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  • Print publication year: 2007
  • Online publication date: October 2013

13 - Metal and mineral transformations: a mycoremediation perspective

from IV - Fungal bioremediation



In the periodic table, about 75% of the elements are classified as metals. While many metals are essential, e.g. K, Na, Ca, Mn, Mg, Fe, Cu, Zn, Co and Ni, many others have no apparent essential functions, e.g. Rb, Cs, Al, Cd, Ag, Au, Sr, U, Hg, Pb (Gadd, 1993). However, all can interact with fungi and most of them can exhibit toxicity above a certain threshold concentration, which will vary depending on the organism, metal species and environmental factors (Gadd & Griffiths, 1978; Gadd, 1993).

The redistribution of toxic metals in the biosphere as a result of human activity has become an important process in the biogeochemical cycling of these metals. The main source of metal pollution is industrialization including operational and former mining sites, foundries and smelters, untreated sewage sludge, and as diffuse sources, metal piping, traffic, combustion by-products from coal-burning power stations, and other atmospheric pollution. Arsenic, cadmium, chromium, copper, nickel, lead and mercury are the most common metal pollutants (Knox et al., 2000) with a selection of metal radionuclides also entering the environment from a number of sources (Gadd, 2005).

Unlike degradable organic contaminants, metals are not decomposed in the environment. They can, however, be buried (or otherwise contained), removed and recycled, or transformed into less toxic forms (Knox et al., 2000), these processes employing physical, chemical and biological methods singly or in combination.

