This article reviews and updates data on macro and trace elements and radionuclides in edible wild-grown and cultivated mushrooms. A huge biodiversity of mushrooms and spread of certain species over different continents makes the study on their multi-element constituents highly challenging. A few edible mushrooms are widely cultivated and efforts are on to employ them (largely Agaricus spp., Pleurotus spp., and Lentinula edodes) in the production of selenium-enriched food (mushrooms) or nutraceuticals (by using mycelia) and less on species used by traditional medicine, e.g., Ganoderma lucidum. There are also attempts to enrich mushrooms with other elements than Se and a good example is enrichment with lithium. Since minerals of nutritional value are common constituents of mushrooms collected from natural habitats, the problem is however their co-occurrence with some hazardous elements including Cd, Pb, Hg, Ag, As, and radionuclides. Discussed is also the problem of erroneous data on mineral compounds determined in mushrooms.
Mushrooms are heterotrophic eukaryotic organisms classified in the kingdom of Fungi. Recent estimates based on high-throughput sequencing methods suggest that there are as many as 5.1 million fungal species worldwide (Blackwell 2011). The European continent has witnessed the highest number of studies in this area, and in this continent, at least 75,000 species exist, and of these, more than 15,000 species are macrofungi, i.e., fungi forming fruit bodies (sporocarps) that are visible to the naked eye (Senn-Irlet et al. 2007). The fruit body is the morphological part of the fungus that bears spores and is commonly called mushroom. There are a variety of forms of mushrooms. Depending on the situation, context, and language, the term mushroom is used also as synonymous to any fungus. In the context of this article, the term mushroom relates to the fleshy fruit body of the macrofungi that can be edible or inedible regardless of its shape and kind. According to their lifestyle, mushrooms are recognized as saprotrophs, parasites, and mutualists—ectomycorrhizal symbionts (Gadd 2008).
The study of the role that fungi have played and are playing in geological processes is termed geomycology (Gadd 2007). The fundamental importance of fungi involves organic and inorganic transformations and element cycling, rock and mineral transformations, bioweathering, fungal–clay interactions, metal–fungal interactions, and mycogenic mineral formation. However, despite the crucial roles of fungi in biogeochemical cycling of elements, the extent to which fungi play a critical role in the Earth’s processes is not always appreciated (Hawksworth 2009).
Similar to plants and microbes, fungi are intimately involved in soil mineral weathering and element cycling in the critical zone (Amundson et al. 2007); their mycelia colonize both organic and mineral soils and produce a variety of active chemical compounds including enzymes (Baldrian 2008) and various organic acids (Stijve and de Meijer 1999; Wallander and Wickman 1999; van Schöll et al. 2006a).
Production of enzymes in saprotrophic macrofungi plays an important role in the transformation of humic substances including humus formation and mineralization (Baldrian 2008) and mobilization of metals associated with organic matter. Extracellular enzymes (1) allow access to organic matter in the microporous layer of soil; (2) transform soil organic matter, which is often insoluble or adsorbed on mineral surfaces, into soluble products; and (3) decrease the structural complexity of soil organic matter (Quiquampoix and Burns 2008). Through enzyme production, the ectomycorrhizal mushrooms can utilize organic N and P forms which would otherwise remain largely unavailable to roots (Landeweert et al. 2001). Nutrient mobilization from amino acids, peptides, proteins, amino sugars, chitin, and nucleic acids has been shown (Chalot and Brun 1998), together with transfer of N and P into the host plant (Antibus et al. 1997). Production of organic acids leads to chemical leaching of mineral surfaces and consequent mobilization of nutrients like P, K, Ca, and Mg that can be translocated to the host plants (Jentschke et al. 2000; Wallander 2000a, b; Wallander and Wickman 1999).
Analogous to their organic nutrient mobilizing capabilities, the abilities of different ectomycorrhizal fungi to mobilize inorganic nutrients might be species specific (van Schöll et al. 2006b; Plassard et al. 2011). In vitro experiments have demonstrated that mycelia of mushrooms can solubilize various types of metals and minerals (Fomina et al. 2006, 2007). On the other hand, this process was often accompanied by precipitation of various “mycogenic” minerals on fungal hyphae (Gadd et al. 2012; Rhee et al. 2012). The interactions between ectomycorrhizal fungi and metal elements have been recently reviewed by Urban (2011). The complex chemical action of macrofungi in soils described above leads, however, to a very interesting and not yet well-understood phenomenon: uptake, transport, and accumulation of various chemical elements in mushroom fruit bodies (Fig. 1).
Apart from hyphae (mycelium), rhizomorphs, which are root-like structures and which are known to be spread by species over a huge area of forest, also take part in the uptake of mineral elements. The contribution of rhizomorphs as a highly efficient medium for water and mineral compounds uptake from soils seems to explain the presence of Hg and Ag in fruiting bodies of Armillaria solidipes (Falandysz et al. 2012e; J.F., unpublished). An individual organism of Armillaria bulbosa could spread the mycelium and rhizomorphs over 150,000 m2 of forest (Smith et al. 1992).
Historical and subject overview
The first reports on the chemical composition of macrofungal fruit bodies appeared more than 100 years ago (Zellner 1907) and covered several macroelements including Fe and Mn. Curious enough, Friese (1929) had reported strikingly high Fe concentrations in Suillus variegatus that were rediscovered 46 years later (Drbal et al. 1975a). However, reliable data appeared with the development of advanced instruments and validated analytical methods, especially after 1970 (Drbal et al. 1975a, b; Stijve and Besson 1976; Byrne et al. 1976; Bakken and Olsen 1990; Falandysz et al. 2001). Very high concentrations of toxic metallic elements (Hg, Cd), toxic metalloids (As), essential and toxic nonmetal (Se), and other elements (Ag, Au, Cs, Rb, V, Zn) found in mushrooms from “background areas” have led to many studies which are, however, mostly from European countries. These studies were focused especially on:
Toxic metallic elements and metalloids (As, Sb) which might represent a risk for mushroom consumers (see below)
Possibilities of using mushrooms for environmental monitoring (Wondratschek and Röder 1993)
Radioactive contamination before and after the Chernobyl accident (Reisinger 1994; see below)
The most recent studies usually considered various ecological/environmental aspects (Collin-Hansen et al. 2005; Falandysz et al. 2008a, 2012a; Borovička et al. 2010a; Vinichuk et al. 2011; Aloupi et al. 2011; Gryndler et al. 2012) or molecular approaches are applied to investigate metal transport and sequestration in macrofungi (Courbot et al. 2004; Ramesh et al. 2009; Blaudez and Chalot 2011; Osobová et al. 2011).
Bioaccumulation in macrofungi
In contrast to vascular plants in which high concentrations of metals are mostly observed above metal-rich soils (Kabata-Pendias 2011), macrofungi can accumulate extremely high concentrations of metallic elements even when growing above soils with low metal contents. Furthermore, macrofungi reveal variable and highly specific ability to take up various trace elements (metallic elements, metalloids, and halogens) from soils and accumulate them in their fruit bodies. The ratio of an element in fruit body to its concentration in soil or, more specifically, to its mobility in soil (i.e., extractability by appropriate chemicals), so-called bioaccumulation factor (BAF), describes the ability of a fungus to accumulate a particular element. Apart from BAF, some other synonymous unit-less terms (transfer rate; transfer factor; transfer coefficient; translocation factor; concentration ratio; enrichment factor; index of bioaccumulatiuon, bioconcentration factor), which are simply a quotient from element concentration distributed between two phases, are also used by authors to estimate the potential of species to accumulate elements from soils or other substratum.
Elements typically accumulated in (at least some) macrofungi (BAF > 1) include Au, Ag, As, Br, Cd, Cl, Cs, Cu, Hg, Rb, Se, V, and Zn. Elements with typically low concentrations in macrofungi (BAF < 1) include Co, Cr, F, I, Ni, Sb, Sn, Th, U, and rare earth elements.
In some cases, concentrations of metallic element or metalloid might be rather high in some macrofungi (e.g., 10 or more times greater than in common ones, but BAF < 1); this phenomenon has been reported for Fe in S. variegatus and Hygrophoropsis aurantiaca, Co in Agaricus spp., Mn in Phallaceae and Panaeolus spp., Pb in Lycoperdon, and Sb in Suillus spp. and Chalciporus piperatus (Falandysz et al. 2001b; Borovička et al. 2006).
Factors influencing the bioaccumulation of trace elements in macrofungi and the biological importance of the accumulation process itself are poorly understood. However, the following fundamentals have been recognized:
Natural factors (bedrock geochemistry): The type of geological bedrock influences the concentrations of trace elements. Furthermore, pH/Eh conditions, organic matter content, and other factors influence the “mobility” of elements and their availability to biota (Kabata-Pendias 2011). The influence of these factors on trace element uptake in macrofungi has been poorly investigated. Gast et al. (1988) did not find any influence of soil pH or organic matter on Cd, Cu, Pb, and Zn in Amanita muscaria, Amanita rubescens, Hygrophoropsis aurantiaca, Lepista nabularis, Paxillus involutus, and Suillus luteus that emerged in natural habitats. In other studies, they did not influence the accumulation of Ag, Al, Ba, Ca, Cd, Co, Cr, Cu, Fe, Hg, K, Mg, Mn, Na, Ni, Sr, Pb, Rb, and Zn by A. muscaria, P. involutus, and Leccinum scabrum (Brzostowski et al. 2009, 2011a; Falandysz and Bielawski 2007; Falandysz and Brzostowski 2007; J.F., unpublished).
Concentrations of Ni and Cr were elevated in macrofungi from serpentine soils (Aloupi et al. 2011). Interestingly, metal concentrations in fruit bodies of ectomycorrhizal fungi growing on the same site can/could be very similar over the years (Brzostowski et al. 2011b; J.B., unpublished). The influence of environmental factors was studied also by Campos et al. (2009) who, however, used an inappropriate analytical method, and the published results are not reliable—see Borovička et al. (2011). As demonstrated in a study by Cen et al. (2012), the addition of chelating agents such as ethylenediaminetetraacetic acid and nitrilotriacetate to soil in a pot study enhanced the bioaccumulation of Cd, Cu, and Pb in Coprinus comatus, while the addition of citric acid did not.
Metalliferous areas and environmental pollution: Naturally or artificially elevated levels of metals in soils usually result in greater concentrations in fruit bodies. This has been demonstrated for many elements including Au (Borovička et al. 2010a), Ag (Borovička et al. 2005, 2010b; Kojta et al. 2012), As (Larsen et al. 1998), Cd (Kalač et al. 1991; Falandysz et al. 2011), Cu (Svoboda et al. 2000), Hg (Bargagli and Baldi 1984; Falandysz et al. 2012c, 2012e), Ni (Barcan et al. 1998), Pb (Kalač et al. 1991), and Sb (Borovička et al. 2006).
Fungal lifestyle: Concentrations of Hg, Cd, Pb and Pb are usually greater in terrestrial saprotrophs than those in ectomycorrhizal fungi (Borovička and Řanda 2007 and many others). On the other hand, concentrations of alkali metals, Rb and Cs, are generally greater in ectomycorrhizal species (Klán et al. 1988; Řanda and Kučera 2004; see also Table 12). Some of these differences might be explained by contrasting nutrition strategy of both groups and consequently the differences in the distribution of mycelia in soil profiles (Luis et al. 2005; Christ et al. 2011).
Bioaccumulation of metallic elements, metalloids and non-metals (Se) in fruit bodies is highly species specific: Some macrofungi are able to accumulate elements much more effectively than others; the ability to accumulate a particular element is a characteristic feature of a particular fungal species. In various macrofungi growing above the same substrate, concentrations of elements can vary over a wide range and can differ even a thousand times from species to species (see, e.g., Lavola et al. 2011).
The accumulation process can be highly element specific: Macrofungi may even discriminate elements with similar properties and chemical behavior (homologues). A typical example might be hyperaccumulation/discrimination of As/Sb in Sarcosphaera coronaria (see below).
An extraordinarily high ability of a plant or macrofungal species to accumulate a trace element in its tissues is called hyperaccumulation. To be defined as a hyperaccumulator, the metal concentration should be at least about 100 times greater than the values to be expected in nonaccumulating species on the same substrate (for discussion on this term, see Borovička et al. 2007).
A. muscaria was the first recognized fungal hyperaccumulator. This temperate zone species hyperaccumulates vanadium, and this also applies to its relatives such as Amanita regalis and Amanita velatipes. Whereas concentrations of V in other mushrooms hardly exceed 1 mg kg−1 (related to dry matter, dm), these Amanita spp. accumulate even hundreds of milligram per kilogram of dm. In fruit body biomass, V is present as amavadin, an eight-coordinate V complex of unclear biological function (Garner et al. 2000).
S. coronaria, an ectomycorrhizal ascomycete growing on calcareous bedrock in temperate climate regions, hyperaccumulates arsenic. Despite being relatively low naturally in soils, the As concentrations are commonly as high as 1,000 mg kg−1 dm in fruit bodies of this species (Stijve et al. 1990), with the greatest ever reported value being 7,090 mg kg−1 dm (Borovička 2004). The main As compound identified in biomass was methylarsonic acid (Byrne et al. 1995). Although less toxic than arsenic trioxide, it is still relatively dangerous. Therefore, the Pink Crown should not be eaten though it used to be considered edible in Europe. Hyperaccumulation of As occurs also in several Basidiomycetes (J.B., unpublished; and see also text below).
The most recently discovered hyperaccumulators are Amanita species of the section Lepidella (Borovička et al. 2007). The European Amanita strobiliformis like some others growing worldwide hyperaccumulates silver. Despite very low natural levels in soils (below 1 mg kg−1 dm), Ag concentrations in Amanita spp. may be more than 2,000 times greater and commonly amount to hundreds of milligram per kilogram of dry matter; the greatest reported value was 1,253 mg kg−1 dm. Investigation on the chemical form of Ag has revealed that A. strobiliformis employs cysteine-rich, low molecular weight proteins (metallothioneins) to sequester intracellular Ag in its fruit bodies and extraradical mycelium (Osobová et al. 2011).
