Mushrooms are proven as a functional food due to their numerous beneficial effects on human health. Contemporary consumers purchase cultivated mushrooms that spend some time on the shelf, which makes it questionable whether this food can still be called “functional”. An examination was performed on selected characteristics of white and brown (Portobello) Agaricus bisporus stored in commercial (air) and three modified atmosphere packagings (MAP): high nitrogen, low carbon dioxide and low oxygen packaging. The amount of ascorbic acid decreased throughout 22 days for both varieties, especially in the white variety stored in commercial packaging. Similarly, total flavonoids decreased, although not to a significant degree. Metal chelating ability was pronounced throughout the storage period, with minor changes in the case of the brown variety. Diabetes-connected enzymes were inhibited by A. bisporus, while inhibition was significantly higher toward α-amylase. Nitrogen-rich packaging suppressed α-amylase and stimulated α-glucosidase in the white strain. Both the commercial packaging and the MAP samples exhibited changes in their functional characteristics over three weeks of cold storage. MAP, especially the low oxygen packaging, provided the best option for the preservation of the majority of functional characteristics examined in this research. Enzymes activities appeared to be more specifically tuned, and dependent on parameters not covered here. Brown variety was more resistant to environmental changes with respect to its functional characteristics.
Agaricus bisporus is one of the most widely cultivated mushroom species and comes to the fourth place based on the worldwide produced volume per year (15%) [1, 2]. However, the white button mushroom undergoes fast deterioration after its harvest and after one to three days at room temperature, it is no longer suitable for the market . Globally, 45% of all produced mushrooms go to the market as fresh, where in Europe it is almost doubled (80%), so it is not surprising that advanced technologies which diminish economical losses and prolong the mushroom's shelf life and quality are needed [4, 5]. In a review by Zhang et al.  there is an extensive look into the traditional methods with some novel modifications as well as into the contemporary industrial-scale solutions like modified atmosphere packaging, MAP, ultrasound or the electrolyzed water that can be applied to prolong the shelf life of mushrooms. Still, MAP is considered as the most efficient, easy to perform, and an economical method for fresh mushroom preservation.
The United States International Trade Commission has announced a rise of the mushroom market, especially the mushrooms stored in innovative packages . Another fact that has a strong influence on this market is the increase in the number of so-called “health consumers” who apprize the functional/medicinal benefits of food . Although white button mushroom is considered as a high-quality food that even positively affects cognitive function in humans and express anti-obesity activity , the inevitable deterioration of the fruit body during the shelf life must affect its functionality as well.
Most of the current studies are focused on sensory and nutritional changes that occur in mushrooms during the post-harvest period [8,9,10]. On the other side, A. bisporus possesses bioactive compounds with therapeutic properties , so it can be considered as a functional food. The question arises as to what happens to the functional characteristics of A. bisporus if stored for a long time? Moreover, how does the button mushroom functionality aspect change when stored in MAP?
Aiming to clarify the issues important for mushroom purchasing, especially as a part of the functional food market, this study explores several functional characteristics of white and brown (Portobello) A. bisporus when stored in three types of MAP during 22 days at the temperature of 4 °C. Namely, we tested the levels of ascorbic acid and flavonoids given the fact that they are common antioxidants in mushrooms . Based on the connection, and especially the correlation between antioxidant compounds and metal ion chelating ability, we also tested the Fe2+ chelation activity. Other methods for antioxidant activity evaluation such as 2, 2′-azinobis-(3-ethylbenzothiazoline-6-sulfonate radical scavenging activity was evaluated in our previous study . Recently, it was confirmed in animal studies that button mushroom might be beneficial in treating diabetes [14, 15]. Therefore, we examined in vitro changes in samples activity toward two diabetes-connected enzymes, α-amylase and α-glucosidase. Selected characteristics were followed for 22 days based on our previously published studies which tested a wide range of changes during shelf life and proved that prolonged MAP can positively affect the nutritional value as well as microbiological profile (safety) . Similar was observed by Gholami et al. . No pathogenic bacteria such as Clostridium botulinum has been found in our samples. To the best of our knowledge, this is the first study that screens changes of the selected functional characteristics of two types of A. bisporus stored in MAP.
