Abstract
The aim of the study was to calculate the content of non-freezing water (NFW) as well as amount of water associated with the evaporation process (Nev) in the chosen species of fungi. The study focused on lyophilized in vitro mycelium and commonly cultivated mushrooms Agaricus bisporus, Boletus badius and Cantharellus cibarius. Both NFW and Nev were examined by means of differential scanning calorimetry (DSC). The above-mentioned types of water are important components of the state diagram that is a kind of functional graph helping in identifying food stability during storage and selecting suitable conditions of temperature and moisture content for processing. The content of non-freezing water in all examined samples ranged between 0.19 and 0.31 g g−1. The estimated amount of water associated with the evaporation process was found to be between 0.05 and 0.13 g g−1. The obtained results were variable and highly dependent on fungus species, origin (in vitro mycelium vs cultivated) and content of accumulated metals. The influence of these factors is discussed. In order to determine statistical significance, selected samples were measured at least 5 times; the relative standard of deviation (%RSD) did not exceed 4.45 of measured enthalpies. In the group of mycelium from in vitro cultures, the DSC method was used for the first time. The publication also compared the NFW and Nev values with those obtained for naturally grown fruiting bodies of the same species.
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Introduction
State diagram is a kind of graph identifying and visualizing different regions of food as a function of water (or solids) content and temperature. In other words, it is an useful tool showing the complex changes of food while water content and/or temperature is changed. It is also suitable in selecting optimal conditions for further food processing. The idea of state diagram combines water activity and glass transition concepts and was probably used for the first time by Levine et al. [1], widely exploited by other scientific research groups [2,3,4] and then modified by Rahman [5]. One of the important components of state diagram is non-freezing water (NFW) [6,7,8,9,10], defined as a strongly bounded fraction that is not able to crystallize [11, 12] and where typical exothermic peak cannot be calorimetrically measured. The appropriate low water contents found in the hydrophilic polymer are considered to be non-freezing [11]. Water binding is associated with hydrogen bonding and the presence of “nanocavities” formed in the matrix [11]. Depending on water concentration and grade of polymer chains, it can lead to form new reversible and stable structures [13]. Moreover, content of NFW distinctly increases when ionic groups are present in the polymer structure [14]. Berthold et al. [15] concluded that the counter-ion favouring water adsorption is Li+, followed, in decreasing order of efficiency, by Na+, K+, Ca2+ and H+.
Generally, the storage of food is associated with its initial processing. Very often, this involves vaporization of water during a thermal drying, whereas other methods such as sublimation are less frequently used. Removing of free water is held at a temperature up to 100 °C. However, vaporization of water strongly attached to polymer chains by hydrophilic groups could be observed at temperature higher than 100 °C. For example, for samples containing both non-freezing and free water, Hatakeyama et al. [16] reported two states of vaporization in TG studies. The first was terminating lower than 100 °C, and the second was ranging from 147 to 197 °C. An agreement between the results of differential thermal analysis and the mass decrease obtained by TG was confirmed in other investigations of the same author [17]. Thus, in a similar way as non-freezing, the water associated with the evaporation process (Nev) can be considered as water that remains in the material at temperatures significantly exceeding 100 °C or even 140 °C. The measured enthalpy of vaporization (ΔH) is considered as the energy required to evaporate absorbed molecules of water from hydrated material and can be normalized using mass of either dry sample or water. In this research, we used the first method, since it is recommended by Kučerík et al. [18]. In his opinion, it reflects better the mutual interactions between polysaccharide chains and water.
In this way, evaporation of water can be an additional approach to characterize the hydration and water-holding behaviour of mushroom materials. It is suggested that Nev content could be an useful complement of the state diagram in the part describing water evaporation from the liquid and solid phases. Rahman illustrated this segment with respective lines MD and DP (Fig. 1 [5]).
Selected edible mushroom species, both in vitro and natural origin, as Agaricus bisporus, Boletus badius and Cantharellus cibarius, are known as highly valued source of vitamins (especially riboflavin, ergocalciferol), bioelements (for example, selenium, magnesium, copper, iron, calcium, zinc and potassium) [19,20,21,22,23,24,25] and antioxidant substances (phenols, flavonoids, terpenes, steroids, carotenoids) [26,27,28]. For that reason, optimal drying and freezing data for further processing are necessary in the maintenance of chemical and microbiological stability of mushrooms under study.
The aim of the study was to calculate the content of non-freezing water NFW as well as amount of water associated with the evaporation process Nev in the chosen species of lyophilized in vitro mycelium and commonly cultured mushrooms Agaricus bisporus, Boletus badius and Cantharellus cibarius. In the research, the differential scanning calorimetry method was used. The technique was previously applied in various synthetic and semi-synthetic polysaccharides [14, 29,30,31,32]. In the group of mycelium from in vitro cultures, the method was used for the first time. The publication also compared the NFW and Nev values with those obtained for naturally grown fruiting bodies of the same species.
Materials and methods
Mushrooms samples
The in vitro mycelium material of Agaricus bisporus, Cantharellus cibarius and Boletus badius was obtained from Department of Pharmaceutical Botany, Pharmaceutical Faculty, Medical College, Jagiellonian University, as a gift. The naturally grown fruiting bodies of these mushrooms were purchased in local vegetable shops.