The biological importance of elemental hyperaccumulation in macrofungi is unclear but this extraordinary feature can be thought of in theory as being attributable to the “defense hypothesis” (Boyd 2007). It has been shown in vascular plants that elemental hyperaccumulation may have several functions, including plant defense against natural enemies; at least some tests have demonstrated defense by hyperaccumulated As, Cd, Ni, Se, and Zn in plants. In view of this fact, the high Ag concentrations in hyperaccumulating macrofungal species might have some protective effect against pathogenic microfungi, bacteria, insect larvae, or gastropoda, but this is yet to be tested. Interestingly, Gryndler et al. (2012) have demonstrated that Ag-rich fungal biomass strongly influences the soil bacterial community.
Edible mushrooms and mineral constituents
Numerous wild-grown mushrooms are more or less valued as gourmet by nations worldwide (Tüzen et al. 2007; Zhang et al. 2010; Costa-Silva et al. 2011; Li et al. 2011; Nnorom et al. 2012a; Giannaccini et al. 2012; Figs. S1–S4, Supporting material). Also, in China and elsewhere, mushrooms collected in the wild are still used in traditional medicine, e.g., Ganoderma lucidum (Zhao et al. 2004), which is also cultivated in China. Another example can be sclerotium (or storage tuber that is formed by dense mass of mycelium) of Wolfiporia extensa used in Chinese traditional medicine and of Pleurotus tuber-regium that are also considered a popular food (Figs. S5–S7, Supporting material). Products based on mycelium that were biotechnologically enriched in desired trace element could be considered possible nutraceuticals (food supplements), and an example can be Se-enriched mycelium of Lenitula edodes mushroom (Turło et al. 2010). There are growing attempts to enrich cultivated mushrooms with biologically active and medicine minerals desired in human nutrition, and typical examples are Se and Li (Zhao et al. 2004; Silva et al. 2010; Bhatia et al. 2011; Hong et al. 2011; Assunção et al. 2012).
Mushrooms are valued due to their aroma and taste, as well as their proteins, vitamins, and low fat contents, and they are considered as products rich in mineral compounds. Apart from the abundance of minerals desired in human nutrition in mushrooms, undesired potentially toxic elements including Cd and Hg also occur sometimes at elevated concentrations (Falandysz et al. 2011; Gucia et al. 2012a, b; Giannaccini et al. 2012; Jarzyńska et al. 2012a).
First of all, most of the estimated 2,000 species of edible wild mushrooms grown worldwide are poorly characterized with respect to their multi-mineral composition. Apart from the variability introduced by natural conditions (type of soil bedrock, habitat, environmental factors), little is known of the influence of the processing, storage, and cooking on the contents and changes in mineral compounds composition of mushrooms as well as their accessibility and bio-availability from mushroom meals to man (Svoboda et al. 2002; Sun et al. 2012). Certain mushrooms can be processed and cooked in various ways. An example is Tricholoma equestre, which is suitable for drying, pickling, salting, stewing, souring, and freezing. In a recipe on mushroom soups, “the Yellow Knights’ soup,” it is noted that the fresh specimens of T. equestre do not need to be blanched before soup cooking—that is the specimens, when “cleaned up, cut and well rinsed in running tap water, are poured directly into boiling bullion and boiled for 40 min”. A common practice is blanching of mushrooms (a short-time boiling) by boiling them for 2–3, 5, or 10 min and slightly salted water—depending on the cuisine recipes (Maćkiewicz and Falandysz 2012). Preservation of mushrooms by salting is a practice in China and is good for Boletus and other species (Figs. S8–S10 in Supporting material). Those factors can influence the content (with the possibility of leaching) and chemical species of trace elements of mushroom meals. In China, Tricholoma matsutake can be eaten raw, and raw Agaricus bisporus can be found in salads worldwide. However, this is no longer a common practice in the modern world, and eating of any mushroom raw is not recommended by the authors. When well cooked, mushrooms by volume could be important and attractive components of meals (Fig. S1 in Supporting material).
Some of the mineral constituents, including metallic elements, are macro- and micronutrients to mushrooms. The essential elements are K, P, Mg, Ca, Na, Zn, Cu, Mn, Ni, and Co, while many others have no known biological function. Selenium can be found in all mushrooms but species vary in their Se contents and a few can be considered abundant in this antioxidant (Falandysz 2008). As mentioned, example of elements that are well bioaccumulated by numerous species are Au, Ag, As, Br, Cd, Cl, Cs, Cu, Hg, Rb, Se, and Zn (BAF > 1). Lead, for which BAF is usually <1, is relatively abundant in forest topsoil in background areas and is also a common trace contaminant of mushrooms. Fungi have low potential to bioaccumulate Pb and this keeps its concentration it their flesh below actual limits of tolerable intake from foods (Chudzyński and Falandysz 2008; García et al. 2009; Frankowska et al. 2010; Jarzyńska et al. 2011, 2012b; Giannaccini et al. 2012; Jarzyńska and Falandysz 2012a, b; Malinowska et al. 2004; Rudawska and Leski 2005a, b; Szubstarska et al. 2012).
Macro and trace mineral constituents of nutritional value
Wild-grown edible mushrooms can contain certain minerals essential to humans at relatively high concentrations, and for trace elements such as Cu and Zn, published data are available for numerous but not all species. Some other essential elements depending on species are a little less or not covered at all in literature. However, this is changing in recent years as more and high quality data become available from scientific literature. Within this mini-review, focus is given mostly to elements that are of greater nutritional/medical and toxicological significance and largely by using popular wild-grown Boletus edulis and Macrolepiota procera and cultivated A. bisporus, Pleurotus ostreatus, and some other Pleurotus spp. and L. edodes for which some analytical data were published as examples.
Metals such as K, P, Mg, Ca, Na, Cu, and Zn are among the vital ions to body liquids and tissues and are co-factors of numerous enzymes, while their concentrations in the body of healthy biota are regulated. The flesh of mushrooms can be considered as rich in K and P, and it can also be considered as abundant in trace elements such as Cu and Zn. Both Cu and Zn in the flesh of mushrooms collected from background areas are of nutritional value for humans. The situation can be different if the mushrooms emerged at sites polluted with Cu or Zn. This is because in polluted soils other toxic metals (Cd, Pb, Hg) can co-occur with Cu and Zn and can be bioaccumulated to concentrations much above typical contents of edible species and could become noxious to mushrooms (Collin-Hansen et al. 2005).
Potassium plays many important roles as an essential metal in vegetation. This metal occurred in caps of B. edulis from many sites at 25 ± 0 to 29 ± 3 g kg−1 dm on average, and in stipes, at 20–40 % less (Table 1). The edible cap of M. procera is also rich in K, and its typical concentration is 26 ± 4 to 49 ± 14 g kg−1 dm (Table 1), but the stipes are sometimes richer in this element (Gucia et al. 2012a, b). Wild-grown P. tuber-regium showed K in sclerotia (storage tuber) at a concentration one order of magnitude less compared to the fruit bodies of cultivated Pleurotus spp. (Table 1). Mycelium compared to fruit bodies of wild-grown mushrooms is also one order of magnitude poorer in K (Vinichuk et al. 2011). The values of concentrations in Tables 1 and 12 imply that there are similarities in K contents of fruit bodies of macromycetes, while fluctuations seem be more due to the stage of maturity of the carpophore and the site rather than to the species of the fungus (Tables 1 and 12).
Phosphorus is abundant in wild-grown edible mushrooms and a concentration range of 10 ± 1 to 15 ± 2 g kg−1 dm was reported in the caps of M. procera, while the concentrations (Table 2) in stipes were 40–50 % less (Gucia et al. 2012a, b). The mushroom M. procera is more abundant in P than certain other wild-grown species for which data are available. For example, Leccinum duriusculum (rare species) and L. scabrum showed P in caps of 5.7 and 5.7 g kg−1 dm (median values), and in stipes, these were 1.5 and 2.2 g kg−1 dm, respectively (Jarzyńska and Falandysz 2012b; Zhang et al. 2012). For Suillus grevillei and Xerocomus badius, the concentrations of P are largely similar to those of Leccinum spp. (Table 2), while the values for S. grevillei and X. badius in stipes were much less (Chudzyński and Falandysz 2008; Kojta et al. 2012). The concentrations reported for Cantharellus cibarius (whole fruit bodies) did not deviate from those reported for the species mentioned (Table 2). Also for some cultivated Agaricus spp., Pleurotus spp., and L. edodes, the content of P was similar to that of wild-grown species but much less in commercially processed (conserved) A. bisporus and also in the sclerotia of P. tuber-regium (Table 2).
Sodium in the form of NaCl is added to many food products and meals, and the problem usually is its excessive intake but it is usually not in deficit in the human body. Mushrooms as organic food can be considered low in this element. For example, in the caps of B. edulis, the median sodium concentrations of 100 to 380 mg kg−1 dm and in M. procera at 40 to 500 mg kg−1 dm have been reported (Table 3). Stipes of B. edulis and M. procera are about twice more abundant in Na than the caps (Falandysz et al. 2011; Gucia et al. 2012a, b). The values of Na for B. edulis and M. procera seem to agree with the concentrations reported in some cultivated mushrooms, i.e., three Pleurotus spp. and L. edodes and of some other species but preserved (in brine in tin) A. bisporus is rich of hidden Na (Tables 3 and 12).
Magnesium occurs in a very similar concentration in many mushrooms both wild grown and cultivated (Table 4). Caps of B. edulis contained Mg at 680 to 930 mg kg−1 dm and less than half this concentration were in stipes (Falandysz et al. 2011). Magnesium contents of processed A. bisporus is about half the contents of unprocessed mushrooms, and it seems that large amounts of elements can be lost from this species when boiled in saline water (Table 4).
Calcium in caps of B. edulis, M. procera, and Leccinum spp. are in similar concentrations and more Ca have been reported in cultivated mushrooms (Table 5). An exception can be preserved (in brine in tin) A. bisporus that contained Ca at concentrations >2,000 mg kg−1 dm, but this could be due to Ca from industrial brine (Table 5). In B. edulis, M. procera, and Leccinum spp., both caps and stipes are similarly rich in Ca (Falandysz et al. 2011; Gucia et al. 2012a, b; Jarzyńska and Falandysz 2012a, b; Zhang et al. 2012).
Copper in caps of B. edulis from many sites was at 24 to 79 mg kg−1 dm (median) (Table 6), and the stipes contained less than half of these amounts (Falandysz et al. 2011). Some quality data on Cu for B. edulis are also available from other sources (Collin-Hansen et al. 2002; Řanda and Kučera 2004). The species Boletus tomentipes collected in Yunnan (China) seems to be less rich in Cu compared to B. edulis (Table 6). Some mushrooms of the genus Leccinum, which are related to the genus Boletus, showed Cu in a similar concentration, and Leccinum rufum with Cu contents of 45 to 97 (median) mg kg−1 dm in caps (Table 6) seems to be an exception. The stipes of Leccinum mushrooms contained around half Cu compared to the caps (Jarzyńska and Falandysz 2012a, b; J.F., unpublished; Zhang et al. 2012).
In the caps of M. procera, the contents of Cu (many individual samples from background sites) were between 83 and 230 (median) mg kg−1 dm (Table 6). The Italian authors examined caps and inedible stipes together (whole fruit bodies), and the Cu contents were similar as in the caps above, i.e., at 170 (median) mg kg−1 dm (Table 6). In stipes of M. procera, the contents of Cu can be the same as in caps or lower (Gucia et al. 2012a). Copper is an essential element and its uptake to some degree can be regulated by the fungus. Data reviewed above on Cu in B. edulis and M. procera are based on large sets of results and mushrooms collected from several sites. The data showed that apart from being statistically significant (0.05 < p < 0.01), spatial variations were noted for a particular species, while the contents of Cu can vary between species too. Hence, the significance of a particular species of mushrooms as a potential (and local) source of Cu to man can vary between regions, while differences in Cu content between species occur also.
Zinc in B. edulis was reported at between 100 and 210 mg kg−1 dm (median for caps and whole fruit bodies) and much lower values in B. tomentipes (Table 7). The content of Zn in stipes of B. edulis is usually about half or even less than in caps (Falandysz et al. 2008a). Similarly, the stipe of M. procera on average contained less Zn, about half the content in the cap (Gucia et al. 2012a). Cultivated A. bisporus, P. ostreatus, and L. edodes showed less Zn than A. subrufescens and in other wild-grown species reviewed in this paper (Table 7), but the number of data available for cultivated mushrooms is less. The edible wild-grown and cultivated mushrooms can be considered as foods relatively abundant in/with K, Cu, and Zn, and taking into consideration that these elements are also abundant in many staple foods, clearly there is no need to bio-fortify any mushroom with them.
Selenium and lithium in mushrooms as examples of highly/specifically desired micronutrients
Selenium is frequently deficient in soils and foods worldwide, and in wild-grown mushrooms, its content varies depending on the species (Falandysz 2008; Rayman 2008; Jarzyńska and Falandysz 2011a, b). This element is highly potent and has great health impacts. It is needed in the synthesis of mammalian selenoenzymes, and glutathione peroxidase-3 and selenoprotein-P are dominant Se compounds secreted in the blood. There are many factors for which Se plays a role, and these need to be considered when deciding on the optimal human supplementation with dietary Se (or its species) including a key co-occurrence in vitamin E and other antioxidants but also other mineral constituents such as hazardous As, Cd, and Hg (Jarzyńska and Falandysz 2011a, b).
A good bio-available source of Se from foods is needed for the full expression of selenoproteins with antioxidant function and particularly in diseases associated with oxidative stress. Dietary daily intake of Se for humans is recommended at 57 μg (range 30–85 μg), but this sometimes can be insufficient for the expression of selenoprotein-P, and its high adequate intake rate is estimated for approximately 100–200 μg per day (Rayman 2008). The margin of safety for Se is narrow. In the past, overdosing causing selenosis happened to horses (Se poisoning) grazing on Se-hyperaccumulating plants and humans eating foods from areas contaminated with Se-containing waste.