Material and methods
Methanol, 2,6-dichlorphenolindophenol (DFIF), metaphosphoric acid, catechin, NaNO2, AlCl3, NaOH, FeSO4, ferrozine, EDTA, phosphate buffer (pH 7.5), DMSO, 4-nitrophenyl-α-D-glucopyranoside (PNPG), α-glucosidase (EC 184.108.40.206, from Saccharomyces cerevisiae), phosphate buffer (pH 6.0), α-amylase (EC 220.127.116.11, from Bacillus subtilis), 2-chloro-4-nitrophenyl-α-D-maltotrioside (CNP-G3) were purchased from Sigma Aldrich (St. Louis, MO, USA).
Mushrooms and packaging
In this study, freshly harvested fruit bodies of white button mushroom and the brown strain (Portobello) (A. bisporus, Italspawn, strains F599 and FB30, commercial varieties) were purchased from the same local producer in Belgrade, Serbia. All samples were cultivated using chicken litter-based compost (standardized), originated from the same growing tunnel, the same cycle, and were harvested during the first flush. A cap diameter was 30–70 mm. After being harvested, the mushrooms were transferred to a laboratory in a refrigerated vehicle and stored at 4 °C before packaging.
Only the carpophores free from defects (scars, blemishes, not whole, not healthy or good looking), were selected for the experiment. The characteristics of packaging material were: 85 mm thick (PA/PE/PE) bags, transmission rates of 60 mL O2, 12 mL N2, 180 mL CO2 m−2 d−1 atm−1, size of 200–300 mm. The bags were packed and sealed with a HVC-510 T/2A packaging machine. All bags were the same weight (250 g).
Active modified packaging conditions were: N2 (Gourmet N, 100% N2), CO2 (Gourmet N70, 30% CO2 and 70% N2) and O2 (30% O2 and 70% N2). All gas-combinationes were supplied by Messer Tehnogas (Belgrade, Serbia) as already prepared (food industry grade). Every first packaging was checked with gas analyzer (Oxybaby, Witt-Gastechnik GmbH & Co KG, Witten, Germany), while the last packaging was checked and verified to confirm that all conditions were as defined. Control sample contained only air to simulate the common commercial packaging. After being sealed, all packages were stored at 4 °C and relative humidity 95% for 22 days. Analyses were done on the 5th, 8th, 12th, 15th, 19th and 22nd day.
Mushroom samples were cut into thin slices and lyophilized (Christ BETA 2–8 LD plus freeze dryer, Osterode, Germany), powdered and subjected to methanol extraction. The solvent of choice (methanol) favors the extraction of compounds analyzed in this study and it is readily available. Sample (10 mg) was mixed with methanol (200 mL) and macerated for 24 h, on a magnetic stirrer (1 × g) at room temperature. Then, the material was filtered through Whatman No. 4 and the liquid portions were collected. The procedure was repeated three times and liquid parts were combined before low pressure evaporation (Büchi Rotavapor RII, Flawil, Switzerland) at 37 °C. The dry extracts were kept in the refrigerator at 4 °C before analysis. All results are expressed based on dry extract mass.
Ascorbic acid content
The method described by Barros et al.  was adjusted for a 96-well microplate assay. The extract (50 mg) was dissolved in 1% metaphosphoric acid (1 mL) and macerated for 20 min on a magnetic stirrer at room temperature. The sample was then centrifuged (six min, 18,000 × g) and an aliquot of the supernatant was mixed with 240 µL of DFIF. The absorbance was read after six min at 490 nm (Microplate reader Biohit ELx808, BioTek, Winooski, US; the same reader was used in all other methods) against a blank (sample with 1% metaphosphoric acid). All samples were analyzed in triplicates and calculated based on the standard curve of L-ascorbic acid (concentration range: 0.03125–0.25 g L−1). The results are expressed as g kg−1 of ascorbic acid (based on dry extract mass).
