Bioremediation and Heavy Metal Uptake: Microbial Approaches at Field Scale

  • Frank Schindler
  • Matthias Gube
  • Erika Kothe
Part of the Soil Biology book series (SOILBIOL, volume 31)


The remediation of metal-contaminated soil is generally achieved by technical solutions. Bioremediation approaches include phytoremediation with plants taking up metals from the soil with the water phase and enriching these in above-ground biomass, which then can be further processed. On the other hand, phytostabilization is achieved when plants exclude the metals from uptake into above-ground tissue, thus allowing for the use of biomass for downstream applications such as energy production. The performance of plants is dependent on metal mobility in the soil, which is greatly influenced by the soil microbial population. Thus, phytoremediation strategies are evaluated here with regard to microbial impact. Emphasis is laid on field-scale experiments, which are performed to allow for assessing the function of soil bacteria and fungi for enhancement of plant performance in either phytoextraction or phytostabilization. Another bioremediation strategy is the use of fungal fruiting bodies for the accumulation of metals from the soil environment. This mycoremediation depends on the performance of fungi for metal uptake, which generally exceeds plant rates for metal uptake by far. Microbially enhanced phytoremediation is tested for its performance at the former uranium mining site near Ronneburg, Germany, where a test field site has been established. Furthermore, naturally occurring fungal fruiting bodies are collected and analyzed for use in mycoremediation.


Fruiting Body Bioavailable Fraction Microbial Inoculation Pisolithus Tinctorius Fungal Fruiting Body 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are grateful to FSU Jena Applied Geology staff especially D. Merten, U. Buhler, I. Kampand and G. Weinzierl for laboratory assistance, and to S. Formann for help in collecting fruiting bodies. The work was financially supported by the excellence graduate school JSMC and DFG GRK1257.


  1. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New YorkGoogle Scholar
  2. Agerer R (2001) Exploration types of ectomycorrhizae – a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  3. Arnolds E (1988) Dynamics of macrofungi in 2 moist heathlands in Drenthe, the Netherlands. Acta Bot Neerlandica 37:291–305Google Scholar
  4. Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91CrossRefGoogle Scholar
  5. Baum C, Hrynkiewicz K, Leinweber P, Meissner R (2006) Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix x dasyclados). J Plant Nutrition Soil Sci 169:516–522CrossRefGoogle Scholar
  6. Bazała MA, Gołda K, Bystrzejewska-Piotrowska G (2008) Transport of radiocesium in mycelium and its translocation to fruitbodies of a saprophytic macromycete. J Environ Radioact 99:1200–1202PubMedCrossRefGoogle Scholar
  7. Brunnert H, Zadražil F (1983) The translocation of mercury and cadmium into the fruiting bodies of 6 higher fungi – a comparative-study on species specificity in 5 lignocellulolytic fungi and the cultivated mushroom agaricus-bisporus. Eur J Appl Microbiol Biotechnol 17:358–364CrossRefGoogle Scholar
  8. Büchel G, Bergmann H, Ebena G, Kothe E (2005) Geomicrobiology in remediation of mine waste. Chemie Erde-Geochemistry 65S1:1–5CrossRefGoogle Scholar
  9. Carlsson E, Büchel G (2005) Screening of residual contamination at a former uranium heap leaching site, Thuringia, Germany. Chemie Erde-Geochemistry 65S1:75–95CrossRefGoogle Scholar