Of around 200 edible species reviewed (belonging to 21 families and 56 genera), most were relatively low in Se, i.e., <1 mg kg−1 dm (Falandysz 2008). The fruit bodies of some species of wild-grown edible mushrooms are naturally rich in selenium. Albatrellus pes-caprae with ~200 mg kg−1 dm on the average (maximum up to 370 mg kg−1 dm) is the richest among the species surveyed. Several other representatives of the genus Albatrellus are also abundant in Se. Of the most popular edible wild-grown mushrooms, the B. edulis is considered abundant in Se as well; on average, it contains ~20 mg kg−1 dm (maximum of up to 70 mg kg−1 dm). Some species of the genus Boletus, such as Boletus pinophilus, Boletus aereus, Boletus reticulatus, and Boletus erythropus can also accumulate considerable amounts of selenium. Some other species relatively rich in Se include A. strobiliformis, which contains, on average, ~20 mg kg−1 dm (up to 37 mg kg−1 dm), and the Lycoperdon spp., with an average of ~5 mg kg−1 dm (Falandysz 2008). The mushroom M. procera with a range of ~3–5 to <10 mg Se kg−1 dm in caps can be also be considered to be rich in this element (Tüzen et al. 2007; Falandysz 2008; Giannaccini et al. 2012).
For several wild-grown species of the genus Agaricus, the selenium content (~5 mg kg−1 dm) is much greater than that from cultivated Champignon mushroom; these include Agaricus bitorquis, Agaricus campestris, Agaricus augustus, Agaricus macrosporus, and Agaricus sylvaticus (Falandysz 2008). In cultivated commercially available A. bisporus, the contents of Se were between 1.9 ± 0.1 and 3.7 ± 0.9 mg kg−1 dm (Vetter 2003) and 0.28 ± 0.68 and 1.4 ± 0.1 mg kg−1 dm (Costa-Silva et al. 2011). Canned (preserved) commercially available A. bisporus was much less in Se (<0.5 mg kg−1 dm) compared to fresh mushrooms examined by Vetter (2003). And in recent studies of cultivated P. ostreatus from the European market, Se was at 0.10 ± 0.01 to 0.26 ± 0.20 mg kg−1 dm (Costa-Silva et al. 2011), while the Se content of samples from the USA was 0.2 mg kg−1 dm (Hong et al. 2011).
Different Se compounds can be utilized in the formation of Se enzymes, and the most desired is Se cysteine, which is low in plant or mushroom proteins compared to Se methionine. In mushrooms, several Se compounds have been identified including selenomethionine, selenocysteine, Se methylselenocysteine, selenite, seleno-polysaccharides, and several other unidentified seleno-compounds that occur in varying proportions (Falandysz 2008).
In early attempts to produce Se-enriched edible mushrooms (using A. bisporus and L. edodes), inorganic Se salts were used as additives to the substratum (Falandysz 2008). Compost fortified with inorganic Se (Na2SeO3) at a rate of 8.1 and 14.4 mg kg has been used, and the Se-enriched Pleurotus eryngii contained, respectively, 4.6 and 9.3 mg Se kg−1 dm (<1.5 mg kg−1 dm in reference fruit bodies) (Estrada et al. 2009).
Recently, a new approach to obtain Se-enriched foods is by the use of Se-laden vegetation instead of inorganic Se in the cultivation of mushrooms. In a study by Hong et al. (2011), the fruit bodies of P. ostreatus emerged in Se-laden plant compost contained 2.9 mg Se kg−1 dm. In experiments with Pleurotus florida cultivated using Se-rich wheat straw (Se in straw was at 26 ± 0, and grains contained 89 ± 1 mg kg−1 dm) from the seleniferous belt of Punjab of India, the Se content of fruit bodies was spectacularly high at 130 ± 2 mg kg−1 dm, and in reference mushrooms, it was 0.16 ± 0.01 mg kg−1 dm (Bhatia et al. 2011).
Also available are data on the impact of boiling/blanching on the Se content of A. bisporus (44 % loss) and in Lactarius torminosus (32 % loss). Data on Se bioavailability from a meal containing B. edulis (weak bioavailability) and cultivated A. bisporus and wild-grown B. edulis (weak bioavailability) have been reported too. The intake of Se-enriched A. bisporus (53 mg kg−1 dm) increased the activities of the liver and mammary glutathione S-transferase (GCT) (cited after Falandysz 2008).
In a recent study on the availability of Se to rats that were fed with Se-enriched P. ostreatus (feed contained 0.15, 0.30, or 0.45 mg Se kg−1) and ordinary feed fortified with sodium selenate (0.15 Se kg−1), the profile of some Se-containing proteins in plasma was similar for all animals, while the rate of Se absorption was not given. Selenium from mushroom was the highest in a peptide of 8 kDa size, while the feed with mushroom component resulted in a greatest content of this peptide in rats’ blood (7 μg Se L−1) compared to 2–5 μg Se L−1 from other diets (Silva et al. 2010).
A mushroom meal that contains 0.005–0.05 mg Se kg−1 wet weight (many species) when consumed in quantities of 100 or 300 g—assuming a limited availability of Se from mushrooms (circa 15–25 %) and its loss (circa 40 %) during mushroom blanching—can provide, respectively, circa 0.6–6 and 1.8–18 μg of bioavailable Se, respectively. Hence, if the values of the recommended daily intake of 57 μg Se (range 30–85 μg) and of high adequate intake of 100–200 μg are taken into account, the species of wild-grown mushrooms rich in Se and also cultivated mushrooms that are well bio-enriched in Se can be considered as good sources of this element for mushroom fanciers. From B. edulis and B. reticulatus with an average content of 20 mg Se kg−1 dm, the intake of bioaccessible Se is 24 μg (for a 100-g mushroom portion) and 72 μg (for a 300-g portion), and intake from B. pinophilus can be twofold greater. And if Boletus spp. is prepared in a manner allowing only on a negligible if any loss of “body liquid”—and so also of minerals—out of a meal (e.g., a specific Chinese or other cuisine recipes), certainly the intake will be higher. The problem in assessing intake is the fact that the same mushroom species when processed or cooked in various ways, the leakages/leaching of minerals could be anticipated. Also, the contents of minerals in industrially processed mushrooms can vary significantly from what is in fresh mushrooms, and a typical example is the data for fresh and preserved A. bisporus (Vetter 2003).
Lithium is a trace mineral in biota, and the lithium salt, Li2CO3, is therapeutic for neurodisorders (i.e., as a psychiatric medicine) for many years, but a deeper insight of its role has not been discovered. Mushrooms seem to be low in this element. In a study by Vetter (2005), the Li content of 14 taxa of mushrooms was between 0.064 ± 0.039 and 0.19 ± 0.13 mg kg−1 dm and higher amounts were found in A. strobiliformis (0.52 ± 0.55 mg kg−1 dm), Craterellus cornucopioides (0.116 ± 0.70 mg kg−1 dm), and Psathyrella candolleana (0.39 ± 0.38 mg kg−1 dm). However, entirely different data—with a range from 0.030 to 12 mg kg−1 dm (for some species, only a single result reported as single specimen was examined)—have been reported recently for Russula virescens, Trogia spp., Lactarius hygrophoroides, Thelephora vialis, Russula lepida, Amanita exitialis, and T. matsutake collected in the northern parts of Yunnan in China (Yin et al. 2012). In that study, except for Trogia spp., all other species contained Li at >1.0 and most at >2.0 mg kg−1 dm, and this needs to be clarified in further studies.
In a study by Giannaccini et al. (2012), the Li content of B. edulis was at 0.2 ± 0.2 (median 0.1 and range 0.04–0.9) mg kg−1 dm and of M. procera at 0.3 ± 0.4 (median 0.1 and range 0.03–1.6) mg kg−1 dm, and these results agree with the findings for other mushrooms cited above as reported by Vetter (2005). In the only study on bio-enrichment of mushrooms with Li known, the species P. ostreatus cultivated in the substratum (coffee husk; 94 mg Li kg−1 dm) fortified with LiCl (62.5 to 500 mg kg−1) accumulated this element in fruit bodies and as the authors claim: “Li concentration in mushrooms was directly influenced by increasing LiCl concentration in the substrate (p < 0.05)” (Assunção et al. 2012). However, the Li content of nonenriched P. ostreatus in that study was around 50 mg kg−1 dm (no clear figures were given), and this is about the highest Li concentration reported for mushrooms so far. One thing noticed, however, is that the accessibility (in vitro gastrointestinal digestion) of Li was higher from bio-enriched mushrooms than from common (nonenriched) mushrooms and, in practice, is not acceptable for use in psychiatric drug (Li2CO3) (Assunção et al. 2012).
Toxic mineral constituents in mushrooms (Hg, As, Cd, Pb, Ag)
Among the hazardous minerals that occur naturally in substrates decomposed by fungi and in the flesh of mushrooms are Hg, As, Cd, Pb, and Ag. Metallic elements such as Hg, Cd, Pb, and Ag and the metalloid As, and other, due to mining, metallurgy, use, wastes, and recovery processes, are classified as environmental pollutants. Elevated contents of Hg, Cd, Pb, and Ag in mushrooms were confirmed at polluted sites (see below).
Mercury can be efficiently bioaccumulated by many mushrooms and especially when it is present in small concentrations in forest soils, e.g., for caps of M. procera, the BAF values vary from 16 ± 6 to 220 ± 110 (total range from 0.52 to 470), and for B. edulis, these were from 41 ± 6 to 130 ± 39 (total variation between 13 and 170) (Falandysz et al. 2007a; Falandysz and Gucia 2008). The problem of Hg in mushrooms has been evaluated in detail for many species from different countries in recent times (Falandysz and Chwir 1997; Falandysz 2002; Falandysz and Bielawski 2001, 2007; Alonso et al. 2000; Falandysz et al. 2001a, 2002a, b, c, d, 2003a, b, c, d, 2004, 2007a, b, f, 2012c, d, e, f, 2013; Tüzen and Soylak 2005; Cocchi et al. 2006; Falandysz and Brzostowski 2007; Chudzyński et al. 2009, 2011; Melgar et al. 2009; Nasr and Arp 2011; Pilz et al. 2011; Reider et al. 2011; Chojnacka et al. 2012; Drewnowska et al. 2012a, b; Giannaccini et al. 2012; Maćkiewicz and Falandysz 2012; Nnorom et al. 2012a).
Data on the rates of highly neurotoxic methylmercury (MeHg) bioaccumulation by mushrooms vary between studies, and some have shown that it is a form more bioavailable compared to inorganic forms (considered as “total” Hg). MeHg is less abundant than the inorganic Hg, both in the wild-growing and cultivated mushrooms, i.e., it is found between ~2 and 60 % of total Hg, though the proportions vary depending on the investigator, concentration, and analytical method (Table 8) (Falandysz 2010; Fischer et al. 1995; Pilz et al. 2011; Reider et al. 2011).
Mushrooms B. edulis and M. procera even when they emerged at background sites in Italy, Poland, and Spain can contain total Hg at elevated concentrations, i.e., for caps, was at 1.2 ± 1.4 to 7.6 ± 3.1 (total range 0.02 to 14) mg kg−1 dm and, for whole fruit bodies, at 1.2 ± 0.7 to 8.4 ± 7.4 (0.05 to 22) mg kg−1 dm, respectively (Falandysz et al. 2007a, b; Melgar et al. 2009; Giannaccini et al. 2012). They can be a source of elevated Hg intake. For example, in a study of M. procera, the median Hg concentration in caps varied for the sites between 1.3 and 7.0 mg kg−1 dm (0.13 and 0.7 mg kg−1 fresh weight; assuming water content is 90 %). The estimated intake of Hg resulting from the consumption of 300 or 500 g portions of caps was assessed as 39–210 and 65–350 μg, and this is equivalent to 0.65–3.5 and 1.1–5.8 μg kg−1 body mass (an adult of 60 kg bm) (Gucia et al. 2012b). It was concluded, that if taken into account, that provisionally tolerable weekly intake (PTWI) of Hg is 300 μg (equivalent to 5 or 0.7 μg kg−1 bm per day), and a reference dose of 0.3 μg kg−1 bm per day, Hg in caps of M. procera for some pristine areas might be of concern especially if eaten by fanciers frequently in the mushrooming season.
Both B. edulis and of M. procera apart from Hg can also contain Se (especially B. edulis) at high concentrations (see above), and this can have protective roles against Hg in biological activity but no facts are known. The accessibility and bioavailability of Hg from mushroom meals is unknown.
Wood-decaying mushroom species are low in Hg compared to the numerous soil mushrooms, and good examples are Pleurotus spp. with P. ostreatus containing between 0.028 ± 0.008 and 0.031 ± 0.011 in caps and 0.028 ± 0.006 and 0.0370 ± 0.005 mg kg−1 dm in stipes (Nnorom et al. 2012a). The sclerotia of wood-decaying P. tuber-regium are low in Hg and did contain from 0.024 ± 0.036 to 0.048 ± 0.030 mg kg−1 dm (Nnorom et al. 2012a). Also wood-decaying species such as A. solidipes that has of root-like rhizomorphs (tentacles, bootlaces) can be more abundant in Hg—specimens collected from two background areas of Poland showed Hg in caps of 0.020 ± 0.008 to 0.070 ± 0.020 mg kg−1 dm, on average, and significantly more, i.e., between 0.11 ± 0.03 and 0.30 ± 0.07 mg kg−1 dm was observed for specimens from ten other background sites (Falandysz et al. 2012e).
Arsenic in a real environment (nature) is the most hazardous inorganic element due to the carcinogenic risk, and there are no safe levels of arsenic. Different mushrooms can respond in different ways for the same chemical elements contained in the substratum where they live and a good example seems to be just a case of As. Many mushrooms are usually low in As (well <0.5 mg kg−1 dm) (Stijve et al. 1990; Giannaccini et al. 2012; Li et al. 2011; Liu et al. 2012). Some mushrooms are specifically rich in this metalloid, i.e., Laccaria amethystina with up to 250 mg kg−1 dm and Laccaria fraterna with up to 270 mg kg−1 dm (Stijve et al. 1990). Arsenic in S. coronaria can be at concentrations of up to 2,000 mg kg−1 dm and is stored mainly in the form of methylarsonic acid (Byrne et al. 1995). Arsenic accumulated by L. amethystina in the flesh was in the form of dimethylarsinic acid (the most identified form), methylarsonic acid, trimethylarsine oxide, arsenic acid, and arsenobetaine and insoluble in water and unidentified arsenicals contributed to total As in 15 to 32 % (Larsen et al. 1998; Stijve et al. 1990). At a site contaminated with As in Denmark, the metalloid content of L. amethystina was up to 1,400 mg kg−1 dm and dimethylarsinic acid dominated (at 68–74 % of total As) and the As content of L. amethystina at a reference site was between 23 and 77 mg kg−1 dm (Larsen et al. 1998).
