Visn. Nac. Akad. Nauk Ukr. 2017. (6):61-76
https://doi.org/10.15407/visn2017.06.061

G.A. Grodzynska
Institute for Evolutionary Ecology of National Academy of Sciences of Ukraine, Kyiv

RADIONUCLIDE CONTAMINATION OF MACROMYCETES

This article reviews the literature and original data on radionuclides of natural and technogenous origin in wild-grown macromycetes. Wild edible mushrooms from contaminated areas (as a result of the Chornobyl catastrophe) are still dangerous for health in cases of medicinal and food use. Taking into account the complex nature of radionuclides contamination of wild macromycetes, the need for long-term radio-ecological monitoring is emphasized.
Keywords: radionuclides, macromycetes, bioaccumulation.

Language of article: ukrainian

REFERENCES

1.     Dighton J., Clint G.M., Poskitt J. Uptake and accumulation of 137Cs by upland grassland soil fungi: a potential pool of Cs immobilization. Mycol. Res. 1991. 95(9): 1052.

2.     Steiner M., Linkov I., Yoshida S. The role of fungi in the transfer and cycling of radionuclides in forest ecosystems. J. Environ. Radioact. 2002. 58(2–3): 217.

3.     Gadd G.M. Influence of microorganisms on the environmental fate of radionuclides. Endeavour. 1996. 20: 150.

4.     Grodzinskaya A.A., Syrchin S.A., Wasser S.P., Kuchma N.D. Macromycetes accumulative activity in radionuclide contamination conditions of the Ukraine territory. In: Zhdanova N.N. (ed.). Mycobiota of Ukrainian Polesie: Consequences of the Chernobyl disaster. (Kyiv: Naukova Dumka, 2013). P. 217–260; 368–373.

5.     Tyler G. Metals in sporophores of Basidiomycetes. Trans. Br. Mycol. Soc. 1980. 74: 41.

6.     Haselwandter K., Berreck M., Brunner P. Fungi as bioindicators of radiocesium contamination: pre- and post-Chernobyl activities. Trans. Br. Mycol. Soc. 1988. 90: 171.

7.     Haselwandter K., Leyval C., Sanders F.E. Impact of arbuscular mycorrhizal fungi upon plant uptake of heavy metals and radionuclides from soil. In: Gianianazzi S., Schuepp H. (eds.). Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems. (Basel: Birkhauser, 1994). P. 179–189.

8.     Dietl G., Breitig D. Radioaktives Caesium in Pilzen aus dem Raume Schwabisch Gmund. Zeitschrift für Mykologie. 1988. 54(1): 109.

9.     Dighton J., Horrill A.D. Radiocaesium accumulation in the mycorrhizal fungi Lactarius rufus and Inocybe longicystis, in upland Britain, following the Chernobyl accident. Trans. Br. Mycol. Soc. 1988. 91(2): 335.

10. Teherani D.K. Determination of 134Cs and 137Cs radioisotopes in various mushrooms from Austria one year after the Chernobyl incident. J. Radioanal. Nucl. Chem. Lett. 1988. 6(6): 401.

11. Haselwandter K., Berreck M. Radiocesium accumulation in fruitbodies of Basidiomycetes collected in the province of Parma, Italy. Fungi atque loci Natura, Atti del IV Convegno Intern. micol. del 27–30 IX 1987. Borgo Val di Taro, Italy, 1989. P. 89–92.

12. Haselwandter K., Berreck M. Accumulation of radiocesium in fungi. In: Winkelmann G., Winge D.R. (eds.). Metal ions in fungi. (New York; Basel; Hong Kong: Marcel Dekker, 1994). P. 259–277.

13. Bakken L.R., Olsen R.A. Accumulation of radiocaesium in fungi. Can. J. Microbiol. 1990. 36: 704.

14. Bem H., Lasota W., Kuśmierek E., Witusik M. Accumulation of 137Cs by mushrooms from Rogozno area of Poland over the period 1984–1988. J. Radioanal. Nucl. Chem. Lett. 1990. 145(1): 39.

15. Fraiture A., Guillite O., Lambinon J. Interest of fungi as bioindicators of the contamination in forest ecosystems. In: Desmet G., Nassimbeni P., Belli M. (eds.). Transfer of radionuclides in natural and semi-natural environments. (London; New York: Elsevier Applied Science, 1990). P. 477–484.

