in the case of the white variety, where the light colour of fruiting bodies (high value of the L* parameter) indicates a high degree of freshness [59]. The blanching process caused a significant decrease in the L* value to 74.91 ± 1.38 and 49.52 ± 5.34 in the white and brown mushroom samples, respectively. Concurrently, the values of parameters a* and b* increased substantially. As shown by Gałazka-Czarnecka and Krala [60], the blanching process results in approximately 10% deterioration of colour brightness. In turn, Jaworska et al. [58] have demonstrated that the deterioration of colour brightness in mushrooms blanched in food acid solutions may range from 9% to even 26%. The fermentation process caused considerable changes in all colour parameters. The value of the L* parameter increased, which is a favourable phenomenon in the case of white mushrooms. The fermented fruiting bodies of the brown variety were lighter in colour than the fresh ones as well. All the fermented samples exhibited a significant decrease in the redness value with a simultaneous high increase in the yellowness parameter. The colour parameters did not change substantially during the refrigerated storage time. In most cases, there were no significant differences between samples fermented by the different starter cultures. Liu et al. [61] subjected fruiting bodies of Pleurotus spp. to lactic fermentation and found a similar significant increase in the b* parameter caused by this process. However, opposite trends were observed in the case of the redness and brightness parameters. The Pleurotus fermentation process led to significant darkening of the fruiting bodies as well as a decrease in the L* value and an increase in the value of parameter a*. This was explained by the authors by the impact of enzymatic and non-enzymatic darkening reactions.
Firmness is an important textural property of fresh and processed mushrooms. Firmness is known to be related to cell turgor pressure, cell size, cell wall strength, and intercellular adhesion in cells [62]. This parameter was determined as the force required to puncture the cap tissue. The firmness of the fresh mushroom fruiting bodies differed significantly between the varieties. The maximum puncture force was 3.21 ± 0.23 N in the brown variety and 2.78 ± 0.22 N in the white button mushrooms (Table 2). In both cases, the values of this parameter increased significantly after the blanching process to 5.59 ± 0.3 N and 4.90 ± 0.43 N, respectively. These results are consistent with the findings reported by Zivanovic and Buescher [63], who analysed changes in mushroom texture induced by thermal processing. The authors showed that blanching caused a significant increase in the puncture force from 2.33 N in fresh mushrooms to 4.92 N in blanched fruiting bodies. They explained these findings by the significant decrease in the mass and volume caused by water loss during the blanching process with the associated reduction of intercellular spaces and, consequently, the tighter arrangement of hyphae in the cap tissue. As shown by Jaworska et al. [58], blanching has a detrimental effect on the texture of pilei, making them hard and rubbery. Despite its adverse effect on the texture and colour properties of mushroom fruiting bodies, the process of blanching should not be omitted. It leads to inactivation of enzymes, improves microbiological quality, and removes air from fungal tissues, which is important for the correct course of lactic acid fermentation [1]. In the present study, the fermentation of the mushroom fruiting bodies led to a decrease in their firmness, which was statistically significant in the case of the brown variety. There were no differences in firmness between samples fermented by the different starter cultures. Noteworthy, the value of this parameter was unchanged throughout the refrigerated storage period, which had a significant impact on the quality of the fermented product. Tissue softening, mainly caused by enzyme activity, is an important and common shortcoming of fermented vegetables [64].

4. Conclusions

Mushrooms should be regarded as potentially biogenic amine-rich food products. The lactic acid fermentation process has a significant impact on the content of these compounds. It is extremely important to use proven starter cultures to ensure that fermented mushrooms will be safe food products. No histamine, i.e., an amine that potentially poses the greatest threat to health, was found in the mushrooms fermented with the L. plantarum 299v and L. plantarum EK3 strains. Both fresh and processed mushroom cultivars contained the highest content of spermidine. Many recent research results indicate that spermidine-rich foods can be used in the treatment and prevention of age-related diseases. The determination of the role of mushrooms in the diet in this respect seems to be an interesting issue for further research.
The technological process applied in the study had an impact on the physical properties of the mushrooms, as it changed the colour parameters and tissue firmness significantly. The pretreatment blanching process appeared to be highly important, as it deteriorated the colour parameters and increased the puncture force. The process of lactic acid fermentation had a significant impact on the brightness parameter of mushroom fruiting bodies and increased the yellowness parameter in the colour structure. The refrigerated storage did not change the firmness of fermented mushroom fruiting bodies.