Mushrooms that bioaccumulate As include Sarcodon imbricatus, Entoloma lividum, Lycoperdon perlatum, and some Agaricus spp. (Byrne et al. 1995). Arsenobetaine that is the major As compound in S. imbricatus, A. sylvaticus, and A. moelleri is considered much less toxic than many other naturally occurring types of arsenic. In E. lividum, the major arsenicals are the arsenite and the arsenate (Byrne et al. 1995). At the gold mine site contaminated with As in Yellowknife of Canada, the metalloid content of non-As accumulators was elevated, i.e., at 8.3 mg kg−1 dm in L. scabrum, 14 mg kg−1 dm in Psathyrella candolleana, and 36 mg kg−1 dm in P. involutus (Koch et al. 2000). In two other species, potential As accumulators, the concentrations were 410 mg kg−1 dm in C. comatus and 1,000 mg kg−1 dm in Lycoperdon pyriforme. In certain mushrooms, arsenobetaine was dominant as water-soluble arsenic compound, while in other species several compounds have been found and the proportions of arsenicals contained varied between them (Koch et al. 2000).
Cultivated A. bisporus when they emerge at the substratum fortified with as much as 1,000 mg As kg−1 dm (added as As2O5) weakly accumulated this metalloid, i.e., the value of BAF was 0.0009. In a control experiment, A. bisporus cultivated in a typical (clean) substratum that contained 3.8 mg As kg−1 dm [several As(III) and As(V) compounds were determined] contained in the flesh 0.50 mg As kg−1 dm, and BAF for total As was 0.13 (Soeroes et al. 2005). Cultivated mushrooms such as A. bisporus, Agaricus spp., P. ostreatus, P. florida, P. eryngii, P. ostreatus, Pleurotus salmoneo-stramineus, and L. edodes purchased in Brazil contained As in concentrations between 0.009 and 0.210 mg kg−1 dm (Maihara et al. 2008).
Cadmium as indicated earlier is well bioaccumulated and can be found at elevated concentrations in wild-grown mushrooms. This metal in the flesh of edible wild mushrooms is among the toxic substances of concern. The maximum concentration of Cd permitted by the European Union regulation in cultivated A. bisporus, P. ostreatus, and L. edodes is 0.20 mg kg−1 fw (equivalent to 2.0 mg kg−1 dm, assuming 90 % moisture), and for other mushrooms, it is 1.0 mg kg−1 fw (10 mg kg−1 dm) (cited after Gucia et al. 2012b).
Wild-grown mushrooms frequently contain Cd in a concentration exceeding 2.0 mg kg−1 dm but rarely above 10 mg kg−1 dm. An example is the highly valued and tasty B. edulis and M. procera mushrooms for which several data are available and for numerous and also for some species of the genus Leccinum (Table 9). Cadmium concentration exceeding 10 mg kg−1 dm can be observed for a few individual samples at unpolluted areas, but at areas contaminated with Cd, this threshold can be exceeded frequently.
Cultivated mushrooms such as A. bisporus, P. ostreatus, and L. edodes from Hungary showed Cd in caps of 0.17 ± 0.13, 0.91 ± 0.32, and 0.71 ± 0.48 mg kg−1 dm (Vetter et al. 2005), and this is at the lower edge of the average Cd concentrations noted in some wild-grown species (Table 9). The reported Cd contents of A. bisporus, Agaricus spp., P. ostreatus, P. florida, P. eryngii, P. salmoneo-stramineus, and L. edodes on sale (or purchased) in Brazil are 0.011 to 0.23 mg kg−1 dm, and these are only weakly contaminated (Maihara et al. 2008). Surprisingly high concentration of Cd with an average value of 10 ± 1 mg kg−1 dm, which exceeds the European Union limit of 2.0 mg kg−1 dm by fivefold (see below), has been noted in the fruit bodies of commercially cultivated Agaricus blazei bought at a market in Kunming (Yunnan, China) (Sun et al. 2012). The PTWI set by the Joint FAO/WHO Expert Committee on Food Additives for Cd is 7 mg kg−1 bm (equivalent to 1 mg kg−1 bm per day) (from Gucia et al. 2012b), and a tolerable weekly intake (TWI) of 2.5 μg/kg bw (equivalent to 0.36 mg kg−1 bm per day) was established by EFSA (from Gucia et al. 2012b).
M. procera is a mushroom with a large size and its caps are highly valued by mushrooming fanciers. In one study, Cd intake resulting from the consumption of a 300- or 500-g portion of caps of M. procera was estimated as 4.7–111 and 24.5–185 μg (median Cd content between 0.049 and 0.37 mg kg−1 fw, assuming water content of 90 %), and these are equivalent to 0.078–1.85 and 0.41–3.1 μg kg−1 bm (for an adult of 60 kg bm) (Gucia et al. 2012b). It was concluded in this study by Gucia et al. (2012b) that in a good “mushroom” year, the consumption of large quantities of M. procera will lead to a short time (2 weeks to up to 2 months) exposure of fanciers to elevated Cd doses that exceeded the PTWI and TWI recommendations. Hence, Cd in caps of M. procera at some of the sites surveyed might be of concern to consumers, if eaten frequently by an individual in the mushrooming season.
Cadmium is among the minerals leached out of fruit bodies during boiling. The boiling and microwaving, with water, of A. blazei reduces its Cd content by 36 and 30 %, respectively (Sun et al. 2012). Accessibility of Cd from mushroom meals is more or less limited (cited after Gucia et al. 2012b). Accessibility of Cd from raw A. blazei will be greater (78 % by stomach and 69 % by gastrointestinal mimetic digestion) compared to when the mushrooms are boiled (51 and 46 %) and microwaved (58 and 50 %) (Sun et al. 2012). It should be noted that we do not recommend eating of any mushroom raw, and one of the reasons is agaritin, which is a phenylhydrazine derivative present in mushrooms of the genus Agaricus and that is hazardous to human health (Andersson and Gry 2004). Agaritin is deactivated when mushrooms are heat-cooked.
Lead as discussed earlier is excluded in mushrooms (BAF < 1), but this toxic metallic element compared to Cd or Hg is more abundant in the top layers of forest soils. For example, Pb in the top layer of soils beneath B. edulis and/or M. procera in the mountain areas of Tuscany of Italy was at 26 to 47 mg kg−1 dm (Giannaccini et al. 2012), at 6.7 to 37 mg kg−1 dm in Tucholskie forests of Poland (Jarzyńska et al. 2011), and 26 to 270 mg kg−1 dm in the top soil beneath X. badius at the forested mine dump site of a medieval gold and copper mine in Sudety mountains (Kojta et al. 2012). Hence, even if the potential to bioaccumulate Pb by species is low (BAF < 1), a quantity of Pb sequestered in the flesh by a small portion of mushrooms that emerged at “unpolluted” sites can ordinarily be of health concern (Table 10), but metal accessibility from this type of food is unknown. The maximum concentration of Pb permitted by the European Union regulation in cultivated A. bisporus, P. ostreatus, and L. edodes is 0.3 mg kg−1 fw (equivalent to 3.0 mg kg−1 dm, assuming 90 % moisture) (cited after Gucia et al. 2012b).
In a recent study, the concentrations of Pb in hymenophore and the rest of the fruit body of such edible but probably not frequently eaten species such as C. comatus, A. campestris, and Lepista nuda were at 3.6 and 4.1, 3.0 and 2.2, and 2.5 and 2.3 mg kg−1 dm (no statistical difference between those morphological parts was noted) (García et al. 2009). In cultivated species, Pb concentrations were mostly low, below 3.0 mg kg−1 dm, and examples are data from Mexico where A. bisporus (caps) contained on average 0.41 mg kg−1 dm and P. ostreatus (whole) 0.91 mg kg−1 dm, while the spread of data for both species from reports on global scale is wide (Muñoz et al. 2005).
The acceptable daily intake of Pb for adults is between 0.21 and 0.25 mg per day and 1.5 and 1.75 mg per week (from Jarzyńska and Falandysz 2011a, b). In the case of M. procera, the estimated Pb intake from consumption of 300 or 500 g caps was 42–267 and 70–445 μg per meal, respectively. These values were based on the median concentrations of Pb found. It was concluded that, at some sites, the Pb intake rates show a cause for concern associated with Pb resulting from the consumption of between 300 and 500 g caps daily, on a frequent basis in the mushrooming season (Gucia et al. 2012b).
Silver is toxic to animal cells and Ag+ ion is highly toxic to bacteria. This is because Ag ion has a high affinity for sulfhydryl, amino, and phosphate groups, and it readily complexes with many endogenous ligands of the mammalian body. As given earlier, Ag at background and in geoanomalous and contaminated areas is very efficiently bioaccumulated by many mushrooms (Borovička et al. 2007, 2010b; Falandysz et al. 1994a, b; Falandysz and Danisiewicz 1995; Kojta et al. 2012). Data on Ag in several mushrooms from areas with Ag anomaly can be found in the article by Borovička et al. (2010b).
Apart from hyperaccumulators of this element (see above), it can be found at elevated contents in popular species, e.g., M. procera that were collected from background areas contained up to 4.8 mg kg−1 dm (median value) (Table 11). Silver was found also in cultivated A. bisporus (Table 11), but the number of available data for cultivated mushrooms seems to be very limited. To our knowledge, no data were published on the accessibility of Ag from mushrooms (cooked) to man, and the content of this metal in foods is not regulated.
Radioactivity of mushrooms
Wild-grown mushrooms in several reports are described as biota that are efficient accumulators and bioindicators of environmental diffusion of radionuclides. Emphasis is frequently given on long-lived 137Cs that polluted the surface of the Earth due to global radioactive fallout after testing of nuclear weapons and from nuclear power plant accidents, but some others as well as naturally occurring radionuclides are also intensively studied in mushrooms (Horyna and Řanda 1988; Bakken and Olsen 1990; Tsvetnova and Shcheglov 1994; Dahlberg et al. 1997; Kirchner and Daillant 1998; Rühm et al. 1997; Skwarzec and Jakusik 2003; Strandberg 2004; Baeza et al. 2004a, b; Kostiainen 2007; Vaartamaa et al. 2009; Mietelski et al. 2002, 2010; Taira et al. 2011; Vinichuk et al. 2011; Castro et al. 2012; and many others).
The capacity of mushrooms to sequester radioactive elements in fruit bodies and so the rates of their uptake vary between species, and good examples to illustrate this are data on the contents of the most studied—137Cs. There is no reason for mushrooms to discriminate between stable and radioactive isotopes of elements when absorbed by the mycelium and accumulated in the mushroom flesh, but their accessibility at sites where the mycelium lives can be different. There are several types of radioactivity, and the decay of elements results in the emission of extremely toxic subatomic particles such as alpha (α) particle (helium nuclei, i.e., two protons, He2+) and less potent beta minus (energetic electrons, β −) and beta plus (β+, positrons) particles and also of gamma (γ) ray (photon) with nuclide’s half-life (T 1/2) equivalent respectively from several days to millions of years (Skwarzec 2012).
Some of the radioactive elements naturally occurring in nature that are the primordial non-series radionuclides of terrestrial (e.g., 40K and 87Rb) and cosmogenic origin (e.g., 3H, 7Be, 14C, 22Na) and that of uranium (238U), thorium (232Th), actino-uranium (235U), and neptunium (237 Np) decay series have been found in mushrooms, but published data are few (see below). The cosmogenic 3H, 7Be, 14C, and 22Na are among the most important radionuclides because of their long half-life (T 1/2) equivalent to 12.33 years for 3H, 53 days for 7Be, 5,740 years for 14C, and 2.6 years for 22Na, and they are of β − (3H, 14C) and β+ (22Na) radioactivity, and 7Be is capturing electrons. These cosmogenic radionuclides in foods are without radiotoxic importance because they occur at an extremely small concentration in nature (Skwarzec 2012).
The decay series radionuclides are 238U (T 1/2 of 4,500 million years; α), 232Th (T 1/2 of 14,100 million years; α), 235U (T 1/2 of 704 million years; α), and 237 Np (T 1/2 of 2.14 million years; α) series that during radioactive decay transform into many other radioactive elements, which can be, respectively, the emitters of α and β− particles. And apart from 238U, 232Th, 235U, and 237 Np, the most risky in foods are 234U (T 1/2 of 245,500 years; α) and 230Th (T 1/2 of 75,380 years; α), while much weaker source of radiation dose are 231 Pa (T 1/2 of 32,760 years; α), 228Th (T 1/2 of 1.9 years; α), 229Th (T 1/2 of 734 years; α), 227Th (T 1/2 of 18.7 days; α), 225Ac (T 1/2 of 10 days; α), 223U (T 1/2 of 159,200 years; α), and 210Po (T 1/2 of 138 days; α). Data on these types of element in mushrooms are almost non-existing and the exception is U for which many details can be found in the article by Gadd and Fomina (2011).
Since the 1940s, many radionuclides of anthropogenic origin have been released into the environment, and their sources relate to the testing of nuclear weapons, operation of nuclear power plants, radioactive waste disposal, and the manufacture of radioactive compounds. They are categorized into three groups: neutron activation products (1), fission products (2), and transuranic elements (3) (Skwarzec 2012).