16. Wasser S.P., Grodzynska G.A., Lyugin V.O. Cs-134 and Cs-137 content in higher Basidiomycetes of Ukrainian Polissya. Ukrainian Botanical Journal. 1991. 48(5): 14.

17. Wasser S.P., Grodzynska G.A., Lyugin V.O. Uptake of radioactive elements by macromycetes of Ukrainian Polissya. Ukrainian Botanical Journal. 1992. 49(5): 79.]

18. Wasser S.P., Bolukh V.O., Brun’ G.O., Virchenko V.M., Grodzynska G.A., Kondratyuk S.Ya., Navrotska I.L., Stupina V.V., Tsarenko P.M. Uptake of radionuclides by cryptogame plants and higher fungi of Ukraine. (Kyiv, 1995).

19. Mietelski J.W., La Rosa J.L., Ghods A. 90Sr and 239+240Pu, 238Pu, 241Am in some samples of mushrooms and forest soils from Poland. J. Radioanal. Nucl. Chem. 1993. 179: 243.

20. Mietelski J.W., Jasinska M., Kubicka B., Kozak K., Macharski P. Radioactive contamination of Polish mushrooms. Sci. Total Environ. 1994. 157: 217.

21. Mietelski J.W., Macharski P., Jasinska M., Broda R. Radioactive contamination of forests in Poland. Biol. Trace Elem. Res. 1994. 4345: 715.

22. Smith M.L., Taylor H.W., Sharma H.D. Comparison of the Post-Chernobyl 137Cs contamination of mushrooms from Eastern Europe, Sweden, and North America. Appl. Environ. Microbiol. 1993. 59(1): 134.

23. Wasser S.P., Grodzinskaya A.A. Content of Radionuclides in Macromycetes of the Ukraine in 1990–1991. In: Fungi of Europe: Investigation, Recording and Conservation. (Royal Botanic Gardens, Kew, 1993). P. 189–210.

24. Yoshida S., Muramatsu Y. Concentrations of radiocesium and potassium in Japanese mushrooms. Environ. Sci. 1994. 7(1): 63.

25. Yoshida S., Muramatsu Y. Concentrations of Alkali and Alkaline Earth Elements in mushrooms and plants collected in a Japanese pine forest, and their relationship with 137Cs. J. Environ. Radioact. 1998. 41(2): 183.

26. Grodzinskaya A.A., Berreck M., Wasser S.P., Haselwandter K. Radiocesium in fungi: Accumulation pattern in the Kiev district of Ukraine including the Chernobyl zone. Sydowia. 1995. 10: 88.

27. Grodzinskaya A.A., Syrchin S.A., Kuchma N.D. Higher Basidiomycetes as bioindicators for radiocaesium contamination of territory of Ukraine. In: Botany and Mycology: modern horizons (to memory of Academician A.M. Grodzinsky (1926–1988). (Kyiv: Academperiodika, 2007). P. 263–275.

28. Grodzinskaya A.A., Syrchin S.A., Kuchma N.D., Bilay V.T. Radioactive contamination of Ukrainian wild-growing mushrooms. In: Mushroom Biology and Mushroom Products: Proc. 7th Int. Conf. (ICMBMP7). Arcachon, 2011. P. 566–572.

29. Fedorov V.N., Yeliashevich N.V. Accumulation of radionuclides in bodies of macromycetes. Radiation Biology. Radioecology. 2000. 40(6): 702.

30. Kalač P. A review of edible mushroom radioactivity. Food Chem. 2001. 75: 29.

31. Kalač P. Radioactivity of European wild growing edible mushrooms. In: Andres S., Baumann N. (eds). Mushrooms: Types, Properties and Nutrition. (New York, Nova Sci. Publ., 2012). P. 215–230.

32. Scheglov A.I. Biogeochemistry of technogenous radionuclides in forest ecosystems. (Moscow: Nauka, 1999).

33. Skwarzec B., Jakusik A. 210Po bioaccumulation by mushrooms from Poland. J. Environ. Monit. 2003. 5: 791.

34. Baeza A., Hernandez S., Guillén F., Moreno G., Manjón J.L., Pascual R. Radiocaesium and natural gamma emitters in mushrooms collected in Spain. Sci. Total Environ. 2004. 318(1): 59.

