Abstract
The edible mushroom Amanita rubescens Pers., regularly collected and consumed in Slovakia, was assessed for health risk due to the mercury content in its fruiting body parts. For this purpose, 364 both from the soil/substrate and mushroom samples from 40 localities in Slovakia were evaluated. At the same time, 21 samples of 7 developmental stages of the fruiting body of A. rubescens were taken in the Žakýlske pleso locality. The total mercury content in the soil and mushroom samples was determined using an AMA-254 analyzer. The contamination factor (Cf) and index of geoaccumulation (Igeo) were used to detect the level of soil pollution by mercury. The ability of A. rubescens to accumulate mercury from the soil environment was evaluated using the bioconcentration factor (BCF), and the distribution of mercury in the mushroom body was evaluated using the translocation quotient (Qc/s). To determine the health risks resulting from mushroom consumption, the percentages of provisional tolerable weekly intake (%PTWI) and target hazard quotient (THQ) were used. The obtained results have confirmed serious content of mercury soil pollution, especially in former mining areas, where the situation is alarming from a health risk point of view. Consumption of A. rubescens was found to be risky, not only in former mining areas, but higher values of mercury were also detected in other parts of Slovakia. Evaluation of the developmental stages of the fruiting body of A. rubescens showed that the highest bioconcentration factor was determined at developmental stage no. VI for caps with a value of 2.47 mg kg−1 and developmental stage VII for stipes with a value of 1.65 mg kg−1 DW.
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Introduction
Fungi including mushrooms are crucial for the degradation, utilization, and transformation of organic and inorganic substrates [1, 2]. For centuries, edible mushrooms have been collected from forest areas or cultivated and consumed for their nutritional benefits, medicinal utility, and distinguishable flavor. Wild edible mushrooms are rich in many nutritionally beneficial components, such as amino acids, vitamins, polysaccharides, and lipids [3, 4]. However, mushrooms contain trace metals such as cadmium, mercury, lead, and silver, which are undesirable and toxic to mammals [5]. Owing to their nutritional, therapeutic, and economic benefits, mushrooms are currently consumed worldwide and are suitable food for vegetarians and vegans. In the last few decades, studies focusing on mushroom composition have become a matter of great interest to researchers because of their immunomodulatory, antimicrobial, antioxidant, anticancer, and antitumor properties [6,7,8,9]. Mushroom picking and eating are traditional activities in Slovakia, thanks to the lush forests and diverse types of mushrooms [10, 11]. For many years, Slovaks have been collecting mushrooms for both culinary and medicinal purposes, and this activity remains popular. Boletus spp., Leccinum spp., and C. cibarius are the most popular Slovak mushroom species [10]. Mercury is a global pollutant that has raised great concerns worldwide. Unlike many other risk metals, mercury can persist in the atmosphere for a long time and migrate long distances. Mercury is a carcinogenic metal toxin that considerably affects the immune system and causes blockage of the autonomic nervous system. Manifestations of mercury poisoning differ based on the chemical forms of mercury (organic or inorganic), the type of poisoning (acute or chronic), and the amount of mercury present.
High mercury concentrations can permanently damage the brain, kidneys, and fetal development [12, 13]. Inorganic mercury can be converted to highly neurotoxic methyl mercury (MeHg), which is bioaccumulated and biomagnified in the food chain, endangering human health. Mushrooms efficiently mobilize Hg from soil and its subsequent sequestration within fruiting bodies [8]. The differences in Hg uptake from soils among mushroom species may be genetically influenced. Edible parts of wild-growing mushrooms are products that show a higher content of Hg compared to fruits, vegetables, and other kinds of plant-based foods and animals [14,15,16].
The genus Amanita includes some of the best-known gourmet mushrooms, such as A. rubescens Pers., A. fulva, A. ovoidea, A. baccata, A. vaginata, and A. caesarea; on the other hand, it is responsible for over 90% of lethal mushroom poisonings worldwide (A. phalloides) [17, 18]. Most of the species in this genus are ectomycorrhizal fungi that are associated with over ten tree families and play important roles in forest ecosystem health. Many species of the Amanitaceae family are inedible, for example, A. pantherina, A. phalloides, A. virosa, and A. muscaria, and are well-known for their psychedelic properties [9]. Although some of the listed mushrooms are edible and delicious, they are protected in Slovakia and, therefore, cannot be collected.
This publication is part of a series of articles devoted to the mercury content of the body parts of different mushroom species from various regions of Slovakia and the health risks resulting from their consumption [19,20,21]. A. rubescens is widely available and well-liked wild edible mushroom that exhibits excellent sensory quality. The fruiting bodies of A. rubescens can also bioaccumulate pollutants from the environment and ultimately pose a risk to consumers in the form of intoxication [14, 22,23,24].
In addition to geochemical anomalies, the primary source of soil pollution in Slovakia is a wide range of anthropogenic activities [25]. As mining activity has a long and rich history on the territory of Slovakia, it is one of the important polluters of the soil environment, along with industry, agriculture, and transport [26]. The threat in the form of increased content of toxic elements in the soil environment is mainly represented by former mining areas with untreated and un-reclaimed mining works.
The aims of this study were (a) to evaluate soil mercury pollution within Slovakia using the contamination factor (Cf) and index of geoaccumulation (Igeo); (b) to evaluate the relationship between soil mercury pollution and mercury content in mushroom body parts using the bioconcentration factor (BCF); (c) to determine the health risks resulting from the consumption of mushrooms using the percentage of provisional tolerable weekly intake (%PTWI) and the target hazard quotient (THQ); and (d) to evaluate the mercury content in the body of A. rubescens depending on the stage of development.