Total flavonoid content
Quantification of total flavonoids in mushroom samples was done based on colorimetric microplate assay . The mushroom extract (5 g) was dissolved in methanol and added to the microplate well in the amount of 25 µL. After the addition of 125 µL of redistilled water and 7.5 µL of 5% NaNO2 the mixture was incubated for five min at room temperature. Then, 15 µL of 10% AlCl3 were added and the plate was incubated for another 5 min at room temperature. Finally, 50 µL of 1 M NaOH and 27.5 µL of redistilled water were added and the absorbance (510 nm) was measured immediately. Prior to the absorbance reading the microplate was mixed for 10 s. Similarly, a blank was prepared by adding methanol instead of the mushroom extract solution. Standard catechin solutions (0.0625–2 g L−1) were used to construct the standard curve. The results are expressed as mean ± standard deviation (g kg−1 catechin equivalents). All measurements were performed in triplicates.
Fe2+ chelation ability
The ability of mushroom samples to chelate Fe2+ ion was tested based on microplate assay by Santos et al. . 160 µL of redistilled water together with 20 µL of 0.3 mM FeSO4 were added to the mushroom extract (5 mg) dissolved in methanol, and incubated for five min. Then, 30 µL of 0.8 mM ferozine solution were added. The plate was then incubated for 15 min at room temperature and the absorbance was measured at 490 nm against a blank (sample contained all components except the mushroom extract, which was replaced with methanol). The results are expressed as % of Fe2+ chelation. The measurements were performed in triplicates.
α-amylase inhibitory activity
In-vitro α-amylase inhibition assay adjusted for microplates was conducted according to the previously described method . The mushroom extract was dissolved in 5% DMSO and 10 µL of its solution were added into the plate as well as 90 µL of phosphate buffer (0.1 M, pH 6.0, containing 0.02% NaN3). The next step was the addition of 80 µL of enzyme solution prepared in phosphate buffer (the concentration of α-amylase in the microplate well was 0.05 U mL−1). At the end 20 µL of CNP-G3 were added. The reaction was monitored throughout 30 min at a wavelength of 405 nm; the value was recorded every three min. The ability of mushroom samples to inhibit α-amylase was calculated based on equation:
In-vitro α-glucosidase inhibitory activity
A microplate assay described by Kirakosyan et al.  was used to determine the A. bisporus ability to inhibit α-glucosidase. 90 µL of 0.1 M phosphate buffer (pH 7.5) and 10 µL of the mushroom extract sample dissolved in methanol were added into the microplate. The enzyme was then added (80 µL) so that its concentration in the well was 0.08 U mL−1 followed by the addition of PNPG (20 µL). The colorimetric reaction was followed for 35 min with reading on every 30 sek at 405 nm. The results were calculated according to the same equation as above:
All measurements were performed in triplicates and the results were given as mean values ± standard deviation. Statistica software 12.0 (Statistica, Tulsa, OK, SAD) was used for data processing: one-way analysis of variance and Tukey’s HSD post hoc test (p < 0.05).
Results and discussion
Ascorbic acid content
The level of ascorbic acid in both A. bisporus strains is presented in Table 1. The white variety contained a significantly higher level of ascorbic acid (1.28–5.51 g kg−1 ascorbic acid) followed by brown (0.54–1.88 g kg−1 ascorbic acid) throughout the whole storage period. Barros et al.  reported much lower contents (0.02–0.04 g kg−1 of extract), while others obtained higher results but for fresh or dry samples, and not extracts. The difference in the amount of ascorbic acid has already been noticed in mushrooms and is ascribed to factors such as geographical origin, maturity stage, genotype and climate conditions .
Generally, mushrooms are not considered as rich sources of ascorbic acid. However, fungi produce erythroascorbate, an analog of ascorbate through of at least three biosynthetic pathways which point to its physiological role for the mushroom itself [20,21,22]. According to Georgiou et al. ascorbate caused a reduction of lipid peroxidation in a sclerotial strain of fungi, being a mechanism of oxidative stress defense . And although present in amounts that are not especially high, vitamin C act as a synergist for other antioxidants thus adding to a mushroom’s contribution to a functional diet for humans .
