On the possible role of macrofungi in the biogeochemical fate of uranium in polluted forest soils

Journal of Hazardous Materials

Volumn 280, Issue , 2014, Pages 79-88

  Kubrová, Jaroslava ^a,b   Žigová, Anna ^c   Řanda, Zdeněk ^b   Rohovec, Jan ^c   Gryndler, Milan ^d   Krausová, Ivana ^b   Dunn, Colin E ^e   Kotrba, Pavel ^f   Borovička, Jan ^b,c  

^a CHARLES UNIVERSITY   (Czech Republic)

^b NUCLEAR PHYSICS INSTITUTE   (Czech Republic)

^c INSTITUTE OF GEOLOGY   (Czech Republic)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^e Department of Biochemistry and Microbiology Institute of Chemical Technology Prague ^*  (Canada)

^f INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

Author keywords

Bioaccumulation; Ectomycorrhizae; Fungi; Lead; Silver; Soil; Thorium; Uranium

Indexed keywords

BIOACCUMULATION; BIOCHEMISTRY; DNA SEQUENCES; FORESTRY; FRUITS; LEAD; SILVER; SOILS; THORIUM; URANIUM; FUNGI;

BCR SEQUENTIAL EXTRACTION; BIOGEOCHEMICAL; CHEMICAL FRACTIONATION; CZECH REPUBLIC; DNA SEQUENCING; ECTOMYCORRHIZAE; ECTOMYCORRHIZAL; TOTAL CONTENT; FOREST SOILS; MACROFUNGI;

FUNGI; BIOACCUMULATION;

LEAD; SILVER; THORIUM; URANIUM; SOIL; SOIL POLLUTANT;

BIOACCUMULATION; BIOGEOCHEMISTRY; BIOTRANSFORMATION; CONIFEROUS FOREST; ECTOMYCORRHIZA; FOREST SOIL; FUNGUS; LEAD; SILVER; SOIL POLLUTION; THORIUM; URANIUM; BIOREMEDIATION; ENVIRONMENTAL FATE; FRACTIONATION; MICROBIAL ACTIVITY; MINING;

ARTICLE; BIOACCUMULATION; BIOGEOCHEMICAL CYCLE; BIOTRANSFORMATION; CONCENTRATION (PARAMETERS); CZECH REPUBLIC; DNA SEQUENCE; ECTOMYCORRHIZA; ENVIRONMENTAL IMPACT; EXTRACTION; FOREST SOIL; FRACTIONATION; NORWAY SPRUCE; NUCLEOTIDE SEQUENCE; PLANT ROOT; SOIL POLLUTION; ANALYSIS; CHEMISTRY; ECOSYSTEM; METABOLISM; MYCORRHIZA; SOIL; SOIL POLLUTANT; CONTROLLED STUDY; FUNGUS; MACROFUNGUS; NONHUMAN; SAPROTROPH; SPRUCE;

BIOCHEMISTRY; FRUITS; FUNGI; LEAD; NUCLEIC ACIDS; SILVER; SOIL; THORIUM; URANIUM;

CZECH REPUBLIC; PRIBRAM; STREDOCESKY;

CZECH REPUBLIC; ECOSYSTEM; MYCORRHIZAE; SOIL; SOIL POLLUTANTS; URANIUM;

FUNGI;

EID: 84906056482     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2014.07.050     Document Type: Article

References (92)