Material and Methods
Substrate and Mushroom Sampling and the Preparation Before Analysis
Samples of the edible mushroom A. rubescens (n = 364) were collected at 40 sampling localities within Slovakia from 2015 to 2021. The sampling localities are shown in Fig. 1S. The number of samples belonging to a particular locality ranged from 5 to 20. Simultaneously, the A. rubescens samples at seven developmental stages were collected at the locality of Žakýlske pleso. In total, 21 samples (three samples from each of the 7 developmental stages of the fruiting body) were sampled. The samples were collected on 1 day from an area of 2 × 2 m, where all seven developmental stages of A. rubescens were found. We chose such sampling conditions because of the probable presence of different generations of the same mycelium and at the same time low variability of the Hg content in the substrate. The mushroom samples were cleaned of larger impurities in situ and placed in ventilated polyethylene boxes for transportation. A corresponding soil/substrate sample (n = 364) of approximately 200 g from a depth of 0.10 m was taken at each sampling site.
Soil/substrate samples were taken as mixed samples from three random places in the vicinity up to 1 m from the mushroom sample and stored in re-sealable PE bags. Mushroom samples were processed under laboratory conditions on the same day as the sampling. The water content of the fresh samples, used for the analysis of the mercury transfer dynamics within individual developmental stages, was analyzed by moisture analyzer DLB 160-3A (Kern & Sohn GmbH, Germany). After washing in deionized water, the samples were divided into caps and stipes, cut into thin slices, and oven-dried with forced circulation (40 °C for ⁓24 h) in the laboratory oven (Memmert UF 110 m, Memmert & Co. KG, Schwabach, Germany). The dried samples were homogenized using a rotary homogenizer IKA A 10 basic (IKA-Werke GmbH & Co. KG, Staufen, Germany) and stored in re-sealable PE bags prior to the analysis. The soil/substrate samples were crushed, cleaned from impurities, and air-dried at room temperature for 3 weeks. Subsequently, the samples were sieved through a 2-mm sieve and stored in paper bags until analysis.
Total Mercury Content Determination
Cold-vapor atomic absorption spectrometry (CV-AAS) using AMA-254 (AlTec spol. s.r.o., Prague, Czech Republic) coupled with an autosampler ASS-254 (AlTec spol. s.r.o., Prague, Czech Republic) was used for Hg content analysis in soil/substrate and mushroom samples. The detection and quantification limits were set at 0.0011 mg kg−1 and 0.0031 mg kg−1, respectively [27]. Quantitative determination of Hg was performed at λ = 253.7 nm. Two CRM materials were analyzed to check the quality and assurance of the measurements: ERM-CC 141, loam soil (IRMM Geel, Belgium) and ERM-CE 278 k, mussel tissue (IRMM Geel, Belgium). Each CRM was analyzed six times, and in each series, the blank three times. The recovery of the studied reference materials was as follows: ERM-CC 141, loam soil (98.6%; certified value, 0.083 mg kg−1 DW; determined value, 0.0818 mg kg−1 DW) and ERM-CE 278 k, mussel tissue (101.4%; certified value, 0.071 mg kg−1 DW; determined value, 0.072 mg kg−1 DW). The current water content was considered during measurement. Laboratory and analytical procedures focused on pre-treatment (drying, homogenization) have been described in detail in previous papers [19,20,21].
Contamination Factor (C f) and the Index of Geoaccumulation (I geo)
To understand the ecological status of the soil environment in the former mining areas, the selected factors and indices were used. The contamination factor (Cf) reflects the anthropogenic input of elemental pollution and is often used for soil evaluation worldwide [28]. It considers the content of risk elements from the surface of the soil and the background levels [29]. The contamination factor [30] is calculated as follows:
where \(C_{0-1}^i\) is the content of Hg measured in the soil/substrate sample and \(C_n^i\) is the background level of Hg, which was for the Slovak soils set to 0.06 mg kg−1 [31]. The state of pollution was determined based on the following categories: low contamination factor (Cf < 1), moderate contamination factor (1 ≤ Cf < 3), considerable contamination factor (3 ≤ Cf < 6), very high contamination factor (Cf ≥ 6).
The index of geoaccumulation (Igeo) which was originally determined by Müller [32] is calculated as follows:
where Cn is the measured concentration of the element in soil/substrate, and Bn is the geochemical background value of mercury in soils (0.06 mg kg−1) [31]. The values of Igeo are divided into seven categories [32]: background value (Igeo ≤ 0), uncontaminated (0 ≤ Igeo < 1), uncontaminated to slightly contaminated (1 ≤ Igeo < 2), slightly contaminated (2 ≤ Igeo < 3), moderately contaminated (3 ≤ Igeo < 4), strongly contaminated (4 ≤ Igeo < 5), a very strongly contaminated (Igeo ≥ 5).
Bioconcentration Factor (BCF) and Translocation Cap/Stipe Quotient (Q c/s)
Bioconcentration factor (BCF) was used to calculate the level of mercury accumulation from soil/substrate to the fruiting body of A. rubescens as follows:
where Hgms is the total content of mercury in mushroom samples (mg kg−1 DW) and Hgss is the total content of mercury in soil/substrate samples (mg kg−1 DW). The bioconcentration factor was set separately for caps and stipes of mushroom samples. BCF results indicate the excluder species (BCF < 1), indicator species (BCF = 1), and accumulators/hyperaccumulators (BCF > 1) [33].
The translocation cap/stipe quotient (Qc/s) was used to compare the level of Hg translocation within the fruiting body of A. rubescens mushroom. The translocation factor was calculated as follows [34]:
where Hgcap and Hgstipe are the total content of mercury in caps and stipes, respectively.
Health Risk Assessment
Considering that A. rubescens is one of the most frequently collected and consumed mushrooms in Slovakia, the percentage of provisional tolerable weekly intake (%PTWI) was used as an indicator of potential risk arising from long-term mushroom consumption. The PTWI for mercury was established as 0.004 mg kg−1 body weight per week [35]. Since we determined the average weight of an adult to be 70 kg, the provisional tolerable weekly intake was set to 0.28 mg per week. The percentage of PTWI was determined separately for caps and stipes, as follows:
where Hg in mushrooms is the total content of Hg in mg kg−1 determined in the mushroom sample (fresh weight). Intake is the estimated number of mushrooms consumed by an adult person. Based on the Statistical Office of the Slovak Republic [36], the amount of consumed “other vegetables including mushrooms” was 0.23 kg per week. The consumption of mushrooms from a locality may be considered a potential risk if the value exceeds 100%.