The activation of stable isotopes by neutron irradiation can produce various radionuclides, and their major source in nature is nuclear weapon testing, nuclear reprocessing, nuclear power plants, and nuclear research. By using modern radioanalytical methods, it is possible to detect the activation products such as 22Na, 51Cr, 54Mn, 65Zn, 110mAg, and 124Sb. The most important, due to its strong radioactivity and long-life, of the neutron activation (1) products are radionuclides such as 54Mn (T 1/2 of 312 days; electrons capturing), 55Fe (T 1/2 of 2.737 years; electrons capturing), 60Co (T 1/2 of 5.2714 years; β −, γ), 63Ni (T 1/2 of 100.1 years; β −), 64Cu (T 1/2 of 12.7 days; β+), 110mAg (T 1/2 of 249.9 days; β −), 124Sb (T 1/2 of 60.2 days; β −), and 125Sb (T 1/2 of 2.76 years; β−). Some of these radionuclides have been reported in mushrooms (Gentili et al. 1991).
The most important due to strong radioactivity and long-life, the radioactive fission products (2) formed in the explosion of nuclear bombs, both the uranium and plutonium bombs are radionuclides such as: 90Sr (T 1/2 of 28.79 years; β−), 131I (T 1/2 of 8.02 days; β− and γ) and 137Cs (long-lived, T 1/2 of 30.17 years. As indicated earlier, 137Cs in mushrooms is well documented and data on both 137Cs and 134Cs, which have different half life-time, help to study sources of pollution of mushrooms with those nuclides and also diffusion rates in soils (Mietelski et al. 2010).
For explosions in the atmosphere, the depositions of those radionuclides reaching the earth are 78 % from stratospheric, 12 % from local, and 10 % from the tropospheric fallout (Skwarzec 2012). Radiocesium (137Cs) is the most relevant nuclide from this source in mushrooms (see below). Also disasters of nuclear power plants apart from heavy local pollution are relevant regional sources of those radionuclides and largely of 137Cs to soils, plants, mushrooms, and other biota in the food chain, e.g., the Chernobyl accident in 1986 (Dahlberg et al. 1997; Kostiainen 2007; Mietelski et al. 2010) and the Fukushima accident in 2011.
The transuranic elements (3) all are radioactive. Nuclear weapon tests and nuclear power production are major sources of transuranic elements to ambient environment (Np, Pu, Am, and Cm).
From the point of view of strong radioactivity and long-life time, the most important among naturally occurring radionuclides mentioned are 40K, 87Rb, and some of the 238U, 232Th, 235U, and 237 Np decay series. Radon from 238U decay series that emanates from the ground into the atmosphere decays to 210Pb (T 1/2 22 years; β −) and 210Po (T 1/2 138 days; α), and both return to the earth via wet deposition and on particles as dry deposition. The decay of 238U also produces 210Pb and 210Po in soil that are referred to as “supported” 210Pb and 210Po. Complementary sources of atmospheric 210Po include dust storms, coal-burning, forest fires, and plant exudates (Skwarzec 2012). Both 210Po and 210Pb are found in mushrooms (Mietelski et al. 2002; Skwarzec and Jakusik 2003; Baeza et al. 2004a).
Artificial radionuclides with 137Cs as the major nuclide can be found in any wild-grown mushroom due to its deposition from the global radioactive fallout and persistency, while concentrations in mushrooms vary between species and regions and also on time scale. And one of the reasons is that with time passing, the radionuclides also undergo the process of infiltration (diffusion from surface down) into deeper soil layers. This process can be very slow. Mushrooms can capture 137Cs from the surface of soils and decaying litter and from deeper soil layers, and this is related to fungal biology and placement of mycelium and depth and structure of soil layers. Fungi certainly are involved in biogeocycling of 137Cs and by decaying fruit bodies—like in the case of other mineral elements, fungus can recycle 137Cs from deeper soil layers back to the surface of forest carpet (Lepp et al. 1987; Smits and Hoffland 2009; Gryndler et al. 2012). More or less severe cases of mushroom contamination with artificial radionuclides have been reported at sites or regions of nuclear weapons testing and nuclear power plant failure (Taira et al. 2011).
Potassium and radiopotassium
The terrestrial origin of 40K (T 1/2 of 1.248 × 109 years; β−, electrons capturing) and 87Rb (T 1/2 of 4.92 × 1010 years; emits β −) is a significant source of radiation to humans while both occur at low concentrations in the rock crust (<1 mBq kg−1) (Skwarzec 2012). Mushrooms are rich in K and Rb (Tables 1 and 12). Typical contents of K and Rb in mushrooms are around 25,000 to 50,000 and ~100 to 300 mg kg−1 dm, respectively (Table 12). And fruit bodies are at least one order of magnitude richer in K and Rb and also in Cs compared to fungal mycelium (Vinichuk et al. 2011). The radionuclides 40K and 87Rb are common constituents of mushrooms (Baeza et al. 2004a, b, 2005; Mietelski et al. 2010; and many others). The contents of 40K in mushrooms and other foods can be assessed from the concentrations of total K (by multiplying with 0.000117). Rubidium in nature consists of two isotopes, a stable 85Rb (72.2 %) and radioactive 87Rb (27.8 %), and no data published are available on 87Rb in mushrooms.
The activities of 137Cs in fruit bodies were often compared with the natural content of 40K. Potassium as an essential nutrient is “bio-adjustable” in that for a given species a certain concentration of K is favorable, and thus, the activity of 40K is relatively constant and this is typical for the given species and site.
Cesium and radiocesium
Radiocesium (137Cs) is the nuclide on which public interest is mainly focused and it is widely studied in wild-grown mushrooms (Kirchner and Daillant 1998; Baeza et al. 2004b, 2005; Mietelski et al. 2002, 2010; Kostiainen 2007; Taira et al. 2011; Castro et al. 2012; and many others). The 137Cs and other nuclides deposited from fallout are further absorbed by fungi from soils (decaying litter and organic and inorganic soil layers—elements diffused into soil solution), and there is no discrimination between decaying and stable isotopes of a particular element undergoing uptake by mycelia. Hence, the efficiency of radionuclides bioaccumulation in mushrooms as a phenomenon does not vary from that of metals at sites polluted due to depositions from smelters: that which is easily accessible is readily accumulated and no extra energy is lost by the organism. A good example to explain this are metals (e.g., Ni and Cd) found at elevated concentrations in mushrooms collected at sites exposed to metal fumes deposited from metal smelters (Barcan et al. 1998; Collin-Hansen et al. 2002). “Efficient” bioaccumulation of 137Cs by fungi is a feature related to mushroom species which depends on the “need” for stable Cs, which is an abundant element in mushrooms (Table 12) and on the efficiency of radionuclide diffusion into soil solution (stable Cs can be supplied from other pools which can be less accessible and to deficiency of 137Cs in solution).
A large-scale remediation of soils polluted with radionuclides and especially with 137Cs is out of real possibilities and polluted sites become abandoned grounds for years. Rosén et al. (2011) suggested that a single (100 kg K/ha) treatment of forest soil with potassium (KCl) fertilizer in 1992 could have a long-term (even 17 years after application) impact on bioaccumulation of 137Cs by Cortinarius semisanguineus, Lactarius rufus, Cortinarius caperatus, and S. variegatus mushrooms—radioactivity is reduced from 21 to 58 %. An attempt to use stable Cs salts to reduce uptake of 137Cs by forest mushrooms and berries has not been reported.
Mushroom contents of stable Cs vary between its morphological parts, and in caps, it is around twice more abundant in Cs than in stipe. High geographical (spatial) variations in the contents of Cs in mushrooms have been noted. For example, the mycorrhizal species such as B. edulis and L. scabrum with 1.6 to 8.7 mg Cs kg−1 dm (median values) in caps are richer in this element compared to mycorrhizals, such as A. muscaria with 0.063 to 0.83 mg kg−1 dm and up to 20 mg kg−1 dm in P. involutus (Falandysz et al. 2007c, d, e, 2008a). The saprophytic M. procera contained stable Cs in caps at 0.015 to 0.043 mg kg−1 dm (median values) (Falandysz et al. 2008b), and this is low compared to mycorrhizal mushrooms mentioned. Hence, there is no doubt that 137Cs can be more efficiently sequestered in flesh by many mycorrhizal mushrooms than saprophytic mushrooms (Rühm et al. 1997).
As mentioned, the largest radioactivity from artificial radionuclides in mushrooms usually comes from 137Cs, but this can differ regionally. In a study in France, the contribution to the gamma-radioactivity from 134Cs, 137Cs, 210Pb, and 226Ra for the majority of mushrooms was highest for 210Pb. Mushrooms there contained 210Pb at <1.76 to 36.5 Bq kg−1 dm and for 226Ra was an order of magnitude less. And in species that are eaten less frequently and at lower rate, the radioactivity from 137Cs was greatest—up to 2,860 Bq kg−1 dm (Kirchner and Daillant 1998).
In studies in Finland, the activity concentrations of 137Cs in 600 samples of mushrooms collected in 2000–2005 were between 10 and 3,000 Bq kg−1 (low in Leccinum spp., Gyromitra spp., and Scutiger ovinus; medium in B. edulis, C. cibarius, and Russula sp.; and high in, e.g., Cantharellus tubaeformis, C. cornucopioides, Lactarius spp., Hydnum spp., S. variegates, and Cortinarius caperatus), and no significant reduction in activity could be noted over that time (Kostiainen 2007). In addition, after comparison of data given for radioactivity in the same species but collected at the same site in 1986–1988, no decrease was found from 1986 to 2005. For B. edulis, whose mycelium lives relatively deeper in soil layer, the radioactivity increased as the post-Chernobyl 137Cs infiltrated deeper into the soil horizon (Kostiainen 2007). Later, a similar result was noted for B. edulis elsewhere (Mietelski et al. 2010).
Compared to 137Cs and 40K, less data are published on other radionuclides in mushrooms both natural and artificial. Other radionuclides studied in mushrooms include 210Po, 234,238U, 228,230,232Th, 90Sr 239+240Pu, 238Pu 241Am, 134Cs, 85Sr, 60Co and 226Ra (Kirchner and Daillant 1998; Mietelski et al. 2002; Skwarzec and Jakusik 2003; Baeza et al. 2004a; Szántó et al. 2007; Vaartamaa et al. 2009). In view of the current knowledge, the amounts of these radionuclides reported for edible wild-grown mushrooms that emerged at areas not close to sites of nuclear tests and accidents, as well as for cultivated species and mushrooms, are below accepted doses for internal exposure.
Technical problems related to trace minerals in mushrooms
The truth is that accurate and precise analytical methods are needed when studying any mineral constituent in any abiotic or biotic matrices. In several articles (old and new) on trace minerals in mushrooms, unreliable data were published on elements (Se, Hg, Fe, Co, Cr, V, Ni, Rb, Ba, Cs, Sr, U, Zr and on the rare earth elements such as Ga, Nb, Ce, Th, Nd, and also Li, Cd, and Pb) sequestered in fruit bodies. Regrettably, many of such “dubious” data were published in journals that specialized in trace element research. A clear documentation of all such cases will need further investigations, and some aspects of such cases are discussed in detail elsewhere (Falandysz and Lipka 2006; Borovička and Řanda 2007; Falandysz 2008, 2012, 2013; Falandysz et al. 2012a, 2013; Borovička et al. 2011; Jarzyńska and Falandysz 2011a, b; Jarzyńska et al. 2012a). The biased analytical data published give a false picture of the composition and nutritional value of mushrooms with respect to minerals. Certainly, if a well-studied species is not classified as a hyperaccumulator of given mineral elements and is not collected from a polluted or geoanomalous site, a high load of element in its fruit body (example is Se, Hg, Fe, Cr, Co, Li, Cd, V, Ni, Ba, Sr, Zr) is not expected. When species of mushroom is without earlier published data on its mineral composition, the proper choice of analytical method and basic rules of chemical analysis must be applied.
A good example of this kind of problems is the case of Se (total Se) in mushrooms. As discussed earlier (see Se section), mushrooms have high variability in their contents of Se. Some mushrooms are specifically rich in this element and a credible range for all species studied until now is from ~0.01 to 370 mg kg−1 dm (some recent and totally biased data showed even around 190 to 420 mg Se kg−1 dm as typical values for certain species) (Falandysz 2013). Selenium for many reasons remains a challenge to analysts, agronomists, nutritionists, physicians, and the public. As mentioned, Se has a high biological potential and its content in foods is usually small, and also small Se doses are required in human nutrition usually between 1 and 3.3 μg kg−1 bm daily.
Several of the sample preparation methods and instrumental measurement techniques have been applied for the examination of Se in mushrooms. These instrumental techniques include UV–VIS spectrophotometry, gas chromatography, flame atomic-absorption spectroscopy (AAS), hydride generation-atomic absorption spectroscopy (HG-AAS), hydride generation graphite furnace-atomic absorption spectroscopy (HG-GF-AAS), inductively coupled plasma atomic emission spectroscopy (ICP-AES), inductively coupled plasma mass spectrometry, fluorimetry (FLU), and neutron activation analysis (INAA) (Falandysz 2013). To determine total Se content of mushroom after wet digestion (with oxidizing acids), the Se contained in analyte needs to be separated (to enhance sensitivity and remove interferences) before aspiration to flame AAS. This is offered by HG-AAS and HG-GF-AAS but not by ordinary F-AAS because it lacks sensitivity for Se (Figs. 2 and 3). Also in the case of ICP-AES, the Se contained in the wet digested mushroom sample has to be separated (as hydride) before aspiration of digest to plasma. Determination of Se by ICP-AES without its pre-separation suffers due to common, nonspectral interferences, because of the formation of carbonyl ions that interfere with Se spectral line at λ 194.163 nm and this is a well-known fact (Machat et al. 2002). In several reports are given data on Se in mushrooms after determination by ICP-AES but without pre-separation of Se before instrumental measurement (Figs. 2 and 3).