Author Contributions

Conceptualization, E.J.-R.; methodology, E.J.-R., A.S., D.K. and J.S.; software, J.S. and D.K.; validation, J.S., D.K. and K.S.; formal analysis, E.J.-R., A.S. and K.S.; investigation, E.J.-R. and A.S.; resources, E.J.-R. and K.S.; data curation, E.J.-R. and A.S.; writing—original draft preparation, E.J.-R. and A.S.; writing—review and editing, E.J.-R.; visualization, E.J.-R. and K.S.; supervision, E.J.-R.; project administration, E.J.-R.; funding acquisition, E.J.-R. All authors have read and agreed to the published version of the manuscript.

Funding

Project financed under the program of the Minister of Education and Science under the name “Regional Initiative of Excellence” in 2019–2023 project number 029/RID/2018/19 funding amount 11,927,330.00 PLN.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 08957 g001 550
Figure 1. Changes in the number of LAB (a) and the pH value (b) in the fermented mushrooms. W—white button mushroom; B—brown button mushroom; EK3, 299v—starter cultures.
Figure 1. Changes in the number of LAB (a) and the pH value (b) in the fermented mushrooms. W—white button mushroom; B—brown button mushroom; EK3, 299v—starter cultures.
Applsci 12 08957 g001
Table
Table 1. Content of biogenic amines in the mushrooms (mg/kg).
Table 1. Content of biogenic amines in the mushrooms (mg/kg).
Mushroom SamplesWhite Button MushroomsBrown Button Mushrooms
EK3 1299vEK3299v
Spermidine
F 2266.47 ± 13.38 aB 3266.47 ± 13.38 aB367.22 ± 14.19 bC367.22 ± 14.19 bC
B227.92 ± 16.94 aAB227.92 ± 16.94 aA296.02 ± 11.43 bB296.02 ± 11.43 bB
LF7202.22 ± 16.41 aA222.16 ± 14.04 abA246.72 ± 10.04 bcA265.07 ± 12.49 cAB
LF14200.08 ± 18.06 aA225.83 ± 11.19 abA242.13 ± 13.09 bA248.01 ± 19.31 bA
LF42213.82 ± 7.74 aA226.51 ± 5.48 aA259.71 ±15.9 bA265.3 ± 16.49 bAB
Putrescine
FND 4NDNDND
BNDNDNDND
LF70.58 ± 0.25 aA6.93 ± 0.43 bANDND
LF141.81 ± 0.13 aB8.38 ± 0.5 cB4.62 ± 0.5 bA3.61 ± 0.5 bA
LF422.6 ± 0.0 aC10.11 ± 0.5 cC4.48 ± 0.66 bA3.76 ± 0.25 bA
Tyramine
FNDNDNDND
BNDNDNDND
LF71.44 ± 0.25 aAND36.98 ± 3.13 bAND
LF1414.88 ± 2.54 aBND51.42 ± 2.46 bBND
LF4228.89 ± 3.93 aCND69.04 ± 1.39 bCND
1 EK3, 299v—starter cultures. 2 F—fresh sample; B—blanched sample; LF—lacto-fermented samples on days 7, 14, and 42 of the experiment. 3 Data represent mean ± SD of three replicates. Different lowercase letters in the same row and different capital letters in the same column indicate significant differences between mean values (p < 0.05). 4 ND—not detected.
Table
Table 2. Changes in mushroom colour and texture.
Table 2. Changes in mushroom colour and texture.