The targeted hazard quotient (THQ), which expresses the level of non-carcinogenic risk from the intake of pollutants, was used to determine the health risks resulting from the consumption of A. rubescens from different localities [37]. THQ is defined as the ratio of exposure to a toxic element and its highest reference dose, which has no adverse health effects on humans [38]. THQ can be calculated using the following equation:
where Efr is the exposure frequency (365 days); ED is the duration of the exposure (70 years); ADC is the average daily consumption of the mushrooms (33 g per day [35]); CE is the average Hg concentration in mushroom samples (mg kg−1 FW); RfDo is the oral reference dose for mercury (0.0003 mg kg−1 day−1) [39]; BW is the average adult body weight (70 kg); ATn is the average exposure time (25,550 days as the product of 365 days and 70 years); and 10−3 is used for the units conversion. If the THQ reaches a value lower than 1, it indicates a non-carcinogenic effect for the consumer. If the THQ reaches a value higher than 1, it is a sign of a higher increased threat in terms of carcinogenicity.
Statistical Analysis and Map Preparation
All statistical analyses were performed using the PAST statistical program [40]. Data were tested for normality (Shapiro–Wilk test) and log + 1 was transformed before the analysis. Data are expressed using descriptive statistics as average ± standard deviation (minimum–maximum). Spearman’s correlation coefficient was used to determine the relationship between soil mercury content and its content in the body parts (caps and stipes) and the relationship between body parts in terms of total mercury content. The non-parametric Mann–Whitney U test was used to test for significant differences between caps and stipes in total mercury content, BCF, and %PTWI. The non-parametric Kruskal–Wallis test was used to determine the differences in Cf values between the evaluated localities. All the maps were created in the open-source QGIS software (version 3.26.2).
Results and Discussion
The content of mercury determined in soil samples and mushroom (A. rubescens) body parts (caps and stipes) with the number of samples collected in individual locations is shown in Table 1.
Mercury Content in Soil/Substrate Samples
The average content of mercury in the soil was 0.12 ± 1.33 (0.03–10.0) mg kg−1 DW. The highest values were determined in former mining areas of Krompachy 2.38 ± 0.89 (1.54–5.32) mg kg−1 DW), Nižnoslanská Baňa 3.01 ± 0.70 (2.56–8.40) mg kg−1 DW, and Štefánská Huta 4.80 ± 0.89 (1.28–10.0) mg kg−1 DW. The localities reached significantly higher values of soil mercury content (p < 0.001) compared to others. From a statistical point of view, the soil mercury content determined in Štefanská Huta was also significantly higher than that of Krompachy and Nižnoslanská Baňa, while Krompachy and Nižnoslanská Baňa did not differ between themselves. According to Šefčík et al. [31], the average Hg content in Slovak soils was 0.06 mg kg−1 DW. Of the total number of evaluated sampling sites (n = 364), only 25 reached a value lower than the average for Slovakia. The limit value of mercury in the Slovak soils is set at 0.50 mg kg−1 based on the current legislation [41]. The evaluated soil samples exceeded the permissible limit in 30 cases, which was almost 8% of the sampling sites. In most cases, these have already been mentioned in former mining localities.
Contamination Factor (C f) and Index of Geoaccumulation (I geo)
The contamination factor (Cf) was used to evaluate the level of soil contamination and distinguish anthropogenic inputs from soil pollution [42]. The value of the mercury contamination factor was 2.07 ± 22.1 (0.46–167). According to the contamination factor values, 7.70% of the sampling sites had low contamination factor (Cf < 1), 58.8% were moderately contaminated (1 ≤ Cf < 3), 20.9% were considerably contaminated (3 ≤ Cf < 6), and 12.6% of the sampling sites were very highly contaminated by mercury (Cf ≥ 6). The average values of the contamination factors determined for each sampling locality are shown in Fig. 1. Based on the results obtained, we can conclude that mercury pollution in Slovak soils is serious. The highest values of contamination factor were found in former mining areas such as Štefanská Huta (max Cf = 167), Nižnoslanská Baňa (max Cf = 139), and Krompachy (max Cf = 88.6). These localities are known to be problematic in terms of pollution risk. Kimaková et al. [43], who evaluated the Hg content in arable soil in Slovakia, found that the Hg content in Štefanská Huta was 50 times higher than the maximum allowed limit level. Likewise, according to the long-term monitoring of the soil environment in the vicinity of Krompachy, the mercury content in the soil environment is extremely high and significantly exceeds the hygienic standards intended for healthy soils [44].
The index of geoaccumulation (Igeo) is useful for evaluating the anthropogenic contamination of soils by comparing soil concentrations with background concentrations [45] and gives us an understanding of the pollution status of the sampling sites. The average Igeo value was 0.46 ± 1.55 (it ranged between 1.69 and 6.79). Background values of mercury were determined in 31.1% of the samples, 35.4% were uncontaminated, 21.0% were uncontaminated or slightly contaminated, 5.20% were slightly contaminated, 0.60% were moderately contaminated, 1.50% were strongly contaminated, and 5.20% were very strongly contaminated by mercury. The average values for each sampling locality are shown in Fig. 2.