Sample preparation
The freeze-dried in vitro mycelium and naturally grown fruiting bodies of Agaricus bisporus, Cantharellus cibarius and Boletus badius material were additionally dried over phosphorus (V) oxide in desiccator. After 6-week-long storage, the mushroom material (about 28–46 mg) was placed in sample pans and the excess of Milli-Q water was added. In order to obtain the desired water content, defined by a Wc factor (the ratio of mass of water to mass of dry mushroom), the water was allowed to evaporate slowly at room temperature. In further investigations, the samples of known Wc ranging from 0.2 to 3.5 g g−1 (18 different concentrations) were used. The homogeneous hydrated material of about 8–9 mg was quickly transferred to aluminium sample pans and immediately hermetically sealed. To reach an equilibrium state, all obtained samples were conditioned at room temperature for about 30 h. The crucibles with mushroom material were weighted before and after each measurement to insure that there is no loss of mass.
In order to protect from spontaneous reactions with water, the aluminium sample pans were previously passivated in an autoclave at 120 °C for 3 h.
DSC analysis
The DSC experiments were performed in nitrogen atmosphere with a flow rate of 50 mL min−1, using EXSTAR DSC 7020 apparatus (Hitachi Inc.) equipped with immersion cooler ULSP 90 (ULSP BV). The DSC instrument was calibrated with 99.9999% indium and high purity Milli-Q water. The measurements were carried out using the following thermal protocol: starting at 20 °C, cooling from 20 to − 60 °C at 3 °C min−1, isothermal at − 60 °C for 5 min, and heating from − 60 to 20 °C at 3°C min−1. The evaporation studies were realized using the same samples; however, in each run, covering lids were perforated and the nitrogen flow rate was reduced to about 5 mL min−1. The thermal procedure was as follows: starting at 20 °C, cooling from 20 to − 40 °C at 5 °C min−1, and heating from − 40 to 150 °C at 3 °C min−1. The purpose of freezing the sample pans before the evaporation investigations was to identify the onset of evaporation easier.
The measured enthalpies both of melting and evaporating were first normalized to the mass of the dry mushroom material and then plotted against the respective water concentration (Wc). In this way, expected linear dependences ∆H = f(Wc) were obtained. The NFW and Nev contents were estimated by extrapolation ∆H to 0 (∆H = 0).
The interpretation of DSC experiments was performed using Muse Measurement v 9.21U software. Due to observed baseline shifts and nonlinearities, the determination of melting as well as evaporating enthalpies was carried out using a T-Slice Analysis (Integral Tangential). In order to reduce experimental errors, DSC runs were repeated three times and averaged. To determine statistical significance, selected samples were measured at least 5 times. The results were expressed as the relative standard deviation (%RSD) and did not exceed 4.45 of measured enthalpies.
Results and discussion
Figure 1 shows a representative DSC run, obtained from hydrated sample of mushroom under study. One can see that immediately after melting, the vaporization process is starting. This interesting phenomenon is marked with the red circle. The subfigure (A) additionally emphasizes it. A similar shape of curves was also reported by other authors [13, 30, 32, 33].
Typical and representative example of DSC run observed during the studies. The red circle points the area of ending of the melting process and the immediate start of evaporation process—the subfigure (A) additionally emphasizes observed phenomenon. Displayed curve was obtained from in vitro mycelium of freeze-dried Boletus badius with water content Wc= 1.3 g g−1. The evaporation studies were realized using the same samples; however, in each run, covering lids were perforated
The typical stack of DSC curves, illustrating changes in enthalpies with various concentrations of water, obtained during the melting and evaporating processes is displayed in Fig. 2. As it was expected, with increasing water content in the samples, the peak of temperature is shifted towards higher temperatures and peak area under the curve increases.
Figure 3 shows some representative examples of DSC runs, obtained from hydrated (Wc about 1.3 g g−1) naturally grown fruiting bodies (A) and in vitro mycelium (B) of freeze-dried Boletus badius. It demonstrates differences of melting enthalpies state during the study. One can see that in vitro sample is characterized by higher value of ΔH = 326 J g−1 when compared to commonly cultivated counterpart from natural sources 277 J g−1. All other samples behaved similarly.
As it was formerly mentioned, the measured enthalpies of both processes were firstly normalized to the dry mass of mushroom material and then plotted against the respective water concentration Wc. Figure 4 shows an appropriate and typical example of such a relationship. One can see a linear increase in the enthalpy with increasing Wc. The obtained linear ∆H = f(Wc) correlation is strong enough; thus, the non-freezing NFW can be estimated after extrapolation ∆H to 0 (∆H = 0).
A very good fit with the high linear regression was also observed for investigated evaporation processes. The obtained values of NFW and Nev with parameters of linearization and confidence coefficients R2 for all studied samples are listed in Tables 1 and 2. The linear trend was maintained throughout the measuring range.
