Evaluation of the radioactive contamination in fungi genus Boletus in the region of Europe and Yunnan Province in China

Applied Microbiology and Biotechnology, Jun 2015

Numerous species of wild-grown mushrooms are among the most vulnerable organisms for contamination with radiocesium released from a radioactive fallout. A comparison was made on radiocesium as well as the natural gamma ray-emitting radionuclide (40K) activity concentrations in the fruiting bodies of several valued edible Boletus mushrooms collected from the region of Europe and Yunnan Province in China. Data available for the first time for Boletus edulis collected in Yunnan, China, showed a very weak contamination with 137Cs. Radiocesium concentration activity of B. edulis samples that were collected between 2011 and 2014 in Yunnan ranged from 5.2 ± 1.7 to 10 ± 1 Bq kg−1 dry matter for caps and from 4.7 ± 1.3 to 5.5 ± 1.0 Bq kg−1 dry matter for stipes. The mushrooms Boletus badius, B. edulis, Boletus impolitus, Boletus luridus, Boletus pinophilus, and Boletus reticulatus collected from the European locations between 1995 and 2010 showed two to four orders of magnitude greater radioactivity from 137Cs compared to B. edulis from Yunnan. The nuclide 40K in B. badius was equally distributed between the caps and stipes, while for B. edulis, B. impolitus, B. luridus, B. pinophilus, and B. reticulatus, the caps were richer, and for each mushroom, activity concentration seemed to be more or less species-specific.

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Evaluation of the radioactive contamination in fungi genus Boletus in the region of Europe and Yunnan Province in China

Evaluation of the radioactive contamination in fungi genus Boletus in the region of Europe and Yunnan Province in China Jerzy Falandysz 2 Tamara Zalewska 1 2 Grażyna Krasińska 2 Anna Apanel 1 2 Yuanzhong Wang 0 2 Sviatlana Pankavec 2 0 Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences , 2238 Beijing Road, Panlong District, Kunming 650200 , China 1 Institute of Meteorology and Water Management, National Research Institute , Maritime Branch Waszyngtona 42, PL 81-342 Gdynia , Poland 2 Gdańsk University , 63 Wita Stwosza Str., PL 80-803 Gdańsk , Poland 3 Jerzy Falandysz Numerous species of wild-grown mushrooms are among the most vulnerable organisms for contamination with radiocesium released from a radioactive fallout. A comparison was made on radiocesium as well as the natural gamma rayemitting radionuclide (40K) activity concentrations in the fruiting bodies of several valued edible Boletus mushrooms collected from the region of Europe and Yunnan Province in China. Data available for the first time for Boletus edulis collected in Yunnan, China, showed a very weak contamination with 137Cs. Radiocesium concentration activity of B. edulis samples that were collected between 2011 and 2014 in Yunnan ranged from 5.2±1.7 to 10±1 Bq kg−1 dry matter for caps and from 4.7±1.3 to 5.5±1.0 Bq kg−1 dry matter for stipes. The mushrooms Boletus badius, B. edulis, Boletus impolitus, Boletus luridus, Boletus pinophilus, and Boletus reticulatus collected from the European locations between 1995 and 2010 showed two to four orders of magnitude greater radioactivity from 137Cs compared to B. edulis from Yunnan. The nuclide 40K in B. badius was equally distributed between the caps and stipes, while for B. edulis, B. impolitus, B. luridus, B. pinophilus, and B. reticulatus, the caps were richer, and for each mushroom, activity concentration seemed to be more or less species-specific. China/Europe; Forest; Organic food; Radiocesium; Wild mushrooms - The nuclear accident in Chernobyl, which took place on 26th of April 1986 caused large- scale diffusion of radioactivity mostly in the Central and Northern Europe, but it was detected also in other southern areas in Turkey (IAEA 2005; Simsek et al. 2014). Because of that accident, the long-term residual radioactivity in the affected areas comes largely from radiocesium (137Cs) (Bulko et al. 2014). Contamination of soils, pastures, and forests with the post-Chernobyl 137Cs varied between the regions of Europe, and this fact highly impacted on regional appearance of 137Cs in food, feed, mushrooms, grazing