The Mercury Content in A. rubescens
The mercury content of mushrooms is influenced by the mercury content of the soil [46, 47]. The emerging bioindicative properties of mushrooms concerning the soil environment have been described in many studies [48, 49]. Several studies that focused on the impact of the environment on the pollution of the soil environment and subsequently on the growth of mushrooms have confirmed the significant impact of urbanization, transport, and other man-made activities [8, 50]. The authors also highlighted the ability of mushrooms to accumulate more toxic elements than other living organisms, especially plants [51,52,53]. Consistent with these findings, a significant positive correlation between the mercury content in A. rubescens body parts and the underlying soil samples (p < 0.001) was confirmed (Fig. 3). The ability of mushrooms to accumulate soil pollution was exceptional. Several studies have shown that this ability is species-specific [54] and influenced by the anatomy, physiology, and habitat conditions of the evaluated mushrooms [55]. In addition, the storage of risk elements in the bodies of mushrooms has certain specificities. The content of mercury in caps and stipes of A. rubescens was 0.37 ± 2.80 (0.03–19.7) mg kg−1 DW and 0.28 ± 1.50 (0.03–9.32) mg kg−1 DW, respectively. The content of mercury in caps of A. rubescens reached significantly higher values compared to stipes (p < 0.001). Our findings are consistent with those of Drewnowska et al. [9] who evaluated the content of Hg in caps and stipes of A. rubescens collected in Poland. In Central Europe, the risk element content of mushrooms was determined primarily in samples from environmentally polluted areas. In the Czech Republic, the values of mercury in A. rubescens sampled in the vicinity of the lead smelter were 12.0 ± 8.1 mg kg−1 DW, while control samples reached values of 1.3 ± 0.9 mg kg−1 DW [56]. In another Czech Republic historical silver-mining area, the values of mercury in A. rubescens were 1.55 ± 1.22 (0.25–4.0) mg kg−1 DW, while caps and stipes were not analyzed separately [57]. Demirbaş [58] who made research in the Black Sea region have found that the mercury content in A. rubescens was 0.42 ± 0.08 mg kg−1 DW.
Bioconcentration Factor (BCF) and Translocation Quotient Cap/Stipe (Q c/s)
The bioconcentration factor was used to detect the ability of A. rubescens to accumulate mercury from the soil/substrate. The determined values differ significantly (p < 0.001) between caps 2.92 ± 3.57 (0.13–32.9) and stipes 1.80 ± 2.92 (0.08–31.9). These results are in accordance with the findings of Chudzyński and Falandysz [59], who claimed that the mercury content in caps is usually higher because of the higher metabolic activity and the higher content of proteins and enzymes (compared to stipes) that can bind Hg. Only 13.0% of the cap samples and 24.0% of the stipe samples reached BCF values lower than 1 (Fig. 4). Based on the results obtained, we can conclude that A. rubescens can be considered a mercury accumulator. The ability of mushrooms to accumulate mercury from the soil environment, and thus the values of the BCF, is also influenced by the type of substrate, climate, and agricultural or farming activities [60,61,62]. Andráš et al. [63] who evaluated the bioconcentration abilities of 13 mushroom species sampled in a former mining area (Slovakia) have found that only 2 species can be considered excluders (BCF < 1).
The translocation quotient (Qc/s) was used to express the mobility of Hg in the fruiting bodies of mushrooms. The Qc/s values determined for A. rubescens were 1.56 ± 2.51 (0.13–41.6) (Fig. 5). Values of Qc/s higher than 1 indicate that the caps of the mushroom accumulate higher amounts of mercury than the stipes. The Qc/s value was lower than one in only 9.0% of the evaluated samples. Higher concentrations of Hg are usually found in caps than in stipes; additionally, they are largely concentrated in hymenophore gills and tubes [64,65,66]. Likewise, our results showed higher values of Hg in caps, which are more often processed and consumed than stipes.
Percentage of Provisional Tolerably Weekly Intake (%PTWI)
The higher content of mercury in the consumed products can cause serious health problems, which is why the Food and Agriculture Organization/World Health Organization [67] set safe levels of some risky elements in terms of provisional tolerable daily intake. If the level of 100% PTWI is exceeded, there is a real threat to consumer health. The results obtained showed that the %PTWI for caps 30.4 ± 232 (2.54–1617) reached significantly higher values (p < 0.01) compared to stipes 19.5 ± 123 (2.49–765). This level was significantly influenced by the locality of A. rubescens (Fig. 5). The level of 100% PTWI was exceeded in almost 12.0% of the cap samples and 10.0% of the stipe samples. The highest values were determined in former mining areas, which are considered problematic in terms of environmental quality for a long period [68, 69]. All of them (Krompachy, Štefanská Huta, and Nižnoslanská Baňa) are among the environmentally burdened territories and are registered in the Identification System of Environmental Burdens of the Slovak Republic [70]. As stated by several researchers, the consumption of mushrooms collected in the vicinity of mining areas always brings increased health risks [57, 71,72,73]. The values exceeding 100% of PTWI were also recorded at several sampling sites of Veľká Lesná locality which is part of the Pieniny National Park. The pollution in this area may be related to the proximity of large urban centers localized close to the northern border of Slovakia (in Poland) and the transmission of pollutants to this area by wet or dry deposition [74]. However, several studies have stated that the highest content of risk elements in the ambient air of High Tatras may be primarily caused by the proximity of mines and ore processing plants on the Polish side of the Tatras [75]. In addition to metal ore mining and metallurgy, some other industrial and economic activities also took place in the Polish Tatras such as quarries, sawmills, lime works, and two paper mills [76, 77].
Target Hazard Quotient (THQ)
The target hazard quotient was established to determine the health risks resulting from the long-term consumption of mushrooms, considering the highest safety reference dose of mercury. Food is considered safe if the value of 1 is not exceeded. The THQ values were determined for caps 0.58 ± 4.46 (0.05–31.0) and stipes 0.37 ± 2.36 (0.05–14.7) of A. rubescens. Value 1 was exceeded in 25% of cap samples and 17% of stipe samples. By comparing the locations where at least one sample was found to be risky (exceeding the THQ > 1 value), we found that out of the total number of 40 evaluated locations, a health risk related to the consumption of A. rubescens was detected in 22 (Fig. 6). This represents a much higher percentage (55%) of potentially risky locations compared to the %PTWI. It is due to the fact that THQ takes into consideration a health risk resulting from long-term exposure whereas %PTWI determines the acute exposure. All the locations determined as potentially risky by the %PTWI correlated with the THQ results.