  10. Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347PubMedCrossRefGoogle Scholar
  11. Cohen MD, Kargacin B, Klein CB, Costa M (1993) Mechanisms of chromium carcinogenicity and toxicity. Crit Rev Toxicol 23:255–281PubMedCrossRefGoogle Scholar
  12. Colpaert JV, Vanden Koornhuyse P, Adriaensen K, Van Gronsveld J (2000) Genetic variation and heavy metal tolerance in the ectomycorrhizal basidiomycete Suillus luteus. New Phytol 147:367–379CrossRefGoogle Scholar
  13. Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J Plant Physiol 158:777–786CrossRefGoogle Scholar
  14. Deacon JW, Donaldson SJ, Last FT (1983) Sequences and interactions of mycorrhizal fungi on birch. Plant Soil 71:257–262CrossRefGoogle Scholar
  15. Dighton J, Poskitt JM, Howard DM (1986) Changes in occurrence of basidiomycete fruit bodies during forest stand development - with specific reference to mycorrhizal species. Trans Br Mycol Soc 87:163–171CrossRefGoogle Scholar
  16. Doğan HH, Şanda MA, Uyanöz R, Öztürk C, Çetin Ü (2006) Contents of metals in some wild mushrooms. Biol Trace Elem Res 110:79–94PubMedCrossRefGoogle Scholar
  17. Dushenkov S, Vasudev D, Kapulnik Y, Gleba D, Fleisher D, Ting KC, Ensley B (1997) Removal of uranium from water using terrestrial plants. Environ Sci Technol 31:3468–3474CrossRefGoogle Scholar
  18. Dushenkov V, Kumar PBAN, Motto H, Raskin I (1995) Rhizofiltration – the use of plants to remove heavy-metals from aqueous streams. Environ Sci Technol 29:1239–1245PubMedCrossRefGoogle Scholar
  19. Fleming LV (1985) Experimental-study of sequences of ectomycorrhizal fungi on birch (Betula Sp) seedling root systems. Soil Biol Biochem 17:591–600CrossRefGoogle Scholar
  20. Forbes EA, Posner AM, Quirk JP (1976) Specific adsorption of divalent Cd, Co, Cu, Pb, and Zn on goethite. J Soil Sci 27:154–166CrossRefGoogle Scholar
  21. Gadde RR, Laitinen HA (1974) Studies of heavy-metal sorption by hydrous oxides. Abstracts of papers of the American Chemical Society, p 142Google Scholar
  22. Gade LH (2000) Highly polar metal – metal bonds in “early-late” heterodimetallic complexes. Ang Chem-Int Ed 39:2659–2678CrossRefGoogle Scholar
  23. García MA, Alonso J, Fernández MI, Melgar MJ (1998) Lead content in edible wild mushrooms in northwest Spain as indicator of environmental contamination. Arch Environ Contam Toxicol 34:330–335PubMedCrossRefGoogle Scholar
  24. Gast CH, Jansen E, Bierling J, Haanstra L (1988) Heavy-metals in mushrooms and their relationship with soil characteristics. Chemosphere 17:789–799CrossRefGoogle Scholar
  25. Gherghel F (2009) Identification and characterization of Quercus robur ectomycorrhiza in relation to heavy metal contamination. Dissertation, Friedrich-Schiller-Universität Jena, JenaGoogle Scholar
  26. Gisbert C, Ros R, De Haro A, Walker DJ, Bernal MP, Serrano R, Navarro-Avino J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303:440–445PubMedCrossRefGoogle Scholar
  27. Grawunder A, Lonschinski M, Merten D, Büchel G (2009) Distribution and bonding of residual contamination in glacial sediments at the former uranium mining leaching heap of Gessen/Thuringia, Germany. Chemie Erde-Geochemistry 69:5–19CrossRefGoogle Scholar
  28. Gube M (2009) Ontogeny and phylogeny of gasteroid members of Agaricaceae (Basidiomycetes). Dissertation, Friedrich-Schiller-Universität Jena, JenaGoogle Scholar
  29. Hemkes OJ, Kemp A, Vanbroekhoven LW (1983) Effects of applications of sewage-sludge and fertilizer nitrogen on cadmium and lead contents of grass. Neth J Agric Sci 31:227–232Google Scholar