1. Craft E.S., Abu-Qare A.W., Flaherty M.M., Garofolo M.C., Rincavage H.L., Abou-Donia M.B. Depleted and natural uranium: chemistry and toxicological effects. J. Toxicol. Env. Heal. B 2004, 7:297-317.
2. Kabata-Pendias A. Trace Elements in Soils and Plants 2001, CRC Press, Boca Raton. fourth ed.
3. Pulford I.D. Gold and uranium. Trace Elements in Soils 2010, 551-565. Wiley, Chichester. P.S. Hooda (Ed.).
4. Regenspurg S., Margot-Roquier C., Harfouche M., Froidevaux P., Steinmann P., Junier P., Bernier-Latmani R. Speciation of naturally-accumulated uranium in an organic-rich soil of an alpine region (Switzerland). Geochim. Cosmochim. Acta 2010, 74:2082-2098.
5. Bednar A.J., Medina V.F., Ulmer-Scholle D.S., Frey B.A., Johnson B.L., Brostoff W.N., Larson S.L. Effects of organic matter on the distribution of uranium in soil and plant matrices. Chemosphere 2007, 70:237-247.
6. Graham M.C., Oliver I.W., MacKenzie A.B., Ellam R.M., Farmer J.G. An integrated colloid fractionation approach applied to the characterisation of porewater uranium-humic interactions at a depleted uranium contaminated site. Sci. Total. Environ. 2008, 404:207-217.
7. Bernier-Latmani R., Veeramani H., Dalla Vecchia E., Junier P., Lezama-Pacheco J., Suvorova E.I., Sharp J.O., Wigginton N.S., Bargar J.R. Non-uraninite products of microbial U(VI) reduction. Environ. Sci. Technol. 2010, 44:9456-9462.
8. Francis A.J., Dodge C.J. Bioreduction of uranium(VI) complexed with citric acid by Clostridia affects its structure and solubility. Environ. Sci. Technol. 2008, 42:8277-8282.
9. Gadd G.M. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 2007, 111:3-49.
10. Gadd G.M. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 2010, 156:609-643.
11. Gadd G.M., Rhee Y.J., Stephenson K., Wei Z. Geomycology: metals, actinides and Biominerals. Environ. Microbiol. Rep. 2012, 4:270-296.
12. Fomina M., Charnock J.M., Hillier S., Alvarez R., Gadd G.M. Fungal transformations of uranium oxides. Environ. Microbiol. 2007, 9:1696-1710.
13. Fomina M., Charnock J.M., Hillier S., Alvarez R., Livens F., Gadd G.M. Role of fungi in the biogeochemical fate of depleted uranium. Curr. Biol. 2008, 18:R375-R377.
14. Gadd G.M., Fomina M. Uranium and fungi. Geomicrobiol. J. 2011, 28:471-482.
15. Dupré de Boulois H., Joner E.J., Leyval C., Jakobsen I., Chen B.D., Roos P., Thiry Y., Rufyikiri G., Delvaux B., Declerck S. Impact of arbuscular mycorrhizal fungi on uranium accumulation by plants. J. Environ. Radioact. 2008, 99:775-784.
16. Falandysz J., Borovička J. Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl. Microbiol. Biotechnol. 2013, 97:477-501.
17. Guillén J., Baeza A. Radioactivity in mushrooms: a health hazard?. Food Chem. 2014, 154:14-25.
18. Borovička J., Kubrová J., Rohovec J., Řanda Z., Dunn C.E. Uranium, thorium and rare earth elements in macrofungi: what are the genuine concentrations?. Biometals 2011, 24:837-854.
19. García M.A., Alonso J., Melgar M.J. Lead in edible mushrooms: levels and bioaccumulation factors. J. Hazard. Mater. 2009, 167:777-783.
20. Borovička J., Kotrba P., Gryndler M., Mihaljevič M., Řanda Z., Rohovec J., Cajthaml T., Stijve T., Dunn C.E. Bioaccumulation of silver in ectomycorrhizal and saprobic macrofungi from pristine and polluted areas. Sci. Total Environ. 2010, 408:2733-2744.
21. Ruzicka V. Vein uranium deposits. Ore Geol. Rev. 1993, 8:247-276.