The modified atmosphere induced a significant lowering in ascorbic acid level in the first week of the storage in both strains, a fact also reported by Li and Zhang . At the same time, white A. bisporus packed in commercial package (filled with air) resisted this trend, but only for a short period. An elevated concentration of O2, N2, and CO2 generated a stress-environment that disturbed normal metabolism and forced the fruit bodies to activate its reactive oxidative species-defense mechanism. The O2 and N2 MAP were particularly stressful for the first eight days of cold storage. Interestingly, in the second week of the storage, a very pronounced increase in ascorbic acid concentration was observed in all packagings with the white strain, and especially in the mushrooms packaged inr MAP with CO2 and O2. This increase was present but not so prominent in Portobello. However, further storage resulted in additional further reduction, so that the ascorbic acid level was lower than that at the beginning of the storage. The observed trend is in agreement with the findings from other studies dealing with fruit and juice stored in MAP [25, 26]. This behavior was expected since ascorbic acid is the most sensitive compound in fresh mushrooms, especially vulnerable under prolonged storage and changed storage conditions, as in our experiment . After three weeks of cold storage the level of ascorbic acid in both strains was the highest in O2 MAP. The difference between O2 and other MAPs was statistically significant. This could be due to the decreased respiratory metabolism as proposed by Liu et al. .
By comparing the changes in MAP, significant differences were observed for the two A. bisporus varieties, pointing that although they belong to the same species these two strains have different metabolism behaviors.
Total flavonoid content
As is evident from the Table 1 the amount of flavonoids decreased during 22 days of storage, similarly for both mushroom varieties. The average amount of flavonoids was about 1 g kg−1 catechin equivalents which corresponds to the findings of Palacios et al.  and Kaewnarin et al. . Significant changes occurred in the commercial packaging of the white button mushroomafter five days of storage, which was not the case with the brown A. bisporus. The most drastic change appeared in O2 MAP (white variety) and CO2 package (brown variety); it stimulated flavonoid accumulation in both varieties but at different storage times (during the first week in white and the second in Portobello). Gąsecka et al.  pointed that excess of glucose serves as a reservoir for enhanced synthesis of secondary metabolites, such as phenolic compounds. When connected with our previous work , total sugar and flavonoid content were not correlated. However, this should be taken with caution since the method we applied for measuring sugar content has its limitations, like non-selectiveness for different types of carbohydrates present in fungi. The phenol–sulfuric method that we used cannot detect the presence of all sugar forms. This might affect the inconsistencies in the consequent sugar-phenolics correlation. Instead, chromatographic methods might be used to enable a wider range of detection. Methods like high-performance liquid chromatography might be a better choice since they are rapid, simple, and specific . Unfortunately, before the analysis the samples have to be prepared: nonspecifically hydrolyzed with acids (HCl, H2SO4, CrH4O8S2). Another popular choice is enzymatic assays characterized by high specificity and sensitiveness. However, no one enzyme kit can cover all sugars occurring in mushrooms and there is the need to couple it with spectrophotometry . Recently high-performance liquid chromatography coupled to corona charged aerosol detection was proposed as a method with high sensitivity but only for the determination of free sugars and mannitol in mushrooms . The question is an also-which type of phenolic compounds are generated and under which conditions from present glucose. Secondary metabolites, like phenolic compounds, are formed under unfavorable conditions as an organism’s stress response. Different types of stress will stimulate different secondary metabolites like Yan et al. reported for Pleurotus ostreatus exposed to heat stress . The authors identified accelerated glycolysis and the tricarboxylic acid cycle. Similarly, Sudheer et al. measured the increase of total phenolics, flavonoids, polysaccharides, and ganoderic acids when medicinal mushroom Ganoderma lucidum was exposed to external CO2 . Additionally, flavonoids undergo oxidation when exposed to stress so the initial molecule becomes a mixture of compounds with different structural features and might become invisible for a simple screening assay . Another reason for flavonoid changes in our samples might be the fact that they build complexes with proteins . And proteins do go through the degradation process induced by prolonged storage and MAP influence, as we previously proved . Furthermore, the presence of flavonoid-protein compounds in mushrooms restricts the extraction of flavonoids, so that the total amount might be underestimated over time.
Although the white button and Portobello mushroom belong to the same species, genetic differences affected the stress reaction and flavonoid levels in these two strains.