35. Baeza A., Guillén F.J., Salas A., Manjόn J.L. Distribution of radionuclides in different parts of a mushroom: Influence of the degree of maturity. Sci. Total Environ. 2006. 359(1): 255.

36. Ban-Nai T., Muramatsu Y., Yoshida S. Concentrations of 137Cs and 40K in mushrooms consumed in Japan and radiation dose as a result of their dietary intake. J. Radiat. Res. 2004. 45(2): 325.

37. Dvořák P., Kunová V., Beňová K., Ohera M. Radiocesium in mushrooms from selected locations in the Czech Republic and the Slovak Republic. Radiat. Environ. Biophys. 2006. 45(2): 145.

38. Grodzynska A., Syrchyn S., Kuchma M., Кonischuk V. Macromycetes — bioindicators of radiocaesium contamination of Ukrainian forest ecosystems. Visn. Nac. Akad. Nauk Ukr. 2008. (9): 26.

39. Dementyev D.V., Bolsunovsky A.Ya. Accumulation of artificial radionuclides by edible wild mushrooms and berries in the forests of the central part of the Krasnoyarskii Krai. Radioprotection. 2009. 44(5): 115.

40. Falandysz J., Borovička J. Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl. Microbiol. Biotechnol. 2013. 97: 477.

41. Lehto J., Vaaramaa K., Leskinen A. 137Сs, 233,240Pu and 241Am in boreal forest soil and their transfer into wild mushrooms and berries. J. Environ. Radioact. 2013. 116: 124.

42. Falandysz J., Zalewska T., Apanel A., Drewnowska M., Kluza K. Evaluation of the activity concentrations of 137Cs and 40K in some Chanterelle mushrooms from Poland and China. Environ. Sci. Pollut. Res. 2016. 23(19): 20039.

43. Falandysz J., Zhang J., Zalewska T. Radioactive artificial 137Cs and natural 40K activity in 21 edible mushrooms of the genus Boletus species from SW China. Environ. Sci. Pollut. Res. 2017. 24(9): 8189.

44. Grüter H. Radioactive fission product 137Cs in mushrooms in W. Germany during 1963–1970. Health Physics. 1971. 20: 655.

45. Haselwandter K. Radioactives Cäsium (137Cs) in Fruchtkörpern verschiedener Basidiomycetes. Z. Pilzkunde. 1977. 43: 323.

46. Mietelski J.W., Dubchak S., Błażej S., Anielska T., Turnau K. 137Cs and 40K in fruiting bodies of different fungal species collected in a single forest in southern Poland. J. Environ. Radioact. 2010. 101(9): 706.

47. Krolak E., Kwapulinski J., Fischer A. 137Cs and 40K isotopes in forest and wasteland soils in a selected region of eastern Poland 20 years after the Chernobyl accident. Radiat. Environ. Biophys. 2010. 49: 229.

48. Malinovska E., Szefer P., Bojanowski R. Radionuclide content in Xerocomus badius and the other commercial mushrooms from several regions of Poland. Food Chem. 2006. 97(1): 19.

49. Vaaramaa K., Solatie D., Aro L. Distribution of 210Pb and 210Po concentrations in wild berries and mushrooms in boreal forest ecosystems. Sci. Total Environ. 2009. 408: 84.

50. Gwynn J.P., Nalbandyan A., Rudolfsen G. 210Po, 210Pb, 40K and 137Cs in edible wild berries and mushrooms and ingestion doses to man from high consumption rates of these wild foods. J. Environ. Radioact. 2013. 116: 34.

51. Kirchner G., Daillant O. Accumulation of 210Pb, 226Ra and radioactive cesium by fungi. Sci. Total Environ. 1998. 222: 63.

52. Popa K., Pui A., Tanase C., Irimia R. Monitoring of 226Ra and 137Cs radioisotopes on Bistria Valley and their translocation in spontaneous macromycetes. Revista de Chimie (Bucharest). 2010. 61: 894.