22. Suchara I., Sucharová J. Distribution of 36 element deposition rates in a historic mining and smelting area as determined through fine-scale biomonitoring techniques part II: relative long-term accumulated atmospheric deposition levels. Water Air Soil Pollut. 2004, 153:229-252.
23. Nieto P.M., Carbone S.S. Characterization of juvenile maritime pine (Pinus pinaster Ait.) ectomycorrhizal fungal community using morphotyping, direct sequencing and fruitbodies sampling. Mycorrhiza 2000, 19:91-98.
24. Borovička J., Noordeloos M.E., Gryndler M., Oborník M. Molecular phylogeny of Psilocybe cyanescens complex in Europe, with reference to the position of the secotioid Weraroa novae-zelandiae. Mycol. Prog. 2011, 10:149-155.
25. Borovička J., Dunn C.E., Gryndler M., Mihaljevič M., Jelínek E., Rohovec J., Rohošková M., Řanda Z. Bioaccumulation of gold in macrofungi and ectomycorrhizae from the vicinity of the Mokrsko gold deposit, Czech Republic. Soil Biol. Biochem. 2010, 42:83-91.
26. Kõljalg U., Larsson K.H., Abarenkov K., Nilsson R.H., Alexander I.J., Eberhardt U., Erland S., Hoiland K., Kjoller R., Larsson E., Pennanen T., Sen R., Taylor A.F.S., Tedersoo L., Vralstad T., Ursing B.M. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol. 2005, 166:1063-1068.
27. Jahn R., Blume H.P., Asio V.B., Spaargaren O., Schad P. Guidelines for Soil Description 2006, FAO, Rome. fourth ed.
28. IUSS Working Group WRB, World Reference Base for Soil Resources 2006, first update 2007, World Soil Resources Reports 103, FAO, Rome, 2007.
29. Pansu M., Gautheyrou J. Handbook of Soil Analysis: Mineralogical, Organic and Inorganic Methods 2006, Springer, Berlin-Heidelberg.
30. Řanda Z., Soukal L., Mizera J. Possibilities of the short-term thermal and epithermal neutron activation for analysis of macromycetes (mushrooms). J. Radioanal. Nucl. Chem. 2005, 264:67-76.
31. Řanda Z., Kučera J., Mizera J., Frána J. Comparison of the role of photon and neutron activation analyses for elemental characterization of geological, biological and environmental materials. J. Radioanal. Nucl. Chem. 2007, 271:589-596.
32. Rauret G., López-Sánchez J.F., Sahuquillo A., Rubio R., Davidson C., Ure A.M., Quevauviller Ph. Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. J. Environ. Monit. 1999, 1:57-61.
33. Rauret G., López-Sánchez J.F., Sahuquillo A., Barahona E., Lachica M., Ure A.M., Davidson C.M., Gomez A., Lück D., Bacon J., Yli-Halla M., Muntau H., Quevauviller Ph. Application of a modified BCR sequential extraction (three-step) procedure for the determination of extractable trace metal contents in a sewage sludge amended soil reference material (CRM 483), complemented by a three-year stability study of acetic acid and EDTA extractable metal content. J. Environ. Monit. 2000, 2:228-233.
34. Ettler V., Mihaljevič M., Komárek M. ICP-MS measurements of lead isotopic ratios in soils heavily contaminated by lead smelting: tracing the sources of pollution. Anal. Bioanal. Chem. 2004, 378:311-317.
35. Komárek M., Chrastný V., Štíchová J. Metal/metalloid contamination and isotopic composition of lead in edible mushrooms and forest soils originating from a smelting area. Env. Int. 2007, 33:677-684.
36. Evans L.J., Barabash J. Molybdenum, silver, thallium and vanadium. Trace Elements in Soils 2010, 515-549. Wiley, Chichester. P.S. Hooda (Ed.).