cattle, and wildlife and health risk of 137Cs and other nuclides to human consumers (Barret et al. 1999; Battiston et al. 1989; De Cort et al. 1998; Smith et al. 1993; Strandberg and Knudsen 1994; Zarubina 2014). Some but minor (about 10 %) residual radioactivity from 137Cs in the soils and wild-grown mushrooms still comes from the radioactive fallout which had taken place in the 1950s and 1960s because of the nuclear weapon tests in the atmosphere (Haselwandter et al. 1988; Steinhauser et al. 2013; Taira et al. 2011). The nuclear power station in Fukushima Dai-ichi collapsed between 11th and 14th of March 2011 after a mega tsunami episode in the northeastern part of the Honshu Island— Tohoku region in Fukushima prefecture, Japan (Yasunari et al. 2011). In result of the Fukushima accident, a largescale diffusion of radioactivity took place. The radioactivity plume was largely dispersed in the ocean and in small portion on land there (Teramage et al. 2014). At the local scale, mushrooms in the prefecture of Fukushima have been identified as the most relevant source of radiocesium intake among vegetables, especially after the first year of the accident (Merz et al. 2015). Foraging of mushrooms bypass, wittingly or unwittingly, the governmental food measuring campaigns which leads to higher intake of radioactive cesium than when consumers bought their products in commercial shops (Hayano et al. 2013; Normile 2013). The airborne 137Cs that is deposited on land is efficiently taken up and sequestered in fruiting bodies by many wildgrown mushrooms (Macromycetes), which differ in their species-specific capacity to sequester stable Cs as well as many other metallic, non-metallic, and metalloid elements in the flesh (Bakken and Olsen 1990; Barret et al. 1999; Battiston et al. 1989; Brzostowski et al. 2011; Byrne et al. 1979; Eckl et al. 1986; Drewnowska and Falandysz 2015; Falandysz et al. 1994, 2003a, b, 2007a, b, c, d; Gucia et al. 2012; Kirchner and Daillant 1998; Kojta et al. 2012; Vinichuk et al. 2011; Zhang et al. 2010). These chemical elements, depending on their physical and chemical forms, can further be available from soil solution and soil bedrock to fungal mycelia, and sometimes, they can be sequestered in fungal flesh (fruiting bodies) more or less in a dose-effect-related manner. Hence, an elevated content of many metallic elements, metalloids, and Se (nonmetal) can be found in fruiting bodies of exposed populations, while the effectiveness of uptake and sequestration is a function of many variables including biological features related to species of mushroom, mycorrhiza, and geochemical/environmental factors (Falandysz and Borovička 2013). Edible wild-grown mushrooms are popular organic food and are even items of international trade, and Boletus spp. are especially popular in Europe (King Bolete, Bay Bolete, Pine Wood) and especially in Yunnan and several other provinces in China (Falandysz et al. 2011; Wang et al. 2014). This paper reports and compares data on the residual activity from 137Cs as well as natural radionuclide from 40K accumulated in certain Boletus mushrooms collected in Poland, Sweden, and Belarus and in Yunnan of China. The contamination of King Bolete (Boletus edulis) from Yunnan (a land of mushrooms) is reported internationally for the first time. A major source of the residual 137Cs for Poland without doubt is the Chernobyl accident (Mietelski et al. 2010), while for Yunnan, the likely sources include radioactive fallout from nuclear weapon tests in the 1950s and 1960s and possibly also because of the Chernobyl and Fukushima accidents. Materials and methods The fruiting bodies of Boletus badius, B. edulis, Boletus impolitus, Boletus luridus, Boletus pinophilus, and Boletus reticulatus mushrooms were collected in 1995–2014 in Poland, Belarus, and Sweden in Europe and in Yunnan in China. The mushrooms were collected across of Poland from different locations: Kacze Łęgi, Dziemiany, Sobieszewo, Mojusz, Kępice, Wdzydze, Parchowo, Bory Tucholskie, Olsztynek, Puszcza Piska, Puszcza Notecka, Porażyn, Włoszowa in Świętokrzyskie land, Chochołowska Valley in Tatra Mountains, and Kłodzka Dale in Sudety Mountains. Mushrooms from Belarus were collected