53. Baeza A., Guillén J. Influence of the soil bioavailability of radionuclides on the transfer of uranium and thorium to mushrooms. Appl. Radiat. Isot. 2006. 64: 1020.

54. Lonnroth T., Lill J.-O., Bjorkholm A., Haavisto T., Slotte J.M.K. Activities of the 7Be and 137Cs nuclides in mushrooms from Southern and Western Finland. Proc. Radiochim. Acta. 2011. 1: 233.

55. Guillén J., Baeza A. Radioactivity in mushrooms: A health hazard? Food Chem. 2014. 154: 14.

56. Gans I. Radionuklidkonzentrationen in Berliner Pilzen. Z. Mykol. 1986. 52: 446.

57. Gans I. Radionuklidkonzentrationen in Berliner Pilzen (Teil 4). Z. Mykol. 1987. 53: 151.

58. Nifontova M.G., Aleksaschenko V.N. The content of Sr-90 and Cs-134,137 in fungi, lichens and mosses from the near zone of the Chernobyl nuclear power plant. Russian Journal of Ecology. 1992. (3): 26.

59. Rühm W., Kammerer L., Hiersche L., Wirth E. Estimation of future radiocaesium contamination of fungi on the basis of behavior patterns derived from past instances of contamination. J. Environ. Radioact. 1998. 39(2): 129.

60. Tsvetnova O.B., Shatrova N.E., Shcheglov A.I. The accumulation of radionuclides and heavy metals by mushroom’s complex in forestry ecosystems. Coll. Res. Contrib. Research Institute for Nuclear Studies. 2001. 3(5): 171.

61. Eckl P., Hofmann W., Türk R. Uptake of natural and man-made radionuclides by lichens and mushrooms. Radiat. Environ. Biophys. 1986. 25: 43.

62. Battiston G.A., Degetto S., Gerbasi R., Sbrignadello G. Radioactivity in mushrooms in Northeast Italy following the Chernobyl accident. J. Environ. Radioact. 1989. 9: 53.

63. Rückert G., Diehl J.F., Heilgeist M. Radioaktivitätsgehalte von 1987 und 1988 im Raum Karlsruhe gesammelten Pilzen. Z. Lebensm. Unters. Forsch. 1990. 190: 496.

64. Vinichuk M., Johanson K. Accumulation of 137Сs by fungal mycelium in forest ecosystems of Ukraine. J. Environ. Radioact. 2003. 64: 27.

65. Burova L.G. Ecology of macromycete fungi. (Moscow: Nauka, 1986).

66. Heinrich G. Uptake and transfer factors of 137Cs by mushrooms. Radiat. Environ. Biophys. 1992. 31(1): 39.

67. Bulko N.I., Shabaleva M.A., Kozlov A.K., Tolkacheva N.V., Mashkov I.A. The 137Cs accumulation by forest-derived products in the Gomel region. J. Environ. Radioact. 2014. 127: 150.

68. Oolbekkink G.T., Kuyper T.W. Radioactive caesium from Chernobyl in fungi. Mycologist. 1989. 3: 3.

69. Guillite O., Fraiture A., Lambinon J. Soil-fungi radiocaesium transfers in forest ecosystems. In: Desmet G., Nassimbeni P., Belli M. (eds.). Transfer of radionuclides in natural and semi-natural environments. (London: Elsevier, 1990).

70. Gillet A.G., Crout N.M.G. A review of 137Cs transfer to fungi and consequences for modeling environmental transfer. JEnviron. Radioact. 2000. 48: 95.

71. Klán J., Řanda Z., Benada J., Horyna J. Investigation of non-radioactive Rb, Cs, and radiocaesium in higher fungi. Czech. Mycol. 1988. 42: 158.

72. Grodzinskaya A.A., Berreck M., Haselwandter K., Wasser S.P. Radiocaesium Contamination of Wild-Growing Medicinal Mushrooms in Ukraine. Int. J. Med. Mushr. 2003. 5(1): 61.