Mercury Bioconcentration Based on the Developmental Stages
The mercury content in the caps and stipes of A. rubescens at different developmental stages is shown in Fig. 7. It has been found in earlier studies that the Hg content in the edible mushroom bodies is significantly influenced (besides the family, genus, and species affiliation) by developmental stage [78, 79]. The differences in Hg content during the developmental stages could be the result of the dilution effect when the content of the water in the cap changes. Additionally, the older mushroom bodies lose the vitality and the ability to transport nutrients, because the fruiting body of the fungus is dispersed, and its life cycle ends. The ability of A. rubescens to accumulate Hg from the soil in different developmental stages was also expressed by BCF values, separately for caps and stipes (Fig. 7). The results largely replicated the differences found in the total mercury content in individual developmental stages. In both cases (the total Hg content and BCF), it was confirmed that time also plays a key role, since longer exposure to mercury in the soil environment (mushrooms in older developmental stages) resulted in higher BCF values.
Conclusion
The highest concentration of Hg in soil and A. rubescens body samples was recorded in former mining areas. However, other areas of Slovakia cannot be considered uncontaminated. The high Hg content in the soil environment was also manifested by its increased concentrations in the edible mushroom A. rubescens, which can be considered an accumulator of mercury. More than half of the studied 40 locations can be considered risky when it comes to the consumption of A. rubescens. We found the highest health risks at the former mining localities, where the quality of the environment has been a known and unresolved problem for a long time. Considering the Hg content at different developmental stages of the A. rubescens body, we can conclude that from a health point of view, younger mushrooms are more suitable for human consumption.
Data Availability
All data generated or analyzed during this study are included in this published article (and its supplementary information file).
References
Harms H, Schlosser D, Wick L (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192. https://doi.org/10.1038/nrmicro2519
Gadd G (2004) Mycotransformation of organic and inorganic substrates. Mycologist 18(2):60–70. https://doi.org/10.1017/S0269915X04002022
Mustafa F, Chopra H, Baig AA, Avula SK, Kumari S, Mohanta TK, Saravanan M, Mishra AK, Sharma N, Mohanta YK (2022) Edible mushrooms as novel myco-therapeutics: effects on lipid level, obesity and BMI. J Fungi 8:211. https://doi.org/10.3390/jof8020211
Rahi DK, Malik D (2016) Diversity of mushrooms and their metabolites of nutraceutical and therapeutic significance. J Mycol 7654123. https://doi.org/10.1155/2016/7654123
Rhaman AB, Naher SMS, Siddiquee S (2020) Mushroom quality related with various substrates bioaccumulation and translocation of heavy metals. J Fungi 8:42. https://doi.org/10.3390/jof8010042
Maity P, Sen IK, Chakraborty I, Mondal S, Bar H, Bhanja SK, Mandal S, Maity GN (2021) Biologically active polysaccharide from edible mushrooms: a review. Int J Biol Macromol 172:408–417. https://doi.org/10.1016/j.ijbiomac.2021.01.081
Rasalanavho M, Moodley R, Jonnalagadda SB (2020) Elemental bioaccumulation and nutritional value of five species of wild growing mushrooms from South Africa. Food Chem 319:126596. https://doi.org/10.1016/j.foodchem.2020.126596
Širić I, Falandysz J (2020) Contamination, bioconcentration and distribution of mercury in Tricholoma spp. mushrooms from southern and northern regions of Europe. Chemosphere 251:126614. https://doi.org/10.1016/j.chemosphere.2020.126614
Drewnowska M, Jarzyńska G, Kojta AK, Falandysz J (2012) Mercury in European Blushers, Amanita rubescens, mushrooms and topsoils: bioconcentration potential and intake assessment. J Environ Sci Health B 47(5):466–474. https://doi.org/10.1080/03601234.2012.663609
Predanócyová K, Árvay J, Šnirc M (2023) Exploring consumer behavior and preferences towards edible mushrooms in Slovakia. Foods 12:657. https://doi.org/10.3390/foods12030657
Olah B, Kunca V, Gallay I (2020) Assessing the potential of forest stands for ectomycorrhizal mushrooms as a subsistence ecosystem service for socially disadvantaged people: a case study from Central Slovakia. Forests 11:282. https://doi.org/10.3390/f11030282
Sakamoto M, Tatsuta N, Izumo K, Phan PT, Vu LD, Yamamoto M, Nakamura M, Nakai K, Murata K (2018) Health impacts and biomarkers of prenatal exposure to methylmercury: lessons from Minamata. Japan Toxics 6:45. https://doi.org/10.3390/toxics6030045
Al-Saleh I, El-Doush I, Shinwari N, Al-Baradei R, Khogali F, Al-Amodi M (2005) Does low mercury containing skin lightening cream (fair & lovely) affect the kidney, liver, and brain of female mice? Cutan Ocul Toxicol 24(1):11–29. https://doi.org/10.1081/CUS-200046179
Selin NE (2018) A proposed global metric to aid mercury pollution policy. Science 360:607–609. https://doi.org/10.1126/science.aar8256