37. Ribera D., Labrot F., Tisnerat G., Narbonne J.F. Uranium in the environment: occurrence, transfer, and biological effects. Rev. Environ. Contam. Toxicol. 1996, 146:53-89.
38. Graham M.C., Oliver I.W., MacKenzie A.B., Ellam R.M., Farmer J.G. Mechanisms controlling lateral and vertical porewater migration of depleted uranium (DU) at two UK weapons testing sites. Sci. Total. Environ. 2011, 409:1854-1866.
39. 238U atom ratios in soil and earthworms in western Kosovo after the 1999 war. Sci. Total. Environ. 2005, 337:109-118.
40. Oliver I.W., Graham M.C., MacKenzie A.B., Ellama R.M., Farmer J.G. Assessing depleted uranium (DU) contamination of soil, plants and earthworms at UK weapons testing sites. J. Environ. Monit. 2007, 9:740-748.
41. Virtanen S., Vaaramaa K., Lehto J. Fractionation of U, Th, Ra and Pb from boreal forest soils by sequential extractions. Appl. Geochem. 2013, 38:1-9.
42. Oliver I.W., Graham M.C., MacKenzie A.B., Ellam R.M., Farmer J.G. Distribution and partitioning of depleted uranium (DU) in soils at weapons test ranges-investigations combining the BCR extraction scheme and isotopic analysis. Chemosphere 2008, 72:932-939.
43. Ash C., Tejnecký V., Šebek O., Němeček K., Žahourová-Dubová L., Bakardjieva S., Drahota P., Drábek O. Fractionation and distribution of risk elements in soil profiles at a Czech shooting range. Plant Soil Environ. 2013, 59:121-129.
44. Ettler V., Vaněk A., Mihaljevič M., Bezdička P. Contrasting lead speciation in forest and tilled soils heavily polluted by lead metallurgy. Chemosphere 2005, 58:1449-1459.
45. Jacobson A.R., McBride M.B., Baveye P., Steenhuis T.S. Environmental factors determining the trace-level sorption of silver and thallium to soils. Sci. Total Environ. 2005, 345:191-205.
46. Jones K.C., Peterson P.J., Davies B.E. Extraction of silver from soils and its determination by atomic-absorption spectrometry. Geoderma 1984, 33:157-168.
47. Jones K.C., Peterson P.J., Davies B.E., Minski M.J. Determination of silver in plants by flameless atomic absorption spectrometry and neutron activation analysis. Int. J. Env. Anal. Chem. 1985, 21:23-32.
48. K.J. Johanson, I. Nikolova, A.F.S. Taylor, M.M. Vinichuk, Uptake of Elements by Fungi in the Forsmark Area, Stockholm: Swedish Nuclear Fuel and Waste Management Co, Technical Report TR-04-26, 2004.
49. Hrynkiewicz K., Haug I., Baum C. Ectomycorrhizal community structure under willows at former ore mining sites. Eur. J. Soil Biol. 2008, 44:37-44.
50. Kalin M., Stokes P.M. Macrofungi on uranium mill tailings-associations and metal content. Sci. Total Environ. 1981, 19:83-94.
51. Staudenrausch S., Kaldorf M., Renker C., Luis P., Buscot F. Diversity of the ectomycorrhiza community at a uranium mining heap. Biol. Fertil. Soils 2005, 41:439-446.
52. Wichterey K., Sawallisch S. Naturally occurring radionuclides in mushrooms from uranium mining regions in Germany. Radioprotection 2002, 37(C1):353-358.
53. Baumann N., Arnold T., Haferburg G. Uranium contents in plants and mushrooms grown on a uranium-contaminated site near Ronneburg in Eastern Thuringia/Germany. Environ. Sci. Pollut. Res. 2013, 11:6921-6929.
54. Borovička J., Řanda Z. Distribution of iron, cobalt, zinc and selenium in macrofungi. Mycol. Prog. 2007, 6:249-259.
55. Brzostowski A., Falandysz J., Jarzyńska G., Zhang D. Bioconcentration potential of metallic elements by Poison Pax (Paxillus involutus) mushroom. J. Environ. Sci. Heal. Part A-Toxic/Hazard Subst. Environ. Eng. 2011, 46:378-393.
