Skip to main content
SpringerLink
Log in

Bioremediation and Heavy Metal Uptake: Microbial Approaches at Field Scale

  • Chapter
  • First Online:
Bio-Geo Interactions in Metal-Contaminated Soils

Part of the book series: Soil Biology ((SOILBIOL,volume 31))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New York

    Google Scholar 

  • 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 11:107–114

    Article  Google Scholar 

  • Arnolds E (1988) Dynamics of macrofungi in 2 moist heathlands in Drenthe, the Netherlands. Acta Bot Neerlandica 37:291–305

    Google Scholar 

  • Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91

    Article  CAS  Google Scholar 

  • 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 169:516–522

    Article  CAS  Google Scholar 

  • 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 99:1200–1202

    Article  PubMed  Google Scholar 

  • 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 17:358–364

    Article  CAS  Google Scholar 

  • Büchel G, Bergmann H, Ebena G, Kothe E (2005) Geomicrobiology in remediation of mine waste. Chemie Erde-Geochemistry 65S1:1–5

    Article  Google Scholar 

  • Carlsson E, Büchel G (2005) Screening of residual contamination at a former uranium heap leaching site, Thuringia, Germany. Chemie Erde-Geochemistry 65S1:75–95

    Article  CAS  Google Scholar 

  • 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 25:335–347

    Article  PubMed  CAS  Google Scholar 

  • Cohen MD, Kargacin B, Klein CB, Costa M (1993) Mechanisms of chromium carcinogenicity and toxicity. Crit Rev Toxicol 23:255–281

    Article  PubMed  CAS  Google Scholar 

  • 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 147:367–379

    Article  CAS  Google Scholar 

  • 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 158:777–786

    Article  CAS  Google Scholar 

  • Deacon JW, Donaldson SJ, Last FT (1983) Sequences and interactions of mycorrhizal fungi on birch. Plant Soil 71:257–262

    Article  Google Scholar 

  • 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 87:163–171

    Article  Google Scholar 

  • Doğan HH, Şanda MA, Uyanöz R, Öztürk C, Çetin Ü (2006) Contents of metals in some wild mushrooms. Biol Trace Elem Res 110:79–94

    Article  PubMed  Google Scholar 

  • 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 31:3468–3474

    Article  CAS  Google Scholar 

  • Dushenkov V, Kumar PBAN, Motto H, Raskin I (1995) Rhizofiltration – the use of plants to remove heavy-metals from aqueous streams. Environ Sci Technol 29:1239–1245

    Article  PubMed  CAS  Google Scholar 

  • Fleming LV (1985) Experimental-study of sequences of ectomycorrhizal fungi on birch (Betula Sp) seedling root systems. Soil Biol Biochem 17:591–600

    Article  Google Scholar 

  • Forbes EA, Posner AM, Quirk JP (1976) Specific adsorption of divalent Cd, Co, Cu, Pb, and Zn on goethite. J Soil Sci 27:154–166

    Article  CAS  Google Scholar 

  • Gadde RR, Laitinen HA (1974) Studies of heavy-metal sorption by hydrous oxides. Abstracts of papers of the American Chemical Society, p 142

    Google Scholar 

  • Gade LH (2000) Highly polar metal – metal bonds in “early-late” heterodimetallic complexes. Ang Chem-Int Ed 39:2659–2678

    Article  Google Scholar 

  • 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 34:330–335

    Article  PubMed  Google Scholar 

  • Gast CH, Jansen E, Bierling J, Haanstra L (1988) Heavy-metals in mushrooms and their relationship with soil characteristics. Chemosphere 17:789–799

    Article  CAS  Google Scholar 

  • Gherghel F (2009) Identification and characterization of Quercus robur ectomycorrhiza in relation to heavy metal contamination. Dissertation, Friedrich-Schiller-Universität Jena, Jena

    Google Scholar 

  • 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 303:440–445

    Article  PubMed  CAS  Google Scholar 

  • 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 69:5–19

    Article  CAS  Google Scholar 

  • Gube M (2009) Ontogeny and phylogeny of gasteroid members of Agaricaceae (Basidiomycetes). Dissertation, Friedrich-Schiller-Universität Jena, Jena

    Google Scholar 

  • 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 31:227–232

    CAS  Google Scholar 

  • 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 94:12002–12006

    Article  PubMed  CAS  Google Scholar 

  • 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 76:121–132

    Article  PubMed  CAS  Google Scholar 

  • 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 37:463–473

    Article  CAS  Google Scholar 

  • Işiloğlu M, Merdivan M, Yilmaz F (2001) Heavy metal contents in some macrofungi collected in the northwestern part of Turkey. Arch Environ Contam Toxicol 41:1–7

    Article  PubMed  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC, Boca Raton, FL

    Google Scholar 

  • Kalač P, Svoboda L (2000) A review of trace element concentrations in edible mushrooms. Food Chem 69:273–281

    Article  Google Scholar 

  • 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 56:16–20

    Article  PubMed  CAS  Google Scholar 

  • Karamanos RE, Bettany JR, Stewart JWB (1976) Uptake of native and applied lead by alfalfa and bromegrass from soil. Can J Soil Sci 56:485–494

    Article  Google Scholar 

  • Korcak RF, Fanning DS (1985) Availability of applied heavy-metals as a function of type of soil material and metal source. Soil Sci 140:23–34