Falandysz J, Drewnowska M (2015) Distribution of mercury in Amanita fulva (Schaeff.) Secr. mushrooms: accumulation, loss in cooking and dietary intake. Ecotoxicol Environ Saf 115:49–54. https://doi.org/10.1016/j.ecoenv.2015.02.004
Varo P, Lähelmä O, Nuurtamo M, Saari E, Koivistoinen P (1980) Mineral element composition of Finnish foods. VII. Potato, vegetables, fruits, berries, nuts and mushrooms. Acta Agric Scand Suppl 22:S89–S113
Tavassoli M, Afshari A, Letiţia A, Mégarbane AB, Dumanov J, Bastos MM, Tsatsakis PA, Carvalho F, Hashemzaei M, Karimi G, Rezaee R (2019) Toxicological profile of Amanita virosa – a narrative review. Toxicol Rep 6:143–150. https://doi.org/10.1016/j.toxrep.2019.01.002
Klein AS, Hart J, Brems JJ, Goldstein L, Lewin K, Busuttil RW (1989) Amanita poisoning: treatment and the role of liver transplantation. Am J Med 86(2):187–193. https://doi.org/10.1016/0002-9343(89)90267-2
Šnirc M, Jančo I, Hauptvogl M, Jakabová S, Demková L, Árvay J (2023) Risk assessment of the wild edible Leccinum mushrooms consumption according to the total Mercury content. J Fungi 9(3):287. https://doi.org/10.3390/jof9030287
Árvay J, Hauptvogl M, Demková L, Harangozo Ľ, Šnirc Ľ, Bobuľská L, Štefániková J, Kováčik A, Jakabová S, Jančo I, Kunca V, Relić D (2022) Mercury in scarletina bolete mushroom (Neoboletus luridiformis): intake, spatial distribution in the fruiting body, accumulation ability and health risk assessment. Ecotoxicol Environ Saf 232:113235. https://doi.org/10.1016/j.ecoenv.2022.113235
Demková L, Árvay J, Hauptvogl M, Michalková J, Šnirc M, Harangozo Ľ, Bobuľská L, Bajčan D, Kunca V (2021) Mercury content in three edible wild-growing mushroom species from different environmentally loaded areas in Slovakia: an ecological and human health risk assessment. J Fungi 7:434
Štefániková J, Martišová P, Šnirc M, Kunca V, Árvay J (2021) The effect of Amanita rubescens Pers developmental stages on aroma profile. J Fungi 7:611. https://doi.org/10.3390/jof7080611
Zhang Y, Mo M, Yang L, Mi F, Cao Y, Liu C, Tang X, Wang P, Xu J (2021) Exploring the species diversity of edible mushrooms in Yunnan. Southwestern China by DNA barcoding. J Fungi 7:310. https://doi.org/10.3390/jof7040310
Zhou S, Li X, Lüli Y, Li X, Chen ZH, Yuan P, Yang ZL, Li G, Luo H (2021) el cyclic peptides from lethal amanita mushrooms through a genome-guided approach. J Fungi 7:204. https://doi.org/10.3390/jof7030204
Fazekašová D, Petrovič F, Fazekaš J, Štofejová L, Baláž I, Tulis F, Tóth T (2021) Soil contamination in the problem areas of Agrarian Slovakia. Land 10(11):1248. https://doi.org/10.3390/land10111248
Demková L, Árvay J, Bobuľská L, Hauptvogl M, Michalko M, Mihalková J, Jančo I (2020) Evaluation of soil and ambient air pollution around un-reclaimed mining bodies in Nižná Slaná (Slovakia) Post-Mining area. Toxics 8(4):96. https://doi.org/10.3390/toxics8040096
Yaylalı-Abanuz G (2011) Heavy metal contamination of surface soil around Gebze industrial area. Turkey Microchem J 99(1):82–92. https://doi.org/10.1016/j.microc.2011.04.004
Szaková J, Kolihová D, Miholová D, Mader P (2003) Single-purpose atomic absorption spectrometer AMA-254 for mercury determination and its performance in analysis of agricultural and environmental materials. Chem Pap 58(5):311–315
Kowalska JB, Mazurek R, Gąsiorek M, Zaleski T (2018) Pollution indices as useful tools for the comprehensive evaluation of the degree of soil contamination–a review. Environ Geochem Health 40:2395–2420. https://doi.org/10.1007/s10653-018-0106-z
Hakanson L (1980) An ecological risk index for aquatic pollution control. A sedimentological approach. Water Res 14:975–1001
Šefčík P, Pramuka S, Gluch A (2008) Assessment of soil contamination in Slovakia according by index of geoaccumulation. Agriculture 54:119–130
Müller G (1969) Index of geoaccumulation in sediments of the Rhine River. GeoJournal 2:108–118
Baker AJM (1981) Accumulators and excluders strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654. https://doi.org/10.1080/01904168109362867
Busuioc G, Elkes CC, Stihi C, Iordache S, Ciulei SC (2011) The bioaccumulation and translocation of Fe, Zn, and Cu in species of mushrooms from Russula genus. Environ Pollut Res 18:890–896. https://doi.org/10.1007/s11356-011-0446-z
JECFA (2010) Evaluation of certain contaminants in food. In Seventysecond Report of the Joint FAO/WHO Expert Committee on Food Additives. Rome, February 16–25; WHO Technical Report Series 959, JECFA/72/SC. FAO, WHO, Rome, Geneva. Accessed 10 Aug 2023
Statistical Office of the Slovak Republic (2019) Food consumption in the SR in 2018. www.statistics.sk . Accessed 7 Aug 2023
Yin J, Wang L, Chen Y, Zhang D, Hegazy AM, Zhang X (2019) A comparison of accumulation and depuration effect of dissolved hexavalent chromium (Cr6+) in head and muscle of bighead carp (Aristichthys nobilis) and assessment of the potential health risk for consumers. Food Chem 286:388–394. https://doi.org/10.1016/j.foodchem.2019.01.186
US EPA RSL (2016) U.S. Environmental Protection Agency. Regional Screening Levels (RSLs) – Generic Tables. Available online: https://www.epa.gov/risk/regional-screening-levels-rsls-generic-tables-may-2016 . Accessed 25 Jul 2023
Kalač P (2019) Chapter 4 – trace elements. In: Kalač P (ed) Mineral composition and radioactivity in edible mushrooms. Academic Press, pp 75–298. ISBN: 9780128175651