  30. Hibbett DS, Pine EM, Langer E, Langer G, Donoghue MJ (1997) Evolution of gilled mushrooms and puffballs inferred from ribosomal DNA sequences. Proc Natl Acad Sci USA 94:12002–12006PubMedCrossRefGoogle Scholar
  31. Hui N, Jumpponen A, Niskanen T, Liimatainen K, Jones KL, Koivula T, Romantschuk M, Strömmer R (2011) EcM fungal community structure, but not diversity, altered in a Pb-contaminated shooting range in a boreal coniferous forest site in Southern Finland. FEMS Microbiol Ecol 76:121–132PubMedCrossRefGoogle Scholar
  32. Humar M, Pohleven F, Šentjurc M (2004) Effect of oxalic, acetic acid, and ammonia on leaching of Cr and Cu from preserved wood. Wood Sci Technol 37:463–473CrossRefGoogle Scholar
  33. Işiloğlu M, Merdivan M, Yilmaz F (2001) Heavy metal contents in some macrofungi collected in the northwestern part of Turkey. Arch Environ Contam Toxicol 41:1–7PubMedCrossRefGoogle Scholar
  34. Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC, Boca Raton, FLGoogle Scholar
  35. Kalač P, Svoboda L (2000) A review of trace element concentrations in edible mushrooms. Food Chem 69:273–281CrossRefGoogle Scholar
  36. Karakaya A, Ilko M, Ulusu T, Akal N, Isimer A, Karakaya AE (1996) Lead levels in deciduous teeth of children from urban and suburban regions in Ankara (Turkey). Bull Environ Contam Toxicol 56:16–20PubMedCrossRefGoogle Scholar
  37. Karamanos RE, Bettany JR, Stewart JWB (1976) Uptake of native and applied lead by alfalfa and bromegrass from soil. Can J Soil Sci 56:485–494CrossRefGoogle Scholar
  38. Korcak RF, Fanning DS (1985) Availability of applied heavy-metals as a function of type of soil material and metal source. Soil Sci 140:23–34CrossRefGoogle Scholar
  39. Kratz S, Schnug E (2006) Rock phosphates and P fertilizers as sources of U contamination in agricultural soils. In: Merkel BJ, Hasche-Berger A (eds) Uranium in the environment. Springer, Berlin, pp 57–67CrossRefGoogle Scholar
  40. Krpata D, Peintner U, Langer I, Fitz WJ, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112:1069–1079PubMedCrossRefGoogle Scholar
  41. Lange M (1982) Fleshy fungi in grass fields. Dependence on fertilization, grass species, and age of field. Nord J Bot 2:131–143Google Scholar
  42. Lange M (1984) Fleshy fungi in grass fields. 2. Precipitation and fructification. Nord J Bot 4:491–501CrossRefGoogle Scholar
  43. Lange M (1991) Fleshy fungi of grass fields.3. Reaction to different fertilizers and to age of grass turf – periodicity of fruiting. Nord J Bot 11:359–368CrossRefGoogle Scholar
  44. Malinowska E, Szefer P, Falandysz J (2004) Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chem 84:405–416CrossRefGoogle Scholar
  45. McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125PubMedCrossRefGoogle Scholar
  46. Michelot D, Siobud E, Doré JC, Viel C, Poirier F (1998) Update on metal content profiles in mushrooms – toxicological implications and tentative approach to the mechanisms of bioaccumulation. Toxicon 36:1997–2012PubMedCrossRefGoogle Scholar
  47. Mleczko P (2004) Mycorrhizal and saprobic macrofungi of two zinc mines in southern Poland. Acta Biol Cracoviensa Series Botanica 46:25–38Google Scholar
  48. Neagoe A, Ebena G, Carlsson E (2005) The effect of soil amendments on plant performance in an area affected by acid mine drainage. Chemie Erde-Geochemistry 65:115–129CrossRefGoogle Scholar
  49. Nriagu JO (1979) Global inventory of natural and anthropogenic emissions of trace-metals to the atmosphere. Nature 279:409–411PubMedCrossRefGoogle Scholar
  50. Peay KG, Kennedy PG, Bruns TD (2011) Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecol 4:233–230Google Scholar