56. Brzostowski A., Jarzyńska G., Kojta A.K., Wydmańska D., Falandysz J. Variations in metal levels accumulated in Poison Pax (Paxillus involutus) mushroom collected at one site over four years. J. Environ. Sci. Health Part A-Toxic/Hazard Subst. Environ. Eng. 2011, 46:581-588.
57. Gast C.H., Jansen E., Bierling J., Haanstra L. Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 1988, 17:789-799.
58. Mietelski J.W., Baeza A.S., Guillén J., Buzinny M., Tsigankov N., Gaca P., Jasińska M., Tomankiewicz E. Plutonium and other alpha emitters in mushrooms from Poland, Spain and Ukraine. Appl. Radiat. Isot. 2002, 56:717-729.
59. McCreight J.D., Schroeder D.B. Cadmium, lead and nickel content of Lycoperdon perlatum Pers. in a roadside environment. Environ. Pollut. 1977, 13:265-268.
60. Quinche J.-P. Lycoperdon perlatum-mushroom that accumulates heavy metals and selenium [In French]. Mycol. Helv. 1990, 3:477-486.
61. Borovička J., Řanda Z., Jelínek E., Kotrba P., Dunn C.E. Hyperaccumulation of silver by Amanita strobiliformis and related species of the section Lepidella. Mycol. Res. 2007, 111:1339-1344.
62. Osobová M., Urban V., Jedelský P.L., Borovička J., Gryndler M., Ruml T., Kotrba P. Three metallothionein isoforms and sequestration of intracellular silver in the hyperaccumulator Amanita strobiliformis. New Phytol. 2011, 190:916-926.
63. Gryndler M., Hršelová H., Soukupová L., Borovička J. Silver release from decomposed hyperaccumulating Amanita solitaria fruit-body biomass strongly affects soil microbial community. Biometals 2012, 25:987-993.
64. Hooda P.S. Assessing bioavailability of soil trace elements. Trace Elements in Soils 2010, 229-265. Wiley, Chichester. P.S. Hooda (Ed.).
65. Luis P., Kellner H., Zimdars B., Langer U., Martin F., Buscot F. Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microbial. Ecol. 2005, 50:570-579.
66. Robinson C.H., Szaro T.M., Izzo A.D., Anderson I.C., Parkin P.I., Bruns T.D. Spatial distribution of fungal communities in a coastal grassland soil. Soil Biol. Biochem. 2009, 41:414-416.
67. Rosling A., Landeweert R., Lindahl B.D., Larsson K.H., Kuyper T.W., Taylor A.S.F., Finlay R.D. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol. 2003, 159:775-783.
68. Baldrian P. Enzymes of saprotrophic basidiomycetes. Ecology of Saprotrophic Basidiomycetes 2008, 551-565. Elsevier. L. Boddy, J.C. Frankland, P. van West (Eds.).
69. Borovička J., Mihaljevič M., Gryndler M., Kubrová J., Hršelová H., Řanda Z., Žigová A. Lead isotopic signatures of saprotrophic macrofungi of various origins: tracing for lead sources and possible applications in geomycology. Appl. Geochem. 2014, 43:114-120.
70. Clarholm M., Skyllberg U. Translocation of metals by trees and fungi regulates pH, soil organic matter turnover and nitrogen availability in acidic forest soils. Soil Biol. Biochem. 2013, 63:142-153.
71. Stijve T., Vellinga E.C., Herrmann A. Arsenic accumulation in some higher fungi. Persoonia 1990, 14:161-166.
72. Stijve T., Noorloos T., Byrne A.R., Šlejkovec Z., Goessler W. High selenium levels in edible Albatrellus mushroom. Dtsch. Lebensm-Rundsch. 1998, 94:275-279.
73. Borovička J., Řanda Z., Jelínek E. Antimony content of macrofungi from clean and polluted areas. Chemosphere 2006, 64:1837-1844.