Agerer R, Christian J, Mayr C, Hobbie E (2012) Isotopic signatures and trophic status of Ramaria. Mycol Prog 11:47–59
Alonso J, Salgado M, Gariciá M, Melgar M (2000) Accumulation of mercury in edible macrofungi: influence of some factors. Arch Environ Contam Toxicol 38:158–162
Aloupi M, Koutrotsios G, Koulousaris M, Kalogeropoulos N (2011) Trace metal contents in wild edible mushrooms growing on serpentine and volcanic soils on the island of Lesvos, Greece. Ecotoxicol Environ Saf 78:184–194. doi:10.1016/j.ecoenv.2011.11.018
Amundson R, Richter DD, Humphreys GS, Jobbágy EG, Gaillardet J (2007) Coupling between biota and Earth materials in the critical zone. Elements 3:327–332. doi:10.2113/gselements.3.5.327
Andersson HC, Gry J (2004) Phenylhydrazines in the cultivated mushroom (Agaricus bisporus)—occurrence, biological properties, risk assessment and recommendations. Temanord 2004:558
Antibus RK, Bower D, Dighton J (1997) Root surface phosphatase activities and uptake of 32P labelled inositol phosphate in field-collected gray birch and red maple roots. Mycorrhiza 7:39–46
Assunção LS, de Luz JM, de Cássia Soares da Silva, Fontes V, Soares B, Dantas V (2012) Enrichment of mushrooms: an interesting strategy for the acquisition of lithium. Food Chem 134:1123–1127
Baeza A, Guillén J, Mietelski JW (2004a) Uptake of alpha and beta emitters by mushrooms collected and cultured in Spain. J Radioanal Nucl Chem 261:375–380
Baeza A, Hernández S, Guillén J, Moreno G, Manjóon JL, Pascuala R (2004b) Radiocaesium and natural gamma emitters in mushrooms collected in Spain. Sci Total Environ 408:84–91
Baeza A, Guillén J, Bernedo JM (2005) Soil-fungi transfer coefficients: importance of the location of mycelium in soil and of the differential availability of radionuclides in soil fractions. J Environ Radioact 81:89–106
Bakken LR, Olsen RA (1990) Accumulation of radiocaesium in fungi. Can J Microbiol 36:70–710
Baldrian P (2008) Chapter 2: enzymes of saprotrophic basidiomycetes. In: Boddy L, Frankland JC, van West P (eds) Ecology of saprotrophic Basidiomycetes. British Mycological Society Symposia Series, Vol. 28. Elsevier, Amsterdam, pp 19–41
Barcan VS, Kovnatsky EF, Smetannikova MS (1998) Absorption of heavy metals in wild berries and edible mushrooms in an area affected by smelter emissions. Water Air Soil Pollut 103:173–195
Bargagli R, Baldi F (1984) Mercury and methylmercury in higher fungi and their relation with the substrata in a cinnabar mining area. Chemosphere 13:1059–1071
Bhatia P, Prakash R, Cameotra SS, Aureli F, Cubadda F, D’Amato M, Nagaraja TP (2011) Fortification of edible mushrooms with selenium using naturally enriched substrates. 4th International IUPAC Symposium for Trace Elements in Foods (TEF-4). King’s College, Aberdeen, Scotland, 19–22 June 2011. P/19/0040
Blackwell M (2011) The fungi: 1, 2, 3 … 5.1 million species? Am J Bot 98:426–438
Blaudez D, Chalot M (2011) Characterization of the ER-located zinc transporter ZnT1 and identification of a vesicular zinc storage compartment in Hebeloma cylindrosporum. Fungal Genet Biol 48:96–503
Borovička J (2004) A new locality of Sarcosphaera coronaria [In Czech]. Mykol Sborn 81:97–100
Borovička J, Řanda Z (2007) Distribution of iron, cobalt, zinc and selenium in macrofungi. Mycol Prog 6:249–259
Borovička J, Řanda Z, Jelínek E (2005) Gold content of ectomycorrhizal and saprobic macrofungi from non-auriferous and unpolluted areas. Mycol Res 109:951–955
Borovička J, Řanda Z, Jelínek E (2006) Antimony content of macrofungi from clean and polluted areas. Chemosphere 64:1837–1844
Borovička J, Řanda Z, Jelínek E, Kotrba P, Dunn CE (2007) Hyperaccumulation of silver by Amanita strobiliformis and related species of the section Lepidella. Mycol Res 111:1339–1344
Borovička J, Dunn CE, Gryndler M, Mihaljevič M, Jelínek E, Rohovec J, Rohošková M, Řanda Z (2010a) Bioaccumulation of gold in macrofungi and ectomycorrhizae from the vicinity of the Mokrsko gold deposit, Czech Republic. Soil Biol Biochem 42:83–91
Borovička J, Kotrba P, Gryndler M, Mihaljevič M, Řanda Z, Rohovec J, Cajthaml T, Stijve T, Dunn CE (2010b) Bioaccumulation of silver in ectomycorrhizal and saprobic macrofungi from pristine and polluted areas. Sci Total Environ 408:2733–2744
Borovička J, Kubrová J, Rohovec J, Řanda Z, Dunn CE (2011) Uranium, thorium and rare earth elements in macrofungi: what are the genuine concentrations? Biometals 24:837–845
Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176
Brzostowski A, Bielawski L, Orlikowska A, Plichta S, Falandysz J (2009) Instrumental analysis of metals profile in Poison Pax (Paxillus involutus) collected at two sites in Bory Tucholskie. Chem Anal (Warsaw) 54:907–919
Brzostowski A, Falandysz J, Jarzyńska G, Zhang D (2011a) Bioconcentration potential of metallic elements by Poison Pax (Paxillus involutus) mushroom. J Environ Sci Health A 46:378–393
Brzostowski A, Jarzyńska G, Kojta AK, Wydmańska D, Falandysz J (2011b) Variations in metal levels accumulated in Poison Pax (Paxillus involutus) mushroom collected at one site over four years. J Environ Sci Health A 46:581–588
Byrne AR, Ravnik V, Kosta L (1976) Trace element concentrations in higher fungi. Sci Total Environ 6:65–78
Byrne AR, Šlejkovec Z, Stijve T, Fay L, Gössler W, Gailer J, Irgolic KJ (1995) Arsenobetaine and other arsenic species in mushrooms. Appl Organomet Chem 9:305–313
Campos JA, Tejera NA, Sánchéz CJ (2009) Substrate role in the accumulation of heavy metals in sporocarps of wild fungi. Biometals 22:835–841
Castro LP, Maihara VA, Silva PSC, Figueira RCI (2012) Artificial and natural radioactivity in edible mushrooms from Sao Paulo. Brazil J Environ Radioact 113:150–154
Cen F, Chen L, Hu Y, Xu H (2012) Chelator induced bioextraction of heavy metals from artificially contaminated soil by mushroom (Coprinus comatus). Chem Ecol 28:267–280
Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44
Chojnacka A, Jarzyńska G, Drewnowska M, Nnorom IC, Falandysz J (2012) Yellow-cracking Boletes (Xerocomus subtomentosus) mushrooms: content and potential to sequestrate mercury. J Environ Sci Health A 47:2094–2100
Christ S, Wubet T, Theuerl T, Herold N, Buscot F (2011) Fungal communities in bulk soil and stone compartments of different forest and soil types as revealed by a barcoding ITS rDNA and a functional laccase encoding gene marker. Soil Biol Biochem 43:1292–1299
Chudzyński K, Falandysz J (2008) Multivariate analysis of elements content of Larch Bolete (Suillus grevillei) mushroom. Chemosphere 73:1230–1239
Chudzyński K, Bielawski L, Falandysz J (2009) Mercury bio-concentration potential of Larch Bolete, Suillus grevillei, mushroom. Bull Environ Contam Toxicol 83:275–279
Chudzyński K, Jarzyńska G, Stefańska A, Falandysz J (2011) Mercury content and bio-concentration potential of Slippery Jack, Suillus luteus, mushroom. Food Chem 125:986–990
Cocchi L, Vescovi L, Petrini L, Petrini O (2006) Heavy metals in edible mushrooms in Italy. Food Chem 98:277–284
Collin-Hansen C, Yittri KE, Andersen RA, Berthelse BO, Steinnes E (2002) Mushrooms from two metal-contaminated areas in Norway: occurrence of metals and metallothionein-like proteins. Geochem Explor Environ Anal 2:2074–2076
Collin-Hansen C, Pedersen SA, Andersen RA, Steinnes E (2003) First report of phytochelatins in a mushroom: induction of phytochelatins by metal exposure in Boletus edulis. Mycologia 99:161–174
Collin-Hansen C, Andersen RA, Steinnes E (2005) Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycol Res 109:1386–1396
Costa-Silva F, Marques G, Matos CC, Barros AIRNA, Nunes FM (2011) Selenium contents of Portuguese commercial and wild edible mushrooms. Food Chem 126:91–96
Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417
Crane S, Dighton J, Barkay T (2010) Growth responses to and accumulation of mercury by ectomycorrhizal fungi. Fungal Biol 114:873–880
Dahlberg A, Kanikolova I, Johanson K-J (1997) Intraspecific variation in 137Cs activity concentration in sporocarps of Suillus variegatus in seven Swedish populations. Mycol Res 101:545–551
Drbal K, Kalač P, Šeflová A, Šefl J (1975a) Iron and manganese content in some edible macrofungi [In Czech]. Czech Mycol 29:110–114
Drbal K, Kalač P, Šeflová A, Šefl J (1975b) Copper content in some edible macrofungi [In Czech]. Czech Mycol 29:184–186
Drewnowska M, Jarzyńska G, Kojta AK, Falandysz J (2012a) Mercury in European Blusher, Amanita rubescens, mushroom and soil. Bioconcentration potential and intake assessment. J Environ Sci Health B 47:466–474
Drewnowska M, Jarzyńska G, Sąpór A, Nnorom IC, Sajwan KS, Falandysz J (2012b) Mercury in Russula mushrooms: bioconcentration by yellow-ocher Brittle Gills Russula ochroleuca. J Environ Sci Health A 47:1577–1591
Drewnowska M, Lipka K, Jarzyńska G, Danisiweicz-Czupryńska D, Falandysz J (2012c) Investigation on metallic elements of Fly Agaric, Amanita muscaria, fungus and the forest soils from the Mazurian Lakes District of Poland. Fresenius Environ Bull 21. doi:10.3291/F-2012-571pj2013
Estrada AER, Lee H-J, Beelman RB, Jimenez-Gasco M, Royse DJ (2009) Enhancement of the antioxidants ergothineine and selenium in Pleurotus eryngi var. eryngi basidiomata through cultural practice. World J Microbiol Biotechnol 25:1597–1607
Falandysz J (2002) Mercury in mushrooms and soil of the Tarnobrzeska Plain, southeastern Poland. J Environ Sci Health Part A 37:343–352
Falandysz J (2008) Selenium in edible mushrooms. J Environ Sci Health C 26:256–299
Falandysz J (2010) Mercury in certain mushrooms species in Poland. In: Rai M, Kōvics G (eds) Progress in mycology. Scientific, Jodhpur, pp 349–383
Falandysz J (2012) Comments on “Determination of mercury, cadmium, lead, zinc, selenium and iron by ICP-OES in mushroom samples from around thermal power plant in Muğla, Turkey”. doi. 10.1007/s00128-011-0357-1. Bull Environ Contam Toxicol 88:651–653. doi:10.1007/s00128-012-0566-2
Falandysz J (2013) Review: On published data and methods for selenium in mushrooms. Food Chem. doi:10.1016/j.foodchem.2012.10.046
Falandysz J, Bielawski L (2001) Mercury content of wild edible mushrooms collected near the town of Augustów. Pol J Environ Stud 10:67–71
Falandysz J, Bielawski L (2007) Mercury and its bioconcentration factors in Brown Birch Scaber Stalk (Leccinum scabrum) from various sites in Poland. Food Chem 105:635–640
Falandysz J, Brzostowski A (2007) Mercury and its bioconcentration factors in Poison Pax (Paxillus involutus) from various sites in Poland. J Environ Sci Health A 42:1095–1100
Falandysz J, Chwir A (1997) The concentrations and bioconcentration factors of mercury in mushrooms from Mierzeja Wiślana sand-bar, Northern Poland. Sci Total Environ 203:221–228
Falandysz J, Danisiewicz D (1995) Bioconcentration factors (BCF) of silver in wild Agaricus campestris. Bull Environ Contam Toxicol 55:122–129
Falandysz J, Gucia M (2008) Bioconcentration factors of mercury by parasol mushroom (Macrolepiota procera). Environ Geochem Health 30:121–125
Falandysz J, Lipka K (2006) Selen w grzybach [In Polish]. Roczn Państw Zakł Hig 52:217–233
Falandysz J, Bona H, Danisiewicz D (1994a) Silver content of wild-grown mushrooms from northern Poland. Z Lebensm Unters Forsch 199:222–224
Falandysz J, Bona H, Danisiewicz D (1994b) Silver uptake by Agaricus bisporus from an artificially enriched substrate. Z Lebensm Unters Forsch 199:225–228
Falandysz J, Gucia M, Frankowska A, Kawano M, Skwarzec B (2001a) Total mercury in wild mushrooms and underlying soil substrate from the city of Umeå and its surroundings, Sweden. Bull Environ Contam Toxicol 67:767–770
Falandysz J, Szymczyk K, Ichihashi H, Bielawski L, Gucia M, Frankowska A, Yamasaki S (2001) ICP/MS and ICP/AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland. Food Addit Contam 18:503–513
Falandysz J, Bielawski L, Kannan K, Gucia M, Lipka K, Brzostowski A (2002a) Mercury in wild mushrooms and underlying soil substrate from the great lakes land in Poland. J Environ Monit 4:473–476
Falandysz J, Bielawski L, Kawano M, Brzostowski A, Chudzyński K (2002b) Mercury in mushrooms and soil from the Wieluńska Upland in south-central Poland. J Environ Sci Health A 37:1409–1420
Falandysz J, Gucia M, Skwarzec B, Frankowska A, Klawikowska K (2002c) Total mercury in mushrooms and underlying soil from the Borecka Forest, Northeastern Poland. Arch Environ Contam Toxicol 42:145–154
Falandysz J, Lipka K, Gucia M, Kawano M, Strumnik K, Kannan K (2002d) Accumulation factors of mercury in mushrooms from Zaborski Landscape Park, Poland. Environ Int 28:421–427