Flavonoid content was similar for both mushroom strains and the highest level was measured after eight days of cold storage in MAP with O2.
Flavonoids are widely present in nature, especially in plants, but mushrooms also contain this group of phenolic compounds [29, 38]. They are considered as antioxidants, especially active in metal chelating, among other mechanisms of protection against reactive oxygen species . Samples tested in our work showed high metal chelating potential at a concentration of 5 g L−1, during the entire period of 22 days of storage, and in all MAPs (Fig. 1). Chelating ability was similar for both strains over prolonged shelf life. All MAPs except O2 caused a decrease in the white strain chelating ability in a statistically significant degree. CO2 packaging influenced the most pronounced decrease, while O2 appeared as the most stable, variating less than 10%. Interestingly, the white variety experienced a sudden drop on the 19th day for all MAP examined in this study, and the commercial atmosphere packaging showed the highest percentage of the loss of antioxidative ability. On the other side, Portobello tended to be a more stable chelating agent for 22 days of cold storage (between 40 and 60%). Its metal chelating ability ranged from 40 to 65% with a wave-like pattern. Piljac-Žegarac et al.  reported similar behavior in case of pomegranate, strawberry, blueberry, and cranberry juice whose antioxidant activity was assayed by 2,2-diphenyl-1-picrylhydrazyl radical scavenging method. N2 MAP went through antioxidant ability decrease in the first week of cold storage, which was not the case with other MAPs. However, this MAP induced the most stable metal ion chelation over a tested period. O2 acted stimulating for almost two weeks with a significant and sudden drop of antioxidant activity from day 12 to the end of the experiment. In the brown variety standard packaging (air) showed to be the best not just in preserving antioxidant ability but even to increase it.
When connected with total flavonoid content it has been noticed that the drop in flavonoid content was followed by the drop in the chelation ability.
However, the flavonoid decrease was not as pronounced, implying that there are other compounds that also affect this type of antioxidant activity. Another, probably more significant cause might be the change in the flavonoid profile. Some flavonoids like kaempferol or apigenin, which were identified in A. bisporus, are very stable when exposed to alkaline decomposition or enzymatic treatment. Others, such as myricetin, decomposed very fast (4–25 min) [11, 29]. It has been proved that the products of phenolic compounds decomposition (as well as those of flavonoids) save its antioxidant ability in significant percentage, which was probably the case in metal chelation as well. Total phenolic compounds in A. bisporus did not fit into this pattern: their amount did not correlate with the metal chelation ability, which was the proof of the importance of flavonoids when it comes to the overall antioxidant activity of mushrooms [13, 40].
Inhibition of type 2 diabetes mellitus related enzymes
Mushrooms, including A. bisporus, are already recognized as functional food as well as foods that have beneficial effect in preventing and controlling diabetes . There are two enzymes linked with diabetes regulation, α-amylase and α-glucosidase , which inhibition we examined (Fig. 2). All tested samples exhibited a significant inhibition of α-amylase activity (maximal measured % of inhibition was 92.97%). The white strain had a lower ability to inhibit α-amylase when compared with the brown one, and the trend was more extreme (Fig. 2a). During the first week of the storage, the % of α-amylase activity increased in all samples except for N2, and then significantly decreased. The middle of the storage period was the time at which all samples (except N2) showed the highest inhibition of α-amylase (86–88%). On the other side, N2 strongly suppressed the ability of A. bisporus to inhibit this enzyme. The highest fluctuations of enzyme inhibiting activity were observed in O2 packaging. The low oxygen package had the highest values for total phenolic compounds which were reported as being responsible for α-amylase inhibition in methanol extracts of plants [40, 43]. However, no clear trend can be observed: in most of the cases, the increase in total phenolic compound content was followed by the increase in α-amylase inhibition. Inconsistencies present here might be explained through the qualitative profile of phenolics present in mushrooms. The sum of phenolic compounds does not have to be equally potent as some of the specific molecules present in the sample. Furthermore, other biologically active compounds, not covered by this research, might be responsible for the observed trends. Additionally, the decrease in O2 concentration affects cell respiration: O2 is a substrate in cell respiration and during this process, intermediary molecules necessary for secondary metabolites (like phenolic compounds) formation are constituted . So, less of these compounds are present under decreased O2 concentration.