74. Koch E., Kneifel H., Bayer E. Das Vorkommen von Amavadin in Pilzen der Gattung Amanita. Z. Naturforsch. 1987, 42c:873-878.
75. Ebbs S.D., Brady D.J., Kochian L.V. Role of uranium speciation in the uptake and transformation of uranium in plants. J. Exp. Bot. 1998, 49:1183-1190.
76. Rufyikiri G., Thiry Y., Wang L., Delvaux B., Declerck S. Uranium uptake and translocation by the arbuscular mycorrhizal fungus, Glomus intraradices, under root-organ culture conditions. New Phytol. 2002, 156:275-281.
77. 1 cells. Toxicol. Sci. 2008, 101:254-262.
78. Weiersbye I.M., Straker C.J., Przybylowicz W.J. Micro-PIXE mapping of elemental distribution in arbuscular mycorrhizal roots of the grass, Cynodon dactylon, from gold and uranium mine tailings. Nucl. Instrum. Methods Phys. Res. Sect. B-Beam Interact. Mater. Atoms 1999, 158:335-343.
79. + uptake systems. J. Mol. Microbiol. Biotechnol. 2006, 1:10-19.
80. Bertinato J., Cheung L., Hoque R., Plouffe L.J. Ctr1 transports silver into mamalian cells. J. Trace Elem. Med. Biol. 2010, 24:178-184.
81. Sácký J., Leonhardt T., Borovička J., Gryndler M., Briksí A., Kotrba P. Intracellular sequestration of zinc, cadmium and silver in Hebeloma mesophaeum and characterization of its metallothionein genes. Fungal Genet. Biol. 2014, 67:3-14.
82. Colpaert J.V., Wevers J.H.L., Krznaric E., Adriaensen K. How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Ann. For. Sci. 2011, 68:17-24.
83. Meharg A.A. The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol. Res. 2003, 107:1253-1265.
84. Berthelsen B.O., Olsen R.A., Steinnes E. Ectomycorrhizal heavy metal accumulation as a contributing factor to heavy metal levels in organic surface soils. Sci. Total Environ. 1995, 170:141-149.
85. Krupa P., Kozdrój J. Accumulation of heavy metals by ectomycorrhizal fungi colonizing birch trees growing in an industrial desert soil. World J. Microbiol. Biotechnol. 2004, 20:427-430.
86. Kottke I., Qian X.M., Pritsch K., Haug I., Oberwinkler F. Xerocomus badius - Picea abies, an ectomycorrhiza of high activity and element storage capacity in acidic soil. Mycorrhiza 1998, 7:267-275.
87. Chen B.D., Jakobsen I., Roos P., Zhu Y.G. Effects of the mycorrhizal fungus Glomus intraradices on uranium uptake and accumulation by Medicago truncatula L. from uranium-contaminated soil. Plant Soil 2005, 275:349-359.
88. Chen B.D., Zhu Y.G., Smith F.A. Effects of arbuscular mycorrhizal inoculation on uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from a uranium mining-impacted soil. Chemosphere 2006, 62:1464-1473.
89. Rufyikiri G., Huysmans L., Wannijn J., Hees M., Leyval C., Jakobsen I. Arbuscular mycorrhizal fungi can decrease the uptake of uranium by subterranean clover grown at high levels of uranium in soil. Environ. Pollut. 2004, 130:427-436.
90. Chen B.D., Jakobsen I., Roos P., Borggaard O.K., Zhu Y.G. Mycorrhiza and root hairs enhance acquisition of phosphorus and uranium from phosphate rock but mycorrhiza decreases root to shoot uranium transfer. New Phytol. 2005, 165:591-598.
91. Roos P., Jakobsen I. Arbuscular mycorrhiza reduces phytoextraction of uranium, thorium and other elements from phosphate rock. J. Environ. Radioact. 2008, 99:811-819.
92. Chen B.D., Roos P., Zhu Y.G., Jakobsen I. Arbuscular mycorrhizas contribute to phytostabilization of uranium in uranium mining tailings. J. Environ. Radioact. 2008, 99:801-810.