Falandysz J, Brzostowski A, Kawano M, Kannan K, Puzyn T, Lipka K (2003a) Concentrations of mercury in wild growing higher fungi and underlying substrate near Lake Wdzydze, Poland. Water Air Soil Pollut 148:127–137
Falandysz J, Gucia M, Brzostowski A, Kawano M, Bielawski L, Frankowska A, Wyrzykowska B (2003b) Content and bioconcentration of mercury in mushrooms from northern Poland. Food Addit Contam 20:247–253
Falandysz J, Lipka K, Kawano M, Brzostowski A, Dadej M, Jędrusiak A, Puzyn T (2003c) Mercury content and its bioconcentration factors at Łukta and Morąg, Northeastern Poland. J Agric Food Chem 51:2835–2836
Falandysz J, Kawano M, Świeczkowski A, Brzostowski A, Dadej M (2003d) Total mercury in wild-grown higher mushrooms and underlying soil from Wdzydze Landscape Park, Northern Poland. Food Chem 81:21–26
Falandysz J, Jędrusiak A, Lipka K, Kannan K, Kawano M, Gucia M, Brzostowski A, Dadej M (2004) Mercury in wild mushrooms and underlying soil substrate from Koszalin, North-central Poland. Chemosphere 54:461–466
Falandysz J, Frankowska A, Mazur A (2007a) Mercury and its bioconcentration factors in King Bolete (Boletus edulis) Bull. Fr. J Environ Sci Health A 42:2089–2095
Falandysz J, Gucia M, Mazur A (2007b) Content and bioconcentration factors of mercury by Parasol Mushroom Macrolepiota procera. J Environ Sci Health A 42:735–740
Falandysz J, Kunito T, Kubota R, Brzostowski A, Mazur A, Falandysz JJ, Tanabe S (2007c) Selected elements of Poison Pax Paxillus involutus. J Environ Sci Health A 42:1161–1168
Falandysz J, Kunito T, Kubota R, Lipka K, Mazur A, Falandysz JJ, Tanabe S (2007d) Selected elements in Fly Agaric Amanita muscaria. J Environ Sci Health A 42:1615–1623
Falandysz J, Kunito T, Kubota R, Bielawski MA, Falandysz JJ, Tanabe S (2007e) Selected elements in Brown Birch Scaber Stalk Leccinum scabrum. J Environ Sci Health A 42:2081–2088
Falandysz J, Lipka K, Mazur A (2007f) Mercury and its bioconcentration factors in Fly Agaric (Amanita muscaria) from spatially distant sites in Poland. J Environ Sci Health A 42:1625–1630
Falandysz J, Kunito T, Kubota R, Bielawski L, Frankowska A, Falandysz JJ, Tanabe S (2008a) Multivariate characterization of elements accumulated in King Bolete Boletus edulis mushroom at lowland and high mountain regions. J Environ Sci Health A 43:1692–1699
Falandysz J, KunitoT KR, Gucia M, Mazur A, Falandysz JJ, Tanabe S (2008b) Some mineral constituents of Parasol Mushroom Macrolepiota procera. J Environ Sci Health B 43:187–192
Falandysz J, Frankowska A, Jarzyńska G, Dryżałowska A, Kojta AK, Zhang D (2011) Survey on composition and bioconcentration potential of 12 metallic elements in King Bolete (Boletus edulis) mushroom that emerged at 11 spatially distant sites. J Environ Sci Health B 46:231–246
Falandysz J, Chudzyński K, Kojta AK, Jarzyńska G, Drewnowska M (2012a) Comparison of two acid extraction methods for determination of minerals in soils beneath to Larch Bolete (Suillus grevillei) and aimed to estimate minerals sequestration potential in fruiting bodies. J Environ Sci Health A 47:1607–1613
Falandysz J, Drewnowska M, Jarzyńska G, Zhang D, Zhang Y, Wang J (2012b) Mineral constituents in Common Chanterelles and soils collected from a high mountain and lowland sites in Poland. J Mt Sci 9:697–705
Falandysz J, Kojta AK, Jarzyńska G, Drewnowska A, Dryżałowska A, Wydmańska D, Kowalewska I, Wacko A, Szlosowska M, Kannan K, Szefer P (2012c) Mercury in Bay Bolete Xerocomus badius: bioconcentration by fungus and assessment of element intake by humans eating fruiting bodies. Food Addit Contam A 29:951–961
Falandysz J, Kowalewska I, Nnorom IC, Drewnowska M, Jarzyńska G (2012d) Mercury in Red Aspen Boletes (Leccinum aurantiacum) mushrooms and the soils. J Environ Sci Health A 47:1695–1700
Falandysz J, Nnorom IC, Jarzyńska G, Romińska D, Damps K (2012e) A study of mercury bio-concentration by Puffballs (Lycoperdon perlatum) and evaluation of dietary intake risks. Bull Environ Contam Toxicol 89:759–763
Falandysz J, Widzicka E, Kojta AK, Jarzyńska G, Drewnowska M, Danisiewicz-Czupryńska D, Dryżałowska A, Lenz E, Nnorom IC (2012f) Mercury in Common Chanterelles mushrooms: Cantharellus spp. update. Food Chem 133:842–850
Falandysz J, Mazur A, Drewnowska M, Kojta AK, Jarzyńska G, Dryżałowska A, Nnorom IC (2013) Mercury in fruiting bodies of dark honey fungus (Armillaria solidipes) and beneath substratum soils collected from spatially distant areas. J Sci Food Agric 92. doi:10.1002/jsfa.5807
Fischer RG, Rapsomanikis S, Andreae MO, Baldini F (1995) Bioaccumulation of methylmercury and transformation of inorganic mercury by macrofungi. Environ Sci Technol 29:993–999
Fomina M, Alexander IJ, Colpaert JV, Gadd GM (2006) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866
Fomina M, Charnock JM, Hillier S, Alvarez R, Gadd GM (2007) Fungal transformations of uranium oxides. Environ Microbiol 9:1696–1710
Frankowska A, Ziółkowska J, Bielawski L, Falandysz J (2010) Profile and bioconcentration of minerals by King Bolete (Boletes edulis) from the Płocka Dale in Poland. Food Addit Contam B 3:1–6
Friese W (1929) Mineral composition of macrofungi. Z Unters Lebensm 57:604–613
Gadd GM (2004) Mycotransformation of organic and inorganic substrates. Mycologist 18:60–70
Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49
Gadd GM (2008) Fungi and their role in the biosphere. In: Jorgensen SE, Fath B (eds) Encyclopedia of ecology. Elsevier, Amsterdam, pp 1709–1717
Gadd GM, Fomina M (2011) Uranium and fungi. Geomicrobiol J 28:471–482
Gadd GM, Rhee YJ, Stephenson K, Wei Z (2012) Geomycology: metals, actinides and biominerals. Environ Microbiol Rep 4:270–296
García MÁ, Alonso J, Melgar MJ (2009) Lead in edible mushrooms. Levels and bioconcentration factors. J Hazard Mater 167:777–783
Garner CD, Armstrong EM, Berry RE, Beddoes RL, Collison D, Cooney JA, Nigar Ertok G, Helliwell M (2000) Investigations of Amavadin. J Inorg Biochem 80:17–20
Gast CH, Jansen E, Bierling J, Haanstra L (1988) Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 17:789–799
Gentili A, Gremigni G, Sabbatini V (1991) 110mAg in fungi in central Italy after the Chernobyl accident. J Environ Radioact 13:75–78
Giannaccini G, Betti L, Palego L, Mascia G, Schmid L, Lanza M, Mela A, Fabbrini L, Biondi L, Lucacchini A (2012) The trace element content of top-soil and wild edible mushroom samples collected in Tuscany, Italy. Environ Monit Assess 184:7679–7585
Gryndler M, Hršelová H, Soukupová L, Borovička J (2012) Silver release from decomposed hyperaccumulating Amanita solitaria fruit-body biomass strongly affects soil microbial community. Biometals 25:987–993
Gucia M, Jarzyńska G, Kojta AK, Falandysz J (2012a) Temporal variability in twenty chemical elements content of Parasol Mushroom (Macrolepiota procera) collected from two sites over a few years. J Environ Sci Health B 47:81–88
Gucia M, Kojta AK, Jarzyńska G, Rafał E, Roszak M, Osiej I, Falandysz J (2012b) Multivariate analysis of mineral constituents of edible Parasol Mushroom (Macrolepiota procera) and soils beneath fruiting bodies collected from Northern Poland. Environ Sci Pollut Res 19:416–431
Guillén JF, Baeza A, Ontalba MA, Míguez MP (2009) 210Pb and stable lead content in fungi: its transfer from soil. Sci Total Environ 407:4320–4326
Györfi J, Geösel A, Vetter J (2010) Mineral composition of different strains of edible medicinal mushroom Agaricus subrufescens Peck. J Med Food 13:1510–1514
Hawksworth DL (2009) Mycology: a neglected megascience. In: Rai M, Bridge PD (eds) Applied mycology. CABI, Wallingford, pp 1–16
Hobbie EA, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83
Hong J, Bañuelos GS, Fowler T, Lin Z-Q (2011) Use of selenium-laden plant materials from phytoremediation to produce selenium-biofortified edible mushrooms. ICOBTE 2011, 11th International Conference on the Biogeochemistry of Trace Elements. Conference Proceedings Parte I, Congress Center, Florence, Italy, July 3–7, pp. 349–350
Horyna J, Řanda Z (1988) Uptake of radiocesium and alkali metals by mushrooms. J Radioanal Nucl Chem 172:107120. doi:10.1007/BF02164600
Jarzyńska G, Falandysz J (2011a) Selenium and 17 other largely essential and toxic metals in muscle and organ meats of Red Deer (Cervus elaphus)—consequences to human health. Environ Int 37:882–888
Jarzyńska G, Falandysz J (2011b) The determination of mercury in mushrooms by CV-AAS and ICP-AES techniques. J Environ Sci Health A 46:569–573
Jarzyńska G, Falandysz J (2012a) Metallic elements profile of Hazel (Hard) Bolete (Leccinum griseum) mushroom and associated upper soil horizon. African J Biotechnol 11:4588–4594
Jarzyńska G, Falandysz J (2012b) Metallic elements profile of Slate Bolete (Leccinum duriusculum) mushroom and associated soil horizon. J Geochem Explor 121:69–75
Jarzyńska G, Gucia M, Kojta AK, Rezulak K, Falandysz J (2011) Profile of trace elements in Parasol Mushroom (Macrolepiota procera) from Tucholskie Forests. J Environ Sci Health B 46:741–751
Jarzyńska G, Kojta AK, Drewnowska M, Falandysz J (2012a) Notes on selenium in mushrooms data determined by inductively coupled plasma atomic emission spectroscopy (ICP–AES) and hydride generation atomic absorption spectroscopy (HG–AAS) techniques. Afr J Agric Res 7:5233–5237
Jarzyńska G, Chojnacka A, Dryżałowska A, Nnorom IC, Falandysz J (2012b) Concentrations and bioconcentration factors of minerals by Yellow-cracking Bolete (Xerocomus subtomentosus) mushroom collected in Noteć Forest, Poland. J Food Sci 77:H202–H206
Jentschke G, Brandes B, Kuhn AJ, Schröder WH, Becker JS, Godbold DL (2000) The mycorrhizal fungus Paxillus involutus transports magnesium to Norway spruce seedlings. Evidence from stable isotope labeling. Plant Soil 220:243–246
Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC, Boca Raton
Kalač P, Burda J, Stašková I (1991) Concentration of lead, cadmium, mercury and copper in mushrooms in the vicinity of a lead smelter. Sci Total Environ 105:109–119
Kirchner G, Daillant O (1998) Accumulation of 210Pb, 226Ra and radioactive cesium by fungi. Sci Total Environ 222: 63–70
Klán J, Řanda Z, Benada J, Horyna J (1988) Investigation of non-radioactive Rb, Cs, and radiocaesium in higher fungi. Czech Mycol 42:158–169
Koch I, Wang L, Reimer KJ, Cullen WR (2000) Arsenic species in terrestrial fungi and lichens from Yellowknife, NWT, Canada. Appl Organomet Chem 14:245–252
Kojta AK, Gucia M, Jarzyńska G, Lewandowska M, Zakrzewska A, Falandysz J, Zhang D (2011) Phosphorous and metallic elements in Parasol Mushroom (Macrolepiota procera) and soil from the Augustowska Forest and Ełk regions in north-eastern Poland. Fresenius Environ Bull 20:3044–3052
Kojta AK, Jarzyńska G, Falandysz J (2012) Mineral composition and heavy metals accumulation capacity of Bay Bolete’s (Xerocomus badius) fruiting bodies collected near a former gold and copper mining area. J Geochem Explor 121:76–82
Komárek M, Chrastný V, Štíchová J (2007) Metal/metalloid contamination and isotopic composition of lead in edible mushrooms and forest soils originating from a smelting area. Environ Int 33:677–684
Kostiainen E (2007) 137Cs in Finnish wild berries, mushrooms and game meat in 2000–2005. Boreal Environ Res 12:23–28
Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254
Larsen EH, Hansen M, Gössler W (1998) Speciation and health risk considerations of arsenic in the edible mushroom Laccaria amethystina collected from contaminated and uncontaminated locations. Appl Organomet Chem 12:285–291
Lavola A, Aphalo PJ, Lehto T (2011) Boron and other elements in sporophores of ectomycorrhizal and saprotrophic fungi. Mycorrhiza 21:155–165
Lepp NW, Harrison SCS, Morrell BG (1987) A role for Amanita muscaria L. in the circulation of cadmium and vanadium in non-polluted woodland. Environ Geochem Health 9:61–64
Li T, Wang YZ, Zhang J, Zhao YL, Liu H (2011) Trace element content of Boletus tomentipes mushroom collected from Yunnan, China. Food Chem 127:1828–1830
Liu H, Zhang J, Li T, Shi Y, Wang Y (2012) Mineral element levels in wild edible mushrooms from Yunnan, China. Biol Trace Elem Res 147:341–345
Luis P, Kellner H, Zimdars B, Langer U, Martin F, Buscot F (2005) Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microb Ecol 50:570–579
Machat J, Otruba V, Kanicky V (2002) Spectral and non-spectral interferences in the determination of selenium by inductively coupled plasma atomic emission spectrometry. J Anal At Spectrom 17:1096–1102