The brown variety appeared to be much more powerful inhibitor; its activity never dropped below 60% regardless of the type of the MAP sample tested (Fig. 2b).
Portobello stored in O2 and CO2 exhibited almost the same behavior as the control sample, except N2, the α-amylase inhibition activity of which was significantly lower but still high during the first two weeks of cold storage. Tamboli et al.  showed pronounced α-amylase inhibition activity of various extracts obtained from Pleurotus ostreatus mycelium, connecting this activity with flavonoids (especially catechin) and glycoproteins. In the present study, we did not find the dependence between the total flavonoid content and α-amylase inhibitory activity. Compounds like fatty acids are also proved as inhibitors of diabetes connected enzymes as well as glycoproteins . Synergy between constituents of the button mushroom might also be present when it comes to α-amylase inhibition. However, we showed that the moment of mushroom purchase and consumption as well as the type of shelf-life extending technique had a significant impact on this functional aspect of A. bisporus.
Another enzyme important for prevention and control of diabetes mellitus, α-glucosidase, was also inhibited by the methanol extracts of A. bisporus (Fig. 2c and d). The maximal measured activity exceeded 50%, although overall activity was much lower than that of α-amylase. This is not the first case that natural compounds have different behavior against these two enzymes . The white button mushroom was a particularly poor inhibitor of α-glucosidase, since activity disappeared completely between the first and the second week of storage (Fig. 2c). Almost all MAPs were non-effective in preventing the loss of high α-glucosidase inhibitory activity present at the beginning of the storage period. This indicates that A. bisporus is very sensitive in the post-harvest period and that none of the parameters tested were affected like α-glucosidase activity. Surprisingly, N2 packaging showed stable, and even stimulating effect on this parameter. Even, quite contrary to α-amylase activity. The brown variety maintained the ability to inhibit this enzyme, although it had a wave-like pattern, with a day-by-day statistically significant variation. Depending on the storage time, different MAP packaging showed the best stimulation of α-glucosidase inhibition activity in the brown strain.
Matsuura et al. reported less than 50% of α-glucosidase inhibitory ability of wild A. bisporus ethanol extract and about 30% in the case of water extract . This is in accordance with our findings for the fresh sample of the white strain.
The explanation of these changes is beyond the scope of this study, requiring further research, but this phenomenon is also first time reported and expands a simple view on mushrooms as functional food. Not just that strain, genes, cultivation and storage conditions affect mushroom’s nutritional quality, but they also have significant effect on functional characteristics, as discussed in this study.
Although mushrooms do have functional characteristics, contemporary life style and high demand for extended shelf life puts under the question the functional attributes and levels of nutraceuticals in particular food. Preserving techniques (like MAP) can maintain sensory and some nutritional attributes of mushrooms. Based on our findings, MAP can efficiently save, and even promote, selected functional characteristics of A. bisporus for two weeks of cold storage. For most of the measured parameters in white strain packaging with a high level of O2 had the best effect. In case of Portobello CO2 MAP was more effective. The strongest effect on α-glucosidase inhibition activity of white strain was obtained when the mushrooms were stored in N2 packaging. The effect was stable for all 22 days of shelf life. On the contrary, no clear conclusion can be made in the case of the brown variety. On the other side, commercial packaging negatively affected mushroom’s functional characteristics in most of the examined parameters. More in-depth research is needed to elucidate if the food, such as mushrooms, can be called functional after they spend some time on a retail shelf or under changed storage conditions.
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This study was undertaken with the financial support of the Ministry of Education and Technological Development of the Republic of Serbia (project III 46010) Grant no: Contact No. 200116. Special thanks to Ivana Bojkić, a professional translator, for proofreading the article and English language corrections.
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Vunduk, J., Kozarski, M., Djekic, I. et al. Effect of modified atmosphere packaging on selected functional characteristics of Agaricus bisporus. Eur Food Res Technol (2021). https://doi.org/10.1007/s00217-020-03666-x
- α-amylase inhibition
- α-glucosidase inhibition
- Functional food
- Modified atmosphere packaging
- Shelf life