Hammer Ø, Harper DAT, Ryan PD (2001) Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4(1):1–9
AoL - Act of the National Council of the Slovak Republic, No. 220/2004 Coll. http://www.podnemapy.sk/portal/verejnost/konsolidacia/z_220_2004.pdf . Accessed 7 Aug 2023
Pandey B, Agrawal M, Singh S (2016) Ecological risk assessment of soil contamination by trace elements around coal mining area. J Soils Sediments 16:159–168. https://doi.org/10.1007/s11368-015-1173-8
Kimaková T, Vargová V, Onačilová E, Cimboláková I, Uher I, Harich P, Schuster J, Poráčová J (2020) Mercury accumulation in plants from contaminated arable lands in Eastern Slovakia. Ann Agric Environ Med 27(1):29–35. https://doi.org/10.26444/aaem/115282
Musilová J, Arvay J, Vollmannova A, Toth T, Tomas J (2016) Environmental contamination by heavy metals in region with previous mining activity. Bull Environ Contam Toxicol 97(4):569–575. https://doi.org/10.1007/s00128-016-1907-3
Ackah M (2019) Soil elemental concentrations, geoaccumulation index, non-carcinogenic and carcinogenic risks in functional areas of an informal e-waste recycling area in Accra, Ghana. Chemosphere 235:908–917. https://doi.org/10.1016/j.chemosphere.2019.07.014
Alonso J, Salgado MJ, Garcia MA, Melgar MJ (2000) Accumulation of mercury in edible macrofungi: influence of some factors. Arch Environm Contam Toxicol 38:158–162. https://doi.org/10.1007/s002449910020
Falandysz J, Kawano M, Świeczkowski A, Brzostowski A, Dadej M (2003) Total mercury in wild-growing higher mushrooms and underlying soil from Wyzydze Landscape Park. Norther Poland Food Chem 81(1):21–26. https://doi.org/10.1016/S0308-8146(02)00344-8
Türkmen M, Budur D (2018) Heavy metal contaminations in edible wild mushroom species from Turkey’s Black Sea region. Food Chem 254:256–259. https://doi.org/10.1016/j.foodchem.2018.02.010
Wang X, Zhang J, Wu L, Zhao Y, Li T, Li J, Wang Y, Liu H (2014) A mini-review of chemical composition and nutritional value of edible wild-grown mushroom from China. Food Chem 151:279–285. https://doi.org/10.1016/j.foodchem.2013.11.062
Mleczek M, Magdziak Z, Gąsecka M, Niedzielski P, Kalač P, Siwulski M, Rzymski P, Zalicka S, Sobieralski K (2016) Content of selected elements and low-molecular-weight organic acids in fruiting bodies of edible mushroom Boletus badius (Fr.) Fr. from unpolluted and polluted areas. Environ Sci Pollut Res Int 23:20609–20618. https://doi.org/10.1007/s11356-016-7222-z
Mleczek M, Szostek M, Siwulski M, Budka A, Kalač P, Budzyńska S, Kuczyńska-Kippen N, Niedzielski P (2022) Road traffic and abiotic parameters of underlying soils determine the mineral composition and nutritive value of the mushroom Macrolepiota procera (Scop.) Singer. Chemosphere 303: 135213. https://doi.org/10.1016/j.chemosphere.2022.135213
Kalač P (2010) Trace element contents in European species of wild growing edible mushrooms: a review for the period 2000–2009. Food Chem 122:2–15. https://doi.org/10.1016/j.foodchem.2010.02.045
Turkdogan M, Kilicel F, Kara K, Tuncer I, Uygan I (2003) Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ Toxicol Pharmacol 13:175–179. https://doi.org/10.1016/S1382-6689(02)00156-4
Pecina V, Valtera M, Trávníčková G, Komendová R, Novotný R, Brtnický M, Juřička D (2021) Vertical distribution of mercury in forest soils and its transfer to edible mushrooms in relation to tree species. Forests 12:539. https://doi.org/10.3390/f12050539
Ediriweera AN, Karunarathna SC, Yapa PN, Schaefer DA, Ranasinghe AK, Suwannarach N, Xu J (2022) Ectomycorrhizal mushrooms as a natural bio-indicator for assessment of heavy metal pollution. Agronomy 12:1041. https://doi.org/10.3390/agronomy12051041
Kalač P, Burda J, Stašková I (1991) Concentrations of lead, cadmium, mercury and copper in mushrooms in the vicinity of a lead smelter. Sci Total Environ 105:109–119. https://doi.org/10.1016/0048-9697(91)90333-A
Svoboda L, Havlíčková B, Kalač P (2006) Contents of cadmium, mercury, and lead in edible mushrooms growing in a historical silver-mining area. Food Chem 96(4):580–585. https://doi.org/10.1016/j.foodchem.2005.03.012
Demirbaş A (2001) Heavy metal bioaccumulation by mushrooms from artificially fortified soils. Food Chem 74(3):293–301. https://doi.org/10.1016/S0308-8146(01)00155-8
Chudzyński K, Falandysz J (2008) Multivariate analysis of elements content of Larch Bolete (Suillus grevillei) mushroom. Chemosphere 73(8):1230–1239. https://doi.org/10.1016/j.chemosphere.2008.07.055
Huang WH, Lin CC, Liu YY, Huang CM, Yeh YL, Chen TC (2022) Activity concentrations and bioconcentration factors (BCFs) of natural radionuclides (40K, 226Ra, and 232Th) from cultivated substrates to mushrooms. Environ Sci Pollut Res 29:82512–82523. https://doi.org/10.1007/s11356-022-21638-4
Azeez HH, Mansour HH, Ahmad ST (2019) Transfer of natural radioactive nuclides from soil to plant crops. Appl Radiat Isot 147:152–158
Ibikunle SB, Arogunjo AM, Ajayi OS (2019) Characterization of radiation dose and soil-to-plant transfer factor of natural radionuclides in some cities from south-western Nigeria and its effect on man. Sci Afr 3:e00062. https://doi.org/10.1016/j.sciaf.2019.e00062