  51. Radulescu C, Stihi C, Busuioc G, Gheboianu AI, Popescu IV (2010) Studies concerning heavy metals bioaccumulation of wild edible mushrooms from industrial area by using spectrometric techniques. Bull Environ Contam Toxicol 84:641–646PubMedCrossRefGoogle Scholar
  52. Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185PubMedCrossRefGoogle Scholar
  53. Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotech 13:468–474CrossRefGoogle Scholar
  54. Sarikurkcu C, Tepe B, Semiz DK, Solak MH (2010) Evaluation of metal concentration and antioxidant activity of three edible mushrooms from Mugla, Turkey. Food Chem Toxicol 48:1230–1233PubMedCrossRefGoogle Scholar
  55. Scheffer F, Schachtschabel P, Blume H-P, Scheffer S (2002) Lehrbuch der Bodenkunde. 15. Aufl./edn. Spektrum, Akad. Verl., HeidelbergGoogle Scholar
  56. Scheffer F, Schachtschabel P, Blume H-P, Scheffer S (2008) Lehrbuch der Bodenkunde. 15. Aufl., [Nachdr.]/edn. Spektrum, Akad. Verl., HeidelbergGoogle Scholar
  57. Seeger R (1978) Cadmium in mushrooms. Zeitschrift für Lebensmitteluntersuchung und -forschung 166:23–34CrossRefGoogle Scholar
  58. Shaw PJA, Kibby G, Mayes J (2003) Effects of thinning treatment on an ectomycorrhizal succession under Scots pine. Mycol Res 107:317–328PubMedCrossRefGoogle Scholar
  59. Shaw PJA, Lankey K (1994) Studies on the scots pine mycorrhizal fruitbody succession. Mycologist 8:173–175Google Scholar
  60. Staudenrausch S, Kaldorf M, Renker C, Luis P, Buscot F (2005) Diversity of the ectomycorrhiza community at a uranium mining heap. Biol Fertil Soils 41:439–446CrossRefGoogle Scholar
  61. Stijve T, Andrey D, Goessler W, Guinberteau J, Dupuy G (2001) Étude comparative des métaux lourds et d'autres éléments traces dans Gyrophragmium dunalii et dans les agarics jaunissants de la section Arvenses. Bulletin trimestriel de la Société mycologique de France 117:133–144Google Scholar
  62. Street JJ, Lindsay WL, Sabey BR (1977) Solubility and plant uptake of cadmium in soils amended with cadmium and sewage sludge. J Environ Qual 6:72–77CrossRefGoogle Scholar
  63. 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 246:61–67PubMedCrossRefGoogle Scholar
  64. Thomet U, Vogel E, Krähenbühl U (1999) The uptake of cadmium and zinc by mycelia and their accumulation in mycelia and fruiting bodies of edible mushrooms. Eur Food Res Technol 209:317–324CrossRefGoogle Scholar
  65. Tüzen M, Sesli E, Soylak M (2007) Trace element levels of mushroom species from East Black Sea region of Turkey. Food Control 18:806–810CrossRefGoogle Scholar
  66. Vellinga EC (2001) Leucoagaricus. In: Noordeloos ME, Kuyper ThW, Vellinga EC (eds) Flora Agaricina Neerlandica, vol 5. Agaricaceae. A.A. Balkema, Lisse, Abingdon, Exton, Tokyo, pp 85–108Google Scholar
  67. Vellinga EC (2004) Genera in the family Agaricaceae: evidence from nrITS and nrLSU sequences. Mycol Res 108:354–377PubMedCrossRefGoogle Scholar
  68. Wang FY, Lin XG, Yin R (2005) Heavy metal uptake by arbuscular mycorrhizas of Elsholtzia splendens and the potential for phytoremediation of contaminated soil. Plant Soil 269:225–232CrossRefGoogle Scholar
  69. Yilmaz F, Işiloğlu M, Merdivan M (2003) Heavy metal levels in some macrofungi. Turk J Bot 27:45–56Google Scholar
  70. Zeien H, Brümmer GW (1989) Chemische Extraktion zur Bestimmung von Schwermetallbindungsformen in Böden. Mitt Dtsch Bodenkdl Ges 59:505–515Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Institute of MicrobiologyFriedrich-Schiller-UniversitätJenaGermany

Personalised recommendations