The content of non-freezing water calculated for all studied mushroom samples was ranging from 0.19 to 0.31 g g−1 (Table 1). The highest value was found for cultured fruiting body of A. bisporus (0.31 g g−1) that fit in with 0.30 g g−1 obtained by Guizani et al. [8]. The NFW values of B. badius and C. Cibarius from same group were smaller and equal to 0.23 and 0.22 g g−1 respectively. Whereas the content of non-freezing water is influenced, among others, by the type and concentration of dissolved ions, this disparity may be a result of a different forest and greenhouse substrate composition. The fact that mushrooms are able to accumulate elements from the environment explains their attractiveness for researchers. The essential elements are K, P, Mg, Ca, Na, Zn, Cu, Mn, Ni and Co. K, P and Mg are present at levels of mg g−1 dry matter (DM), while Na, Zn, Ca, Fe, Cu, Mn, etc., are present at µg g−1 DM [25]. It is clear that the cations with the highest concentration will play a key role in the investigated water-holding processes (Table 3).
One can see that the highest total concentration of both potassium, magnesium and sodium can be found for A. bisporus. This fact allows to understand why this species is distinguished by the highest NFW. Interestingly, the NFW content of in vitro mycelium was found to be 0.19 g g−1 only. It clearly shows that the essence of greenhouse production is associated with rapid growth and high mass of the product. For other mycelium in vitro cultures, the highest NFW content was calculated for C. cibarius (0.26 g g−1). This fact should be combined with a higher, when compared to the others species, total content of divalent Mg, Zn, Cu and Fe, which is able to be present as di- and trivalent counter-ion as well.
For comparison purposes, the non-freezing water contents calculated for other food materials as cultured fruits, vegetables, meat, fish and bread are collected in Table 4. It can be noted that they are characterized by a large diversity. For example, NFW value of carrot sample was only 0.08 g g−1 while of King fish muscles was as much as 0.37 g g−1. The meat of a fish has much more NFW than the meat of a wild forest mammal (reindeer) (0.15 g g−1), although it is difficult to draw conclusions from two examples only. The non-freezing water-holding behaviour of the vegetables (except for carrot) is ranging from 0.20 g g−1 for garlic powder to 0.32 g g−1 for broccoli. One can see that those contents are higher than can be found for cultured fruits ranging from 0.16 g g−1 for raspberries and mango to 0.27 g g−1 for pineapple.
Comparing to non-freezing water, the effect of ions on the contents of Nev is associated with different mechanism. Průšovă et al. [31] pointed out that the presence of ions with fixed dimension and surface charge makes the structure more “rigid”. This confirms earlier research [44] associated with the influence of pore (“nanocavities”) size on the character and quantity of water in the non-freezing water layer. Due to the presence of ions, each nanocavity has a stable diameter. The more the cations, the more pores with a fixed diameter can be found. In other words and temporarily excluding the effect of water binding by hydrogen bonds, if the size of pore is small enough, such a space can trap water molecules more firmly and for that reason the enthalpy of evaporation is larger than if the size of pore is larger. In such a situation, enthalpy of evaporation is accordingly smaller, because water molecules can desorb from the matrix more easily.
In the group of mushrooms of cultured or natural origin, the appropriate values of Nev were comparable and were 0.08, 0.09 and 0.07 g g−1 for Boletus badius, Cantharellus cibarius and Agaricus bisporus, respectively (Table 2). Calculated amounts lead to the conclusion that the internal structure formed by the fungal polysaccharide chains, in combination with the concentration of cations and relatively low NFW values, created conditions favourable easy desorption of water molecules from the matrix.
With the exception of A. bisporus, very similar Nev values were obtained in the group of in vitro mycelium -0.05 and 0.09 g g−1 for B. badius and C. cibarius, respectively. However, A. bisporus is an example that confirms the correctness of previously observed relationships. The calculated amount of water associated with the evaporation process was equal to 0.13 g g−1. This is understandable because the samples from this material had the highest total content of cations as well as the highest content of NFW.
Similar studies for other food materials have not been met in the literature.
Conclusions
The contents of non-freezing water NFW and water associated with the evaporation process Nev of lyophilized in vitro mycelium and commonly cultivated mushrooms Agaricus bisporus, Boletus badius and Cantharellus cibarius were successfully estimated using a new, in this area of biological samples, differential scanning calorimetry technique. The obtained results were variable and highly dependent on fungus species, origin (in vitro mycelium or cultivated) and content of accumulated metals ions. It was stated that the concentration of NFW increased with the increase in the content of cations. Measured amounts of Nev were low for all investigated samples, suggesting that the non-freezing water consists mostly of water molecules interacting with sorption sites not trapped in pores.
The above-mentioned water contents are important components of the state diagram, which could be used in identifying mushroom stability during storage or selecting suitable conditions of temperature and moisture content for processing.
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Talik, P., Piwowarczyk, J., Muszyńska, B. et al. DSC study of hydration and water-holding behaviour of cultured in vitro mycelium and naturally grown fruiting bodies of freeze-dried Boletus badius, Agaricus bisporus and Cantharellus cibarius. J Therm Anal Calorim 143, 3525–3532 (2021). https://doi.org/10.1007/s10973-020-09654-3
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DOI: https://doi.org/10.1007/s10973-020-09654-3