Assessment of Factors Influencing Trace Element Content of the Basidiomycetes in the European Part of Russia ()
1. Introduction
Fungi are a large group of eukaryotic heterotrophic organisms classified as a separate kingdom (Mycota or Fungi). They keep an intermediate position between the animal and the vegetable kingdoms. On the one hand, fungi lack chlorophyll and therefore need preformed organic compounds for their nutrition. The result of their metabolism is urea. Their cell walls contain chitin, and the storage compound is the glycogen instead of the starch, which is closer to the animals. On the other hand, their way of nutrition (by absorbing the solutions of the organic substances) and their unlimited growth are closer to the plants. The metabolism of the mushrooms leads to the transformation of the complex organic substances into less complex compounds and into the mineral ones at the end. Simple compounds are transferred directly through the cell membranes; the more complex substances are decomposed to monomers by extracellular enzymes. There are data about the Zn-fixation by the organic substances in the metabolism of fungi, the inclusion of Co into the B12-molecule in the synthesis of this vitamin, and the selective accumulation of toxic elements (such as selenium, lead, cadmium, mercury) by some types of fungi [1-3]. In consideration of the numerous literature data, the high concentrations of various trace elements in fungi are not in question [4-7]. For this reason, mushrooms are considered to be the accumulators, and the selective ones, of the trace elements and, in particular, of heavy and toxic metals. However, the combination of the selective accumulation of any trace elements with the osmotrophic (diffuse) way of nutrition of the mushrooms is doubtful. Is the accumulation process actually internal or can the high concentration of the minerals be explained by external reasons? The purpose of this work is to assess the features of the trace element accumulation by basidiomycetes.
2. The Methodology of Sampling and Analysis
Since we were interested only in edible mushrooms we analyzed the trace element composition of the basidiomycetes (Basidiomycota). This group includes the vast majority of fungi used as food, as well as many parasites of cultivated and wild plants. The group of basidiomycetes numbers more than 30,000 species. According to the way of nutrition of the higher fungi they can be saprotrophic, parasitic and symbiotic organisms.
The saprotrophic fungi include most of the pileate and mold fungi, as well as the yeast. Typical representatives of the saprotrophic fungi are russule, woolly milk capsaffron milk cap and champignon.
Higher plants are most often hosts of the parasitic fungi (hemibiotrophs). During their growth fungi secrete enzymes that destroy the middle laminae between plant cells of the host plant, resulting in softening of the tissues. Some parasites gradually suck substances from the host, but do not lead to its death, while other secrete enzymes that decompose the cellulose of the cell walls, resulting in death of the host cell, following which the parasite feeds on the organic remains of the host. Typical representatives of the parasitic fungi are agaric honey, oyster mushrooms and bracket fungi.
Mycorrhiza forming fungi (symbiotrophs) enter into a mutually beneficial relationship with the plants in the form of mycorrhiza. Mycorrhiza is a mutually beneficial co-existence of the fungus and the roots of higher plants. Typical representatives of mycorrhizal fungi are basidiomycetes of the family Boletaceae: brown cap boletuses, aspen mushroom and cepes.
Sampling of mycothalluses was held in Moscow, Moscow Oblast, Kaluga Oblast, Tver Oblast, Nizhny Novgorod Oblast, Tula Oblast and Voronezh Oblast, the Kandalaksha Nature State Reserve and the Kostomuksha Nature Reserve. Samples of Boletus edulis, Leccinum scabrum, Leccinum aurantiacum, Suillus luteus, Russula vesca, Lactarius torminosus, Paxillus involutus, Cantharellus cibarius, Armillariella mellea, Agaricus campestris and Pleurotus ostreatus were selected. Also, the mycothalluses of cepes were sampled in the coastal areas of Iceland. Mushrooms grown in vitro like champignons (Agaricus bisporus) and oyster mushrooms (Pleurotus ostreatus) were selected as well. Mycothallus samples were collected in plastic Ziplock bags, cleared of external contamination, washed twice with distilled water, dried at the temperature t < 60˚C and ground to a size of <1 mm. In the Tver Oblast the soil samples up to the depth of 50 cm were taken simultaneously. The soils were collected in plastic Ziplock bags as well, dried to air-dry state, sifted through a sieve with a hole diameter of 1 mm and reduced to powder.
The trace element analysis of the collected samples was carried out in the laboratory of the Geological Institute of the Russian Academy of Sciences (Moscow) using the instrumental neutron activation (INAA) [6-8] and atomic absorption (AA) methods. The INAA detected concentrations of Na, Mg, Cl, K, Ca, Sc, Cr, Co, As, Se, Br, Rb, Mo, Ag, Sb, I, Cs, La, W, Au, Hg, Th and the AA detected concentrations of Mn, Fe, Ni, Cu, Zn, Cd, Pb.
The quality and reliability control of the results was performed through the analysis of encrypted standard samples of IAEA-SOIL-7, IAEA-336 (Lichen), SRM 1572 (Citrus Leaves) and SRM 1575 (Pine Needles). The quality and reliability of analytical work were systematically confirmed during analytical tests within the framework of international cooperation programs [9,10].
3. Results and Discussion
Table 1 shows the average concentrations of trace elements in the mycothalluses of the symbiotrophs. It is important to stress that the only official criterion for normalizing the concentration of any element in mushrooms is the maximum permissible concentration (MPC) for foodstuff. It is determined by the sanitary inspection of the Russian Federation and is given relative to the “live” weight. Therefore, we can only compare the weight and concentrations with humidity. Moreover, men eat a natural product and not a sublimated one, so the element concentrations should be given relative to the humidity.
The data presented in the Table 1 show that the average concentrations of toxic elements Se, Cd and Hg in the mushrooms Boletus edulis, of Cd and Hg in Leccinum scabrum and of Cd in Leccinum aurantiacum and Suillus luteus exceed the (MPC) [11] for the foodstuff. This refers to the arithmetical mean concentration. The maximal concentration of these toxic elements is almost 100% higher, according to the standard deviation. The concentration of Cr, As and Pb does not exceed the established limits. Variability in concentrations of Na, Mg, Cl, K and Ca is relatively small: 20% - 50%. Variability in concentrations of the other trace elements in mushrooms Boletus edulis, Leccinum scabrum and Leccinum aurantiacum is 50% - 100%, which means a significant irregularity of the trace element accumulation by these fungi.
Table 2 presents data on the concentration of trace elements in mycothalluses of saprotrophic fungi. The data presented in this table show that the average concentrations of Se, Cd and Hg in Agaricus campestris exceed limit values (by 60 times for Cd and 12 times for Hg). The high concentration of precious metals Ag and Au is noteworthy. The variation limits of the standard deviation are much wider than for symbiotrophs.