73. Atlas. Ukraine. Radioactive Contamination. http://radatlas.isgeo.com.ua/

74. Decree of Ministry of Health of Ukraine. No 256. 03.05.2006. http://zakon2.rada.gov.ua/laws/show/z0845-06

75. Seeger R., Schweinshaut P. Vorkommen von Caesium in höheren Pilzen. Sci. Total Environ. 1981. 19: 253.

76. Zagrodzki P., Mietelski J.W., Krośniak M., Petelenz B. Accumulation of cesium and radiocesium in forest litter in selected regions of Poland and its influence on litter-to-mushroom transfer factor. In: Schrauzer G.N. (ed.). Biological Trace Element Research. (Humana Press Inc., 1994). P. 273–277.

77. Kuwahara C., Sugiyama H., Kato F. Cesium uptake by edible mushrooms and microorganisms isolated from mushroom substrata. Radioprotection-Colloques. 2002. 37(1): 347.

78. Horyna J., Randa Z. Uptake of radiocesium and alkali metals by mushrooms. J. Radioanal. Nucl. Chem. Lett. 1988. 127(2): 107.

79. Vinichuk M., Dahlberg A., Rosén K. Cesium (137Cs and 133Сs), Potassium and Rubidium in macromycete fungi and Sphagnum Plants. In: Singh N. (ed.). Radioisotopes Applications in Physical Sciences. (InTech, 2011). P. 279–310.

80. Rosén K., Vinichuk M., Nikolova I., Johanson K. Long-term effects of single potassium fertilization on 137Cs levels in plants and fungi in a boreal forest ecosystem. J. Environ. Radioact. 2011. 102: 178.

81. Heinrich G. Distribution of radiocaesium in the different parts of mushrooms. J. Environ. Radioact. 1993. 18(3): 229.

82. Guillite O., Melin J., Wallberg L. Biological pathways of radionuclides originating from the Chernobyl fallout in a boreal forest ecosystem. Sci. Total Environ. 1994. 157(1): 207.

83. Haselwandter K. Accumulation of the radioactive nuclide 137Cs in fruit-bodies of Basidiomycetes. Health Physics. 1978. 34: 713.

84. Steffan B., Steglich W. Die Hutfarbstoffe des Maronenrohrings (Xerocomus badius). Angew. Chem. 1984. 96: 435.

85. Dorsselaer A.V., Albrecht P., Albrecht-Gary A.M. Allosteric effects in norbadione A. A clue for the accumulation process of 137Cs in mushrooms? Chem. Commun. 2002. 7(9): 944.

86. Aumann D.C., Clooth G., Steffan B., Steiglich W. Complexation of Cesium 137 by the Cap Pigments of the Bay Boletus (Xerocomus badius). Angew. Chem. 1989. 28(4): 453.

87. Lehto J. Americium in the Finnish environment. Boreal Environ. Res. 2009. 14: 427.

88. Outola I. Effect of industrial pollution on the distribution of Pu and Am in soil and on soil-to-plant transfer of Pu and Am in a pine forest in SW Finland. J. Radioanal. Nucl. Chem. 2003. 257(2): 267.

89. Baeza A., Guillén J., Mietelski J.W. Uptake of alpha and beta emitters by mushrooms collected and cultured in Spain. J. Radioanal. Nucl. Chem. 2004. 261(2): 375.

90. Baeza A., Guillén J., Mietelski J.W., Gaca P. Soil-to-fungi transfer of 90Sr, 239+240Pu, and 241Am. Radiochim. Acta. 2006. 94: 75.

91. Dementyev D.V., Zotina T.A., Manukovsky N.S., Kalacheva G.S., Bolsunovsky A.Ya. Biosorption of 241Am from Aqueous Solutions and Its Biochemical Fractionation in Pleurotus ostreatus Mycelium. Doklady Biochemistry and Biophysics. 2015. 460(1–6): 34.

92. Merz S., Shozugawa K., Steinhauser G. Analysis of Japanese Radionuclide Monitoring Data of Food Before and After the Fukushima Nuclear Accident. Environ. Sci. Technol. 2015. 49: 2875.

93. Nakashima K., Orita M., Fukuda N., Taira Y., Hayashida N., Matsuda N., Takamura N. Radiocesium concentrations in wild mushrooms collected in Kawauchi Village after the accident at the Fukushima Daiichi Nuclear Power Plant. Peer J. 2015. 3: e1427.

94. Index Fungorum. http://www.indexfungorum.org/names/Names.asp