from two spatially distant locations: Staroje Janczyna—location in central part, administrative circuit of Minsk, Borysowski Region, and Wasilewiczy in Chojniki area of the Gomel Region. Samples of B. edulis were also collected from the town of Umeå and its outskirts in northern region of Sweden and from Davingiie and Yimen in the Prefecture of Yuxi in the Yunnan Province of China. Fresh fruiting bodies’ samples (separately caps and stipes) were sliced using a plastic knife, dried at 65 °C to constant weight, and further pulverized using ceramic mortar and kept in brand new sealed polyethylene bags that were packed into larger bags and kept under dry and clean condition in a laboratory room until analysis. Before determination of activity concentration of radionuclides, the individual mushroom samples were pooled (separately caps and stipes, from 6 to 34 individuals per pool) to obtain one large (many specimens) integrated sample representing each place and year (Table 1). Activity concentrations of 137Cs and 40K were determined using gamma spectrometer with coaxial HPGe detector with a relative efficiency of 18 % and a resolution of 1.9 keV at 1.332 meV (with associated electronics). The detector was coupled with an 8192-channel computer analyzer and GENIE 2000 software (Zalewska and Staniewski 2011). The equipment was calibrated using a multi-isotope standard, and the method was fully validated. The laboratory involved was subjected for routine checks to ensure the high standards of analytical quality and analytical control as well as took part in the intercomparison exercises organized by IAEA-MEL Monaco (IAEA-414, Irish and North Sea Fish) (Zalewska and Staniewski 2011) to verify the reliability and accuracy of the method. All numerical data gained were recalculated for dehydrated fungal material (at 105 °C) and exact date of the sample collection. Data on radioactivity (expressed in Bq kg−1 dry matter) of 137Cs and 40K in caps and stipes of the Boletus mushrooms are summarized according to species, place of origin, size of sample, and year of collection (Table 1). Samples of B. edulis were from Europe and China. The Chinese mushrooms were collected at altitude of 1600–1650 m above sea level in the Yuxi Prefecture of the mountainous Province of Yunnan in 2011–2014 (Fig. 1). The mushrooms such as B. badius. B. edulis, B. impolitus, B. luridus, B. pinophilus, and B. reticulatus collected in the region of Europe (Belarus, Place and year of collection (number of specimens, n) in a pool Poland, Sweden) in 1995–2010 showed two to four orders of magnitude (depending on species and place) greater activity concentration of 137Cs when compared to B. edulis collected in Yunnan in 2011–2014 (Table 1). The nuclide, 40K, is a normal constituent of total K which is an important nutrient and the most abundant element in the fruiting bodies of mushrooms with a symbiotic or saprophyte life cycle. In B. edulis from Yimen in Yunnan, the activity of 40K was similar to that noted for the samples from Poland and Sweden (Table 1). Significantly lower values, less than 120 Bq kg−1 dm in caps and less than 140 Bq kg−1 dm in stipes, were found in mushrooms collected in 2014 in the Dayingjie region of Yunnan (the same was observed for 40K). This may be an indication of the deficiency of this important mineral nutrient in soils in Dayingjie, and this is worthy of further investigation. Distribution of 40K between the two morphological parts of the fruiting bodies for B. badius (caps and stipes) was nearly equal for most of the sites. The exception to this pattern was for samples from Wasilewiczy (Table 1). For B. edulis, Fig. 1 Localization of the sampling sites (1–21; for details see in Table 1) B. luridus, B. pinophilus, and B. reticlatus, the caps were frequently richer in 40K than the stipes, and only in the case of B. impolitus was the opposite characteristic observed. Data obtained for 137Cs in B. edulis from Kłodzka Dale in the Sudety Mountains (southwestern Poland) showed relatively high contamination of samples with activity in caps of 5700 ± 2 Bq kg−1 dm. Also, samples of B. edulis from the region of Umeå in Sweden collected in 1995 (1102±15 Bq kg−1 dm in caps and 904±12 Bq kg−1 