Mushroom SamplesWhite Button MushroomsBrown Button Mushrooms
EK3 1299vEK3299v
L*
F 289.02 ± 2.55 bC 389.02 ± 2.55 bC58.51 ± 2.85 aB58.51 ± 2.85 aB
B74.91 ± 1.38 bA74.91 ± 1.38 bA49.52 ± 5.34 aA49.52 ± 5.34 aA
LF779.03 ± 1.86 cB77.72 ± 1.54 cB65.19 ± 3.36 bD60.7 ± 2.55 aBC
LF1479.28 ± 2.33 bB78.18 ± 1.88 bB64.82 ± 3.61 aCD64.83 ± 4.16 aD
LF4280.08 ± 2.16 cB77.45 ± 1.74 bB60.93 ± 3.65 aBC63.44 ± 2.89 aCD
a*
F0.73 ± 0.43 aA0.73 ± 0.43 aA9.30 ± 0.55 bA9.3 ± 0.55 bA
B2.65 ± 1.03 aC2.65 ± 1.03 aB10.74 ± 0.9 bB10.74 ± 0.9 bB
LF71.95 ± 0.85 aBC1.82 ± 0.9 aB9.33 ± 1.54 bA9.37 ± 0.32 bA
LF141.82 ± 0.55 aB1.95 ± 0.9 aB10.1 ± 1.3 cAB8.59 ± 1.79 bA
LF421.75 ± 0.32 aB1.89 ± 0.79 aB9.95 ± 1.31 cAB8.76 ± 1.41 bA
b*
F12.8 ± 1.38 aA12.8 ± 1.38 aA16.21 ± 1.26 bA16.21 ± 1.26 bA
B18.56 ± 1.13 aB18.56 ± 1.13 aB19.22 ± 2.53 aB19.22 ± 2.53 aB
LF724.07 ± 2.65 aC25.43 ± 1.45 aC31.38 ± 2.38 cCD28.46 ± 1.91 bC
LF1423.8 ± 2.46 aC24.49 ± 1.36 aC32.98 ± 0.98 cD30.91 ± 0.91 bD
LF4224.8 ± 2.73 aC25.03 ± 1.45 aC29.68 ± 2.09 bC30.21 ± 1.51 bCD
Firmness (N)
F2.78 ± 0.22 aA2.78 ± 0.22 aA3.21 ± 0.23 bA3.21 ± 0.23 bA
B4.90 ± 0.43 aB4.90 ± 0.43 aB5.59 ± 0.3 bC5.59 ± 0.3 bC
LF74.75 ± 0.55 aB4.7 ± 0.64 aB4.97 ± 0.47 aB5.1 ± 0.44 aB
LF144.77 ± 0.49 aB4.74 ± 0.36 aB4.95 ± 0.64 aB5.14 ± 0.39 aB
LF424.69 ± 0.42 aB4.79 ± 0.41 aB4.86 ± 0.39 aB5.01 ± 0.3 aB
1 EK3, 299v—starter cultures. 2 F—fresh sample; B—blanched sample; LF—lacto-fermented samples on days 7, 14, and 42 of the experiment. 3 Data represent mean ± SD of eight (firmness) or fifteen (colour analysis) replicates. Different lowercase letters in the same row and different capital letters in the same column indicate significant differences between mean values (p < 0.05).
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Jabłońska-Ryś, E.; Sławińska, A.; Skrzypczak, K.; Kowalczyk, D.; Stadnik, J. Content of Biogenic Amines and Physical Properties of Lacto-Fermented Button Mushrooms. Appl. Sci. 2022, 12, 8957. https://doi.org/10.3390/app12188957

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Jabłońska-Ryś E, Sławińska A, Skrzypczak K, Kowalczyk D, Stadnik J. Content of Biogenic Amines and Physical Properties of Lacto-Fermented Button Mushrooms. Applied Sciences. 2022; 12(18):8957. https://doi.org/10.3390/app12188957

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Jabłońska-Ryś, Ewa, Aneta Sławińska, Katarzyna Skrzypczak, Dariusz Kowalczyk, and Joanna Stadnik. 2022. "Content of Biogenic Amines and Physical Properties of Lacto-Fermented Button Mushrooms" Applied Sciences 12, no. 18: 8957. https://doi.org/10.3390/app12188957

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