Maćkiewicz D, Falandysz J (2012) Total mercury in Yellow Kinights (Tricholoma equestre) mushrooms and beneath soils. Bull Environ Contam Toxicol 89:755–758
Maihara VA, Moura PL, Catharino MG, Castro LP, Figueira RCL (2008) Arsenic and cadmium content in edible mushrooms from São Paulo, Brazil determined by INAA and GF AAS. J Radioanal Nucl Chem 278:395–397
Malinowska E, Szefer P, Falandysz J (2004) Metals bioaccumulation by bay bolete Xerocomus badius from selected sites in Poland. Food Chem 84:405–416
Manzi P, Gambelli L, Marconi S, Vivanti V, Pizzoferrato L (1999) Nutrients in edible mushrooms: an inter-species comparative study. Food Chem 65:477–482
Melgar MJ, Alonso J, Garcia MÁ (2009) Mercury in edible mushrooms and soil. Bioconcentration factors and toxicological risk. Sci Total Environ 407:5328–5334
Mietelski JW, Baeza AS, Guillen J, Buzinny M, Tsigankov N, Gaca P, Jasińska M, Tomankiewicz E (2002) Plutonium and other alpha emitters in fruitbodies from Poland, Spain and Ukraine. Appl Radiat Isot 56:717–729
Mietelski JW, Dubchak S, Błażej S, Anielska T, Turnau K (2010) 137Cs and 40K in fruiting bodies of different fungal species collected in a single forest in southern Poland. J Environ Radioact 101:706–711
Muñoz AHS, Corona FG, Wrobel K, Soto GM, Wrobel K (2005) Subcellular distribution of aluminum, bismuth, cadmium, chromium, copper, iron, manganese, nickel, and lead in cultivated mushrooms (Agaricus bisporus and Pleurotus ostreatus). Biol Trace Elem Res 106:265–277
Nasr M, Arp PA (2011) Hg concentrations and accumulations in fungal fruiting bodies, as influenced by forest soil substrates and moss carpets. Applied Geochemistry 26:1905–1917
Nnorom IC, Jarzyńska G, Falandysz J, Drewnowska M, Okoye I, Oji-Nnorom Ch G (2012a) Occurrence and accumulation of mercury in two species of wild grown Pleurotus mushrooms from Southeastern Nigeria. Ecotoxicol Environ Saf 84:78–83
Nnorom IC, Jarzyńska G, Falandysz J, Drewnowska M, Pankavec S, Kojta AK (2012b) Analysis of twenty major and trace elements in sclerotium of Pleurotus tuber-regium (Ósū) mushroom from Southeastern Nigeria. J Food Compos Anal. doi:10.1016/j.jfca.2012.10.00.1
Osobová M, Urban V, Jedelský PL, Borovička J, Gryndler M, Ruml T, Kotrba P (2011) Three metallothionein isoforms and sequestration of intracellular silver in the hyperaccumulator Amanita strobiliformis. New Phytol 90:916–926
Petrini O, Cocchi L, Vescovi L, Petrini L (2009) Chemical elements in mushrooms: their potential taxonomic significance. Mycol Prog 8:171–180
Pilz C, Santos CMM, Nunes NAC, Müller EI, Flores ÉMM, Dressler VL (2011) Speciation of Hg in edible mushroom. International Symposium Trace Elements in Food (TEF-4) King’s College, Aberdeen, Scotland, 19–22 June 2011. P/65/0107
Plassard C, Louche J, Ali MA, Duchemin M, Legname E, Cloutier-Hurteau B (2011) Diversity in phosphorus mobilisation and uptake in ectomycorrhizal fungi. Ann For Sci 68:33–43
Quiquampoix H, Burns RG (2008) Interactions between proteins and soil mineral surfaces: environmental and health consequences. Elements 3:369–440
Ramesh G, Podila GK, Gay G, Marmeisse R, Reddy MS (2009) Different patterns of regulation for copper and cadmium metallothioneins of the ectomycorrhizal fungus Hebeloma cylindrosporum. Appl Environ Microbiol 75:2266–2274
Řanda Z, Kučera J (2004) Trace elements in higher fungi (mushrooms) determined by activation analysis. J Radioanal Nucl Chem 259:99–107
Rayman MP (2008) Food-chain selenium and human health: emphasis on intake. Br J Nutr 100:254–268
Reider SR, Brunner I, Horvat M, Jacobs A, Frey B (2011) Accumulation of mercury and methylmercury by mushrooms and earthworms from forest soils. Environ Pollut 159:2861–2869
Reisinger A (1994) Radiocaesium in macrofungi [In German]. Bibl Mycol 155:1–174
Rhee YJ, Hillier S, Gadd GM (2012) Lead transformation to pyromorphite by fungi. Curr Biol 22:237–241
Rosén K, Vinichuk M, Nikolova I, Johanson K (2011) Long-term effects of single potassium fertilization on 137Cs levels in plants and fungi in a boreal forest ecosystem. J Environ Radioact 102:178–184
Rudawska M, Leski T (2005a) Macro- and microelement contents in fruiting bodies of wild mushrooms from the Notecka forest in west-central Poland. Food Chem 92:499–506
Rudawska M, Leski T (2005b) Trace elements in fruiting bodies of ectomycorrhizal fungi growing in Scots pine (Pinus sylvestris L.) stands in Poland. Sci Total Environ 339:103–115
Rühm W, Kammerer L, Hiersche L, Wirth E (1997) The 137Cs/134Cs ratio in fungi as indicator of the major mycelium location in forest soil. J Environ Radioact 35:129–148
Senn-Irlet B, Heilmann-Clausen J, Genney D, Dahlberg A (2007) Gudiance for conservation of macrofungi in Europe. Document prepared for the European Council for Conservation of Fungi (ECCF) within the European Mycological Association (EMA) and the Directorate of Culture and Cultural and Natural Heritage, Council of Europe, Strasbourg
Silva MCS, Naozuka J, Oliveira PV, Vanetti MCD, Bazzolli DMS, Costa NMB, Kasuya MCM (2010) In vivo bioavailability of selenium in enriched Pleurotus ostreatus mushrooms. Metallomics 2:162–166
Skwarzec B (2012) Radioactivity. In: Jorgensen SE (ed) Encyclopedia of environmental management. Taylor & Francis, New York. doi:10.1081/E-EEM-120046097
Skwarzec B, Jakusik A (2003) 210Po bioaccumulation by mushrooms from Poland. J Environ Monit 5:791–794
Šlejkovec Z, Byrne AR, Stijve T, Goessler W, Irgolic KJ (1997) Arsenic compounds in higher fungi. Appl Organomet Chem 11:673–682
Šlejkovec Z, Elteren JT, Woroniecka UD, Kroon KJ, Falnoga I, Byrne AR (2000) Preliminary study on the determination of selenium compounds in some selenium-accumulating mushrooms. Biol Trace Elem Res 75:139–155
Smith ML, Bruhn JN, Anderson JB (1992) The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–431
Smits MM, Hoffland E (2009) Possible role of ectomycorrhizal fungi in cycling of aluminium in podzols. Soil Biol Biochem 41:491–497
Soeroes Cs, Kienzl N, Ipolyi I, Dernovics M, Fodor P, Kuehnelt D (2005) Arsenic uptake and arsenic compounds in cultivated Agaricus bisporus. Food Control 16:459–464
Stijve T, Besson R (1976) Mercury, cadmium, lead, and selenium content of mushroom species belonging to the genus Agaricus. Chemosphere 5:151–158
Stijve T, de Meijer AAR (1999) Hydrocyanic acid in mushrooms, with special reference to wild-growing and cultivated edible species. Dtsch Lebensm Rundsch 95:366–373
Stijve T, Vellinga EC, Herrmann A (1990) Arsenic accumulation in some higher fungi. Persoonia 14:161–166
Stijve T, Noorloos T, Byrne AR, Šlejkovec Z, Goessler W (1998) High selenium levels in edible Albatrellus mushroom. Dtsch Lebensm Rundsch 94:275–279
Stijve T, Andrey D, Goessler W, Guinberteau J, Dupuy G (2001) Comparative study of heavy metals and other trace elements in Gyrophragmium dunalii and in yellowish Agaricus of the subsection Arvenses [In French]. Bull Trimest Soc Mycol Fr 117:133–144
Strandberg M (2004) Long-term trends in the uptake of radiocesium in Rozites caperatus. Sci Total Environ 327:315–321
Sun L, Liu G, Yang M, Zhuang Y (2012) Bioaccessibility of cadmium in fresh and cooked Agaricus blazei Murill assessed by in vitro biomimetic digestion system. Food Chem Toxicol 50:1729–1733
Svoboda L, Zimmermannová K, Kalač 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 246:61–67
Svoboda L, Kalač P, Špička J, Janoušková D (2002) Leaching of cadmium, lead and mercury from fresh and differently preserved edible mushrooms, Xerocomus badius, during soaking and boiling. Food Chem 79:41–45
Szántó Z, Hult M, Wätjen U, Altzitzoglou T (2007) Current radioactivity content of wild edible mushrooms: a candidate for an environmental reference material. J Radioanal Nucl Chem 273:167–170
Szubstarska J, Jarzyńska G, Falandysz J (2012) Trace elements of Variegated Boletes (Suillus variegatus) mushrooms. Chem Pap 66:1026–1032
Taira Y, Hayashidai N, Brahmanandhan GM, Nagayama Y, Yamashita S, Takahashi J, Gutenitc A, Kazlovsky A, Urazalin M, Takamura N (2011) Current concentration of artificial radionuclides and estimated radiation doses from 137Cs around the Chernobyl nuclear power plant, the Semipalatinsk nuclear testing site, and in Nagasaki. J Radiat Res 52:88–95
Tsvetnova OB, Shcheglov AI (1994) 137Cs content in the mushrooms of radioactive contaminated zones of the European part of the CIS. Sci Total Environ155:25–29
Turło J, Gutkowska B, Herold F, Dawidowski M, Słowiński T, Zobel A (2010) Relationship between selenium accumulation and mycelial cell composition in Lentinula edodes (Berk.) cultures. J Toxicol Environ Health A 73:1211-1219
Tüzen M, Soylak M (2005) Mercury contamination in mushroom samples from Tokat, Turkey. Bull Environ Contam Toxicol 74:968–972
Tüzen M, Sesli E, Soylak M (2007) Trace element levels of mushroom species from East Black Sea region of Turkey. Food Control 18:806–810
Urban A (2011) Chapter 11. Metal elements and the diversity and function of ectomycorrhizal communities. In: Rai M, Varma A (eds) Diversity and biotechnology of ectomycorrhizae. Soil Biology, vol 25. Springer, Berlin, pp 231–254
Vaartamaa K, Solatie D, Aro L (2009) Distribution of 210Pb and boreal forest ecosystems 210Po concentrations in wild berries and mushrooms. Sci Total Environ 408:84–91
van Schöll L, Hoffland E, van Breemen N (2006a) Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol 170:153–163
van Schöll L, Smits MM, Hoffland E (2006b) Ectomycorrhizal weathering of the soil minerals muscovite and hornblende. New Phytol 171:805–814
Vetter J (2003) Chemical composition of fresh and conserved Agaricus bisporus mushroom. Eur Food Res Technol 217:10–12
Vetter J (2005) Lithium content of some common edible wild-growing mushrooms. Food Chem 90:31–37
Vetter J, Hajdú J, Györfi J, Maszlavér P (2005) Mineral composition of the cultivated mushrooms Agaricus bisporus, Pleurotus ostreatus and Lentinula eodes. Acta Alim 34:441–451
Vinichuk M, Rosén K, Johanson KJ, Dahlberg A (2011) Cesium (137Cs and 133Cs), potassium and rubidium in macromycete fungi and sphagnum plants. In: Singh N (ed) Radioisotopes—applications in physical sciences. InTech, Rijeka. doi:10.5772/22263, 496 pages. ISBN 978-953-307-510-5
Wallander H (2000a) Uptake of P from apatite by Pinus sylvestris seedlings colonized by different ectomycorrhizal fungi. Plant Soil 218:249–256
Wallander H (2000b) Use of strontium isotopes and foliar K content to estimate weathering of biotite induced by pine seedlings colonised by ectomycorrhizal fungi from two different soils. Plant Soil 222:215–229
Wallander H, Wickman T (1999) Biotite and microcline as potassium sources in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Mycorrhiza 9:25–32
Wondratschek I, Röder U (1993) Monitoring of heavy metals in soils by higher fungi. In: Markert B (ed) Plants as biomonitors, indicators for heavy metals in the terrestrial environment. VCH, Weinheim, pp 345–363
Yin L-L, Shi G-Q, Tian Q, Shen T, Ji Y-Q, Zeng G (2012) Determination of the metals by ICP-MS in wild mushrooms from Yunnan, China. J Food Sci 77:151–155
Zellner J (1907) Chemistry of macrofungi [In German]. Verlag von Wilhelm Engelmann, Leipzig
Zhang D, Frankowska A, Jarzyńska G, Kojta AK, Drewnowska M, Wydmańska D, Bielawski L, Wang J, Falandysz J (2010) Metals of King Bolete (Boletus edulis) collected at the same site over two years. Afr J Agric Res 5:3050–3055
Zhang D, Bielawski L, Jarzyńska G, Morawska E, Drewnowska G, Falandysz J (2013) Trace elements in Leccinum scabrum mushrooms and soils from Kłodzka Dale in Sudety Mountains, Poland. J Mt Sci 10 (accepted)
Zhao L, Zhao G, Zhao Z, Chen P, Tong J, Hu X (2004) Selenium distribution in a Se-enriched mushroom species of the genus Ganoderma. J Agric Food Chem 52:3954–3959
A generous support from Dr. Chidi I. Nnorom is acknowledged. The work on this paper was supported in part by grant no DS 530-8131-0197-13 from Poland and to Jan Borovička by the project 504/11/0484 (Czech Science Foundation); institutional support was provided by Long-term Development Projects RVO61389005 and RVO67985831.
This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
Electronic supplementary material
Below is the link to the electronic supplementary material.
(DOC 23676 kb)
About this article
Cite this article
Falandysz, J., Borovička, J. Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97, 477–501 (2013). https://doi.org/10.1007/s00253-012-4552-8
- Organic food
- Se bioenrichment
- Wild food