dm in stipes) and Mojusz in the Pomerania land of Poland collected in 2007 (1358 ± 17 Bq kg−1 dm in whole fruiting body) were substantially contaminated with 137Cs. The lowest activity concentrations of 137Cs in B. edulis were found in samples gathered in the other Pomeranian region (Parchowo) in 2010 (497±9 Bq kg−1 dm in caps and 265±4 Bq kg−1 dm in stipes) (Table 1). In contrast, the activity concentrations of 137Cs in B. edulis from the Yuxi region of Yunnan were very low, i.e., from 5.2±1.7 to 10±1 Bq kg−1 dm for caps and 4.7±1.3 to 5.5±1.0 Bq kg−1 dm for stipes (Table 1). High activity of 137Cs were found also in other Boletus species: B. luridus collected from the forest with sandy soil bedrock at the Baltic Sea coastal place of the Sobieszewo Island near the city of Gdańsk, B. pinophilus from Puszcza Piska, and in B. reticulatus from Trójmiejski Landscape Park near the city of Gdynia (Table 1). The highest values were found in B. luridus; in 2000, the concentrations reached 3500±36 Bq kg−1 dm in caps and 1000±17 Bq kg−1 dm in stipes, while in B. pinophilus and in B. reticulatus, they were comparable and at the concentration of 1000 Bq kg−1 dm in caps and 400 Bq kg−1 dm in stipes. High levels of contamination with 137Cs were found in B. reticulatus from the outsktits of Wasilewiczy in the Chojniki Distict in the Gomel region of Belarus (Fig. 1). The activity found in this area was 6600 ± 109 Bq kg−1 dm in caps and 3500 ± 30 Bq kg−1 dm in stipes, lower than the values observed in B. badius collected at the same place and time, indicating possible differences in the 137Cs sequester capacity between these two species (Table 1). B. badius is well known to be susceptible to contamination with radiocesium (Malinowska et al. 2006). The samples from the post-Chernobyl polluted region of Gomel in Wasilewiczy, Belarus, collected in 2010 contained high amounts of 137Cs, i.e., around 21,000 Bq kg−1 dry matter (dm) in caps and around 15,000 Bq kg−1 dm in stipes (Table 1). The activity of 137Cs in B. badius from Poland varied depending on the sampling locations, and this could be roughly related to the regional differences in deposition of 137Cs on and in soils because of the Chernobyl nuclear accident (Grodzinskaya and Haselwandter 2003; Haselwandter et al. 1988; Mietelski et al. 2010). The highest values of 5100±45 Bq kg−1 dm in caps and 4600±48 Bq kg−1 dm in stipes were found in samples from the Bory Tucholskie site collected in the year 2000. A slightly lower activity of 137Cs, 4800±61 Bq kg−1 dm in caps and 2180 ± 190 Bq kg−1 dm in stipes, was found in B. badius collected in 1995–1996 from the complex forests of the Wdzydze Landscape Park which is very close to Bory Tucholskie (Malinowska et al. 2006; Falandysz et al. 2003a, b). The mushroom B. badius from two other large forest complexes of the Puszcza Notecka within the outskirts of Porażyn (Fig. 1) that was sampled in 2008 showed much lower levels of contamination when compared to the corresponding values for mushrooms sampled elsewhere in Poland in the 1990s by other researchers with 970±8 Bq kg−1 dm in the caps and 45± 2 Bq kg−1 dm in the stipes (Table 1) (Malinowska et al. 2006). The global radioactive fallout from nuclear weapon tests in the 1950s and 1960s and fallout from the Chernobyl accident has to be taken into account as a source of 137Cs accumulated in B. edulis growing in Europe (García et al. 2015; Malinowska et al. 2006; Mietelski et al. 2010). The 137Cs activity concentrations in B. badius and. B. reticulatus from Belarus, B. badius from Poland, and B. edulis from the Sudety Mountains in Poland are consistent with reported 137Cs general picture and Bhot spot^ deposition for regions of Belarus and Poland due to the Chernobyl accident (De Cort et al. 1998; Mietelski et al. 2010). There is no information available to indicate that the most recent radioactivity release from the Fukushima accident affected Yunnan. Lack of gamma-ray radiation from 134Cs in mushrooms sampled in Yunnan directly after the Fukushima accident in 2011 up to 2014 in this study (Table 1) and two other reports indicated that the contribution of Fukushima to the total radiocesium deposited there should be considered as negligible (Falandysz et al. 2015; Wang et al. 2015). On the other hand, earlier (pre-Fukishima accident period) data on the occurrence of 137Cs in wild-grown mushrooms from Japan and Taiwan (in Asia) showed negligible contamination and thus can indirectly reflects depositions of small amounts of airborne 137Cs after the Chernobyl accident and previous nuclear weapon tests in the atmosphere (134Cs because of short life time, t½ = 2 years, decayed until Fukushima accident) (Muramatsu et al. 1991; Tsukada et al. 1998; Wang et al. 1998). Previous data on 134Cs and 137Cs in Boletus spp. from Yunnan and other regions of China are lacking. The activity concentrations from 137Cs for samples from Yimen and Dayingjie (Yuxi Prefecture) were of the same order of magnitude, and this may indicate similarities in radioactive fallout there. Low activity concentrations of 137Cs determined in fruiting bodies of B. edulis from Yunnan presented in this study as well as in fruiting bodies of pan-tropical mushroom Macrocybe g i g a n t e a ( m e d i a n va l u e f o r de h y d r a t e d c a p s w a s 4.5 Bq kg−1 and 5.4 Bq kg−1 for stipes) and sclerotia of fungus Wolfiporia extensa (range from <1.4 to 7.2±1.1 Bq kg−1 dm) (Falandysz et al. 2015; Wang et al. 2015) definitely imply that radioactive contamination, which could have resulted from both the recent (Fukushima) and earlier (Chernobyl and/or nuclear weapon tests) sources, is negligible in this region. The content of stable Cs in fruiting bodies of mushrooms such as B. edulis and B. badius and also Cortinarius caperatus, Cortinarius saturatus, Cortinarius traganus, Dermocybe semisanguinea, Hydnum repandum, Laccaria amethystina, Lactarius allis, Lactarius piperatus, Lactarius rufus, Paxillus involutus, Suillus luteus, Tricholoma album, Tricholoma flavovirens, Tricholoma fulvum, Tricholoma robustum, Ramaria pallida, Sarcodon scabrum, and Xerocomus chrysenteron was greater when compared to many others (Bakken and Olsen 1990; Byrne et al. 1979; Falandysz et al. 2001b, 2007a, b, c, 2008; Horyna and Řanda 1988; Karadeniz and Yaprak 2010; Tsukada et al. 1998; Yoshida et al. 2004). Nevertheless, data for 134Cs, 137Cs, and stable 133Cs obtained for the same samples of mushrooms available from published literature is little is little (Karadeniz and Yaprak 2010; Yoshida et al. 2000). The relative abundance of 137Cs in mushroom as determined in this study for Boletus mushrooms from Europe can be attributed to three factors: species-specific uptake, requirement of this (stable Cs) element by the mushroom, and lastly by forest soil contamination with 137Cs at the sampling sites. Of secondary importance is the soil depth where the mushroom developed its mycelia, which is species-specific (Byrne 1998; Falandysz et al. 2014a; Stijve and Poretti 1990). The bulk of radioactive fallout as well as other airborne elemental contaminants are deposited and adsorbed on the top organic layer of forest soils. Some mushrooms with shallow mycelia can accumulate them readily and in considerable concentrations (Falandysz et al. 2014b; Mietelski et al. 2010; Stijve and Poretti 1990), and they subsequently infiltrate deeper into the soil layers (and the mycelia therein). This is dependent on the element’s concentration, while topography, humidity of climate, and soil structure can favor quicker vertical passage of the element under consideration into the deeper layers of the soil alongside with infiltrating rain, taking a portion of nuclides that were not readily adsorbed by litter and organic horizon of soil into deeper layers (Teramage et al. 2014). The low concentrations of 137Cs found in B. edulis from Yunnan are important for the inhabitants of the region. One reason is because the Boletus mushrooms are very popular organic foods, and numerous species are collected in Yunnan, which is well known for the mushrooms that can be found there (Wang et al. 2014; Wiejak et al. 2014; Zhang et al. 2010). Another reason is that in Yunnan, Boletes mushrooms are traditionally fried with hot vegetable oil using a wok (Chinese pan) but without pre-boiling (blanching). Blanching is a common procedure when cooking or pickling Boletus mushrooms in many countries including Poland. It results