    Article  CAS  Google Scholar 

  • 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 57–67

    Chapter  Google Scholar 

  • 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 112:1069–1079

    Article  PubMed  Google Scholar 

  • Lange M (1982) Fleshy fungi in grass fields. Dependence on fertilization, grass species, and age of field. Nord J Bot 2:131–143

    Google Scholar 

  • Lange M (1984) Fleshy fungi in grass fields. 2. Precipitation and fructification. Nord J Bot 4:491–501

    Article  Google Scholar 

  • 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 11:359–368

    Article  Google Scholar 

  • Malinowska E, Szefer P, Falandysz J (2004) Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chem 84:405–416

    Article  CAS  Google Scholar 

  • 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 141:115–125

    Article  PubMed  CAS  Google Scholar 

  • 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 36:1997–2012

    Article  PubMed  CAS  Google Scholar 

  • Mleczko P (2004) Mycorrhizal and saprobic macrofungi of two zinc mines in southern Poland. Acta Biol Cracoviensa Series Botanica 46:25–38

    Google Scholar 

  • 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 65:115–129

    Article  CAS  Google Scholar 

  • Nriagu JO (1979) Global inventory of natural and anthropogenic emissions of trace-metals to the atmosphere. Nature 279:409–411

    Article  PubMed  CAS  Google Scholar 

  • 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 4:233–230

    Google Scholar 

  • 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 84:641–646

    Article  PubMed  CAS  Google Scholar 

  • 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 53:1177–1185

    Article  PubMed  CAS  Google Scholar 

  • 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 13:468–474

    Article  CAS  Google Scholar 

  • 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 48:1230–1233

    Article  PubMed  CAS  Google Scholar 

  • Scheffer F, Schachtschabel P, Blume H-P, Scheffer S (2002) Lehrbuch der Bodenkunde. 15. Aufl./edn. Spektrum, Akad. Verl., Heidelberg

    Google Scholar 

  • Scheffer F, Schachtschabel P, Blume H-P, Scheffer S (2008) Lehrbuch der Bodenkunde. 15. Aufl., [Nachdr.]/edn. Spektrum, Akad. Verl., Heidelberg

    Google Scholar 

  • Seeger R (1978) Cadmium in mushrooms. Zeitschrift für Lebensmitteluntersuchung und -forschung 166:23–34

    Article  CAS  Google Scholar 

  • Shaw PJA, Kibby G, Mayes J (2003) Effects of thinning treatment on an ectomycorrhizal succession under Scots pine. Mycol Res 107:317–328

    Article  PubMed  Google Scholar 

  • Shaw PJA, Lankey K (1994) Studies on the scots pine mycorrhizal fruitbody succession. Mycologist 8:173–175

    Google Scholar 

  • Staudenrausch S, Kaldorf M, Renker C, Luis P, Buscot F (2005) Diversity of the ectomycorrhiza community at a uranium mining heap. Biol Fertil Soils 41:439–446

    Article  Google Scholar 

  • 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 117:133–144

    Google Scholar 

  • Street JJ, Lindsay WL, Sabey BR (1977) Solubility and plant uptake of cadmium in soils amended with cadmium and sewage sludge. J Environ Qual 6:72–77

    Article  CAS  Google Scholar 

  • 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 246:61–67

    Article  PubMed  CAS  Google Scholar 

  • 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 209:317–324

    Article  CAS  Google Scholar 

  • Tüzen M, Sesli E, Soylak M (2007) Trace element levels of mushroom species from East Black Sea region of Turkey. Food Control 18:806–810

    Article  Google Scholar 

  • 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 85–108

    Google Scholar 

  • Vellinga EC (2004) Genera in the family Agaricaceae: evidence from nrITS and nrLSU sequences. Mycol Res 108:354–377

    Article  PubMed  CAS  Google Scholar 

  • 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 269:225–232

    Article  CAS  Google Scholar 

  • Yilmaz F, Işiloğlu M, Merdivan M (2003) Heavy metal levels in some macrofungi. Turk J Bot 27:45–56

    Google Scholar 

  • Zeien H, Brümmer GW (1989) Chemische Extraktion zur Bestimmung von Schwermetallbindungsformen in Böden. Mitt Dtsch Bodenkdl Ges 59:505–515

    Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Institute of Microbiology, Friedrich-Schiller-Universität, Neugasse 25, 07743, Jena, Germany

    Frank Schindler, Matthias Gube & Erika Kothe

Authors
  1. Frank Schindler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthias Gube
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erika Kothe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erika Kothe .

Editor information

Editors and Affiliations

  1. , Institute of Microbiology - Microbial Ph, Friedrich Schiller Universität Jena, Neugasse 25, Jena, 07745, Germany

    Erika Kothe

  2. Amity Institute of Microbial Sciences, Amity University Uttar Pradesh, Noida, 201303, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Schindler, F., Gube, M., Kothe, E. (2012). Bioremediation and Heavy Metal Uptake: Microbial Approaches at Field Scale. In: Kothe, E., Varma, A. (eds) Bio-Geo Interactions in Metal-Contaminated Soils. Soil Biology, vol 31. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23327-2_18

Download citation

Publish with us

Policies and ethics

Search

Navigation