Andráš P, Midula P, Grofčík J, Drímal M, Dirner V, Rusko M, Dadová J, Turisová I (2022) Mercury accumulation in wild mushrooms at abandoned Hg-deposit Malachov (Slovakia). Carpathian J Earth and Environ Sci 17:143–147. https://doi.org/10.26471/cjees/2022/017/208
Hanć A, Fernandes AR, Falandysz J, Zhang J (2021) Mercury and selenium in developing and mature fruiting bodies of Amanita muscaria. Environ Sci Pollut Res 28:60145–60153. https://doi.org/10.1007/s11356-021-14740-6
Kavčič A, Mikuš K, Debeljak M, Van Elteren JT, Arčon I, Kodre A, Kump P, Karydas AG, Migliori A, Czyżycki M, Vogel-Mikuš K (2019) Localization, ligand environment, bioavailability, and toxicity of mercury in Boletus spp. and Scutiger pes-caprae mushrooms. Ecotoxicol Environ Saf 184:109623. https://doi.org/10.1016/j.ecoenv.2019.109623
Seeger R, Nūtzel R, Feulner L (1976) Die Verteilung des Quecksilbers in den Fruchtkörpern von Steinpilzen und Champignons. Z Lebensm Unters-Forsch 161:115–117. https://doi.org/10.1007/BF01112853
WHO (2017) Mercury and health. https://www.who.int/news-room/fact-sheets/detail/mercury-and-health. Accessed 7 Aug 2023
Musilová J, Franková H, Lidiková J, Chlpík J, Vollmannová A, Árvay J, Harangozo Ľ, Urminská J, Tóth T (2022) Impact of old environmental burden in the Spiš region (Slovakia) on soil and home-grown vegetable contamination, and health effects of heavy metals. Sci Rep 12:16371. https://doi.org/10.1038/s41598-022-20847-8
Fazekašová D, Fazekaš J (2020) Soil quality and heavy metal pollution assessment of iron ore mines in Nizna Slana (Slovakia). Sustainability 12(6):2549. https://doi.org/10.3390/su12062549
Enviroportal Environmental Burden Information System of Slovak Republic (2019). https://envirozataze.enviroportal.sk/ . Accessed 9 Aug 2023
Falandysz J, Saba M, Liu HG, Li T, Wang JP, Wiejak A, Zhang J, Wang YZ, Zhang D (2016) Mercury in forest mushrooms and topsoil from the Yunnan highlands and the subalpine region of the Minya Konka summit in the Eastern Tibetan Plateau. Environ Sci Pollut Res 23:23730–23741. https://doi.org/10.1007/s11356-016-7580-6
Árvay J, Tomáš J, Hauptvogl M, Kopernická M, Kováčik A, Bajčan D, Massányi P (2014) Contamination of wild-grow edible mushrooms by heavy metals in a former mercury-mining area. J Environ Sci Health B 49(11):815–827. https://doi.org/10.1080/03601234.2014.938550
Svoboda L, Zimmermannová K, Kaláč P (2000) Concentrations of mercury, cadmium, lead, and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. Sci Total Environ 264:61–67. https://doi.org/10.1016/S0048-9697(99)00411-8
Mazurek R, Szymajda K, Wieczorek J (2010) Mercury content in soils of the Pieniny national park. Ecol Chem Eng 17(8):973–979
Szarlowicz K, Reczynski W, Misiak R, Kubica B (2013) Radionuclides and heavy metal concentrations as complementary tools for studying the impact of industrialization on the environment. J Radioanal Nucl Chem 298:1323–1333. https://doi.org/10.1007/s10967-013-2548-1
Bak B, Piestrzynski A, Radwanek-Bak B (1996) Mining traces in the Polish West Tatras. In: Krzan Z (ed) The nature of the Tatra national park and a man. T.3 the anthropogenic influence. TPN Publishing and Earth Sciences Society, Zakopane. [in Polish]
Jost H (1993) Industry on the Tatra National Park area. In: Cichocki W (ed) The Tatra Mountains Protection. The Tatra Mountains Museum Publishing, Zakopane [in Polish]
Falandysz J, Hanć A, Baralkiewicz D, Zhang J, Treu R (2020) Metallic and metalloid elements in various developmental stages of Amanita muscaria (L.) Lam. Fungal Biol 124:174–182. https://doi.org/10.1016/j.funbio.2020.01.008
Battke F, Ernst D, Halbach S (2005) Ascorbate promotes emission of mercury vapour from plants. Plant Cell Environ 28(12):1487–1495. https://doi.org/10.1111/j.1365-3040.2005.01385.x
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Open access funding provided by The Ministry of Education, Science, Research and Sport of the Slovak Republic in cooperation with Centre for Scientific and Technical Information of the Slovak Republic This work was supported by the Agency of the Ministry of Education, Research, Development and Youth of the Slovak Republic, project nos. VEGA 1/0602/22 and VEGA 1/0213/22.
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All authors contributed to the study conception and design. Demková Lenka: writing—original draft, statistical analysis, funding acquisition. Šnirc Marek: writing—original draft. Jančo Ivona: sample analysis, reviewing and editing. Harangozo Ľuboš: analysis and reviewing. Hauptvogl Martin: map processing, reviewing. Bobuľská Lenka: sample preparation and collection, reviewing. Kunca Vladimír: sample collection, identification, and preparation, reviewing. Árvay Július: writing and review editing, sample collection, preparation, analysis, funding acquisition, supervision. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Demková, L., Šnirc, M., Jančo, I. et al. Blusher mushroom (Amanita rubescens Pers.): A Study of Mercury Content in Substrate and Mushroom Samples from Slovakia with Respect to Locality and Developmental Stages. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-024-04280-8
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DOI: https://doi.org/10.1007/s12011-024-04280-8