in the leaching out of some of the mushrooms’ water and water-soluble constituents (including 137Cs) into the water phase, thereby reducing their content in the final mushroom dish (Barret et al. 1999). The radioactive isotopes 134Cs and 137Cs can account for the Btotal^ Cs (stable Cs) content when measured using an instrumental method that is unable to differentiate between 134/137Cs and 133Cs. This is particularly important because the content of 134/137Cs in mushrooms is associated with 133Cs (Karadeniz and Yaprak 2010; Yoshida et al. 2000). As stated earlier, there is a dearth of data on 137Cs in mushrooms from China’s mainland (Marzano et al. 2001). No available information is found concerning the content of 134Cs and 137Cs, stable 133Cs, and 40K in B. edulis from Yunnan or other closely related species like B. pinophilus or B. reticulatus—all three are naturally rich in selenium and certain other chalcophile elements (Falandysz 2008, 2013; Falandysz et al. 2001a, 2007d, 2011; Frankowska et al. 2010; Costa-Silva et al. 2011). They and some other related species are naturally more abundant in stable 133Cs than many other mushrooms (Falandysz et al. 2001b, 2007d, 2008; Horyna and Řanda 1988). The content of potassium (K) is high in fruiting bodies of the mycorrhizal type mushrooms, e.g., at 29,000 ± 3000 mg kg−1 dm in caps of B. edulis, from 38,000±4000 to 55,000± 2000 mg kg−1 dm in Cantharellus cibarius, and from 28,000 ± 3000 to 50,000 ± 14,000 mg kg−1 dm in caps and from 21,000 ± 4000 to 35,000 ± 4000 in stipes of Suillus grevillei (Chudzyński and Falandysz 2008; Falandysz and Drewnowska 2015; Frankowska et al. 2010). Nuclide 40K is a long-living isotope and is a natural part of total K, which is an essential element and undergoes a homeostatic regulation in fruiting bodies by mushrooms (Falandysz and Borovička 2013; Stijve 1996). 40K is a dominant portion of the natural gammaradioactivity contained in the flesh of the fruiting bodies of mushrooms (Karadeniz and Yaprak 2010). The activity concentration of 40K had a little fluctuation and was a substantial portion of the total gamma-radioactivity contained in the flesh of the fruiting bodies of all the Boletus mushrooms foraged in Europe in this study, and in practice, almost a solely source in samples from Yunnan, where >100-fold exceeded activity concentration of 137Cs. In conclusion, the amount of 40K found in the fruiting bodies of a particular species of Boletus mushrooms collected from spatially distant places was more or less species-specific and stable with respect to time. On the other hand, a spatial pattern of activity of 137Cs in these mushrooms was mosaic-like, and this could be attributed to differences in the density of fallout and local soil conditions. For some areas of land located well away from the Chernobyl nuclear unit, the mosaic-like pattern of 137Cs accumulated in mushrooms (Boletus mushrooms) can reflect possible local differences in the density of fallout and the type of nuclides available to fungi when compared to what can be deduced from the expected pattern associated with pollution by 137Cs in European soils. To get a better knowledge on exposure rates and risk to consumers from 137Cs and other radionuclides in wild-grown mushrooms and especially the exposure to individuals, villagers and other high-level consumers of mushrooms need to be highlighted at any locality (e.g., forest) where mushrooms are highly contaminated. Acknowledgments This study in part was supported by the National Science Centre (Decision no. UMO-2011/03/N/NZ9/04136) and the National Natural Science Foundation of China (No. 31460538, 31260496). Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent Informed consent was obtained from all individual participants included in the study. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Boletus badius Pers . 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Jerzy Falandysz, Tamara Zalewska, Grażyna Krasińska, Anna Apanel, Yuanzhong Wang, Sviatlana Pankavec. Evaluation of the radioactive contamination in fungi genus Boletus in the region of Europe and Yunnan Province in China, Applied Microbiology and Biotechnology, 2015, 8217-8224, DOI: 10.1007/s00253-015-6668-0