Andriaensen, K., Lelie, D., Laere, A., Vangrosveld, J. & Colpaert, J. V. (2003). A zinc-adapted fungus protects pines from zinc stress. New Phytologist, 161, 549–55.
Banfield, J. P., Barker, W. W., Welch, S. A. & Taunton, A. (1999). Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proceedings of the National Academy of Sciences USA, 96, 3404–11.
Blaylock, M. J. & Huang, J. W. (2000). Phytoextraction of metals. In Phytoremediation of Toxic Metals: Using Plants to Clean-up the Environment, eds. Raskin, I. & Ensley, B. D.. New York: John Wiley & Sons, Inc, pp. 53–70.
Brandl, H. (2001). Heterotrophic leaching. In Fungi in Bioremediation, ed. Gadd, G. M.. Cambridge: Cambridge University Press, pp. 383–423.
Brown, M. T. & Wilkins, D. A. (1985). Zinc tolerance of mycorrhizal Betula. New Phytologist, 99, 101–6.
Brown, S., Chaney, R., Hallfrisch, J., Ryan, J. A. & Berti, W. R. (2004). In situ soil treatments to reduce the phyto- and bioavailability of lead, zinc, and cadmium. Journal of Environmental Quality, 33, 522–31.
Burford, E. P., Fomina, M., Gadd, G. M. (2003). Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineralogical Magazine, 67, 1127–55.
Burgstaller, W. & Schinner, F. (1993). Leaching of metals with fungi. Journal of Biotechnology, 27, 91–116.
Castaldi, P., Santona, L. & Melis, P. (2005). Heavy metal immobilization by chemical amendments in a polluted soil and influence on white lupin growth. Chemosphere, 60, 365–71.
Chen, X.-B., Wright, J. V., Conca, J. L. & Peurrung, L. M. (1997). Evaluation of heavy metal remediation using mineral apatite. Water, Air and Soil Pollution, 98, 57–78.
Chen, B. D., Shen, H., Li, X. L., Feng, G. & Christie, P. (2004a). Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant and Soil, 261, 219–29.
Chen, B. D., Liu, Y., Shen, H., Li, X. L. & Christie, P. (2004b). Uptake of cadmium from an experimentally contaminated calcareous soil by arbuscular mycorrhizal maize (Zea mays L.). Mycorrhiza, 14, 347–54.
Christie, P., Li, X. L. & Chen, B. D. (2004). Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil, 261, 209–17.
Coleman, N. J., Lee, W. E. and Slipper, I. J. (2005). Interactions of aqueous Cu2 +, Zn2 + and Pb2 + ions with crushed concrete fines. Journal of Hazardous Materials, 121, 203–13.
Colpaert, J. V. & Assche, J. A. (1992). Zinc toxicity in ectomycorrhizal Pinus sylvestris. Plant and Soil, 143, 201–11.
Colpaert, J. V., Muller, L. A. H., Lambaerts, M., Andriaensen, K. & Vangronsveld, J. (2004). Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytologist, 162, 549–59.
Conca, J. L. (1997). Phosphate-induced metal stabilization (PIMS). Final Report to the US Environmental Protection Agency 68D60023, Res. Triangle Park, NC.
Cotter-Howells, J. D. & Caporn, S. (1996). Remediation of contaminated land by formation of heavy metal phosphates. Applied Geochemistry, 11, 335–42.
Fomina, M., and Gadd, G. M. (2002). Metal sorption by biomass of melanin-producing fungi grown in clay-containing medium. Journal of Chemical Technology and Biotechnology, 78, 23–34.
Fomina, M. A., Alexander, I. J., Hillier, S. & Gadd, G. M. (2004). Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiological Journal, 21, 351–66.
Fomina, M., Burford, E. P. & Gadd, G. M. (2005a). Toxic metals and fungal communities. In The Fungal Community: Its Organization and Role in the Ecosystem, eds. Dighton, J., White, J. & Oudemans, P.. Boca Raton, FLA: CRC Press, Taylor & Francis Group, pp. 733–58.
Fomina, M., Hillier, S., Charnock, J. M., Melville, K., Alexander, I. J. & Gadd, G. M. (2005b). Role of oxalic acid over-excretion in toxic metal mineral transformations by Beauveria caledonica. Applied and Environmental Microbiology, 71, 371–81.
Fomina, M. A., Alexander, I. J., Colpaert, J. V. & Gadd, G. M. (2005c). Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biology and Biochemistry, 37, 851–66.
Fomina, M., Charnock, J. M., Hillier, S., Alexander, I. J. & Gadd, G. M. (2006a). Zinc phosphate transformations by the Paxillus involutus/pine ectomycorrhizal association. Microbial Ecology, 52, 322–33.
Fomina, M., Charnock, J., Bowen, A. D. & Gadd, G. M. (2006b). X-ray absorption spectroscopy (XAS) of toxic metal mineral transformations by fungi. Environmental Microbiology (in press).
Fourest, E., Serre, A. & Roux, J. C. (1996). Contribution of carboxylic groups to heavy metal binding sites in fungal cell walls. Toxicological and Environmental Chemistry, 54, 1–10.
Gadd, G. M. (1990). Fungi and yeasts for metal binding. In Microbial Mineral Recovery, eds. Ehrlich, H. & Brierley, C. L.. New York: McGraw-Hill, pp. 249–75.
Gadd, G. M. (1993). Interactions of fungi with toxic metals. New Phytologist, 124, 25–60.
Gadd, G. M. (1999). Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Advances in Microbial Physiology, 41, 47–92.
Gadd, G. M. (2000). Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Current Opinion in Biotechnology, 11, 271–9.
Gadd, G. M. (2001). Metal transformations. In Fungi in Bioremediation, ed. Gadd, G. M.. Cambridge: Cambridge University Press, pp. 250–382.
Gadd, G. M. (2004). Mycotransformation of organic and inorganic substrates. Mycologist, 18, 60–70.
Gadd, G. M. (2005). Microorganisms in toxic metal polluted soils. In Microorganisms in Soils: Roles in Genesis and Functions, eds. Buscot, F. & Varma, A.. Berlin: Springer-Verlag, pp. 325–56.
Gadd, G. M. & Griffiths, A. J. (1978). Microorganisms and heavy metal toxicity. Microbial Ecology, 4, 303–17.
Gadd, G. M., Fomina, M. & Burford, E. P. (2005). Fungal roles and function in rock, mineral and soil transformations. In Microorganisms in Earth Systems, eds. Gadd, G. M., Semple, K. T. & Lappin-Scott, H. M., Cambridge: Cambridge University Press, pp. 201–31.
Garrido, F., Illera, V. & Garcia-Gonzalez, M. T. (2005). Effect of the addition of gypsum- and lime-rich industrial by-products on Cd, Cu and Pb availability and leachability in metal-spiked acid soils. Applied Geochemistry, 20, 397–408.
Garcia-Sanchez, A., Alastuey, A. & Querol, X. (1999). Heavy metal adsorption by different minerals: application to the remediation of polluted soils. Science of the Total Environment, 242, 179–88.
Ghosh, M. & Singh, S. P. (2005). A comparative study of cadmium phytoextraction by accumulator and weed species. Environmental Pollution, 133, 365–71.
Gorbushina, A. A., Krumbein, W. E., Hamann, R., Panina, L., Soucharjevsky, S. & Wollenzien, U. (1993). On the role of black fungi in colour change and biodeterioration of antique marbles. Geomicrobiology Journal, 11, 205–21.
Hartley-Whitaker, J., Cairney, J. W. G. & Meharg, A. A. (2000). Sensitivity to Cd and Zn of host and symbiont of ectomicorrhizal Pinus sylvestris L. (Scots pine) seedlings. Plant and Soil, 218, 31–42.
Hoffland, E., Giesler, R., Jongmans, T. & Breemen, N. (2002). Increasing feldspar tunneling by fungi across a north Sweden podzol chronosequence. Ecosystems, 5, 11–22.
Hu, Z. Q., Yang, X. H., Zhu, Y. G. & Zhang, Y. C. (2004). Remediation of Cu2 + contaminated soil with Na-bentonite. Rare Metal Materials and Engineering, 33, 92–5.
Jentschke, G. & Godbold, D. L. (2000). Metal toxicity and ectomycorrhizas. Physiologia Plantarum, 109, 107–16.
Jones, M. D. & Hutchinson, T. C. (1988). Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. II. Uptake of nickel, calcium, magnesium, phosphorus and iron. New Phytologist, 108, 461–70.
Khan, A. G. (2005). Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. Journal of Trace Elements in Medicine and Biology, 18, 355–64.
Knox, A. S., Seaman, J. C., Mench, M. J. & Vangronsveld, J. (2000). Remediation of metal- and radionuclides-contaminated soils by in situ stabilization techniques. In Environmental Restoration of Metals-Contaminated Soil, ed. Iskandar, I. K.. Boca Raton, FLA: Lewis Publishers, pp. 21–61.
Krämer, U. (2005). Phytoremediation: novel approaches to cleaning up polluted soils. Current Opinion in Biotechnology, 16, 133–41.
Krupa, P. & Kozdroj, J. (2004). Accumulation of heavy metals by ectomycorrhizal fungi colonizing birch trees growing in an industrial desert soil. World Journal of Microbiology and Biotechnology, 20, 427–30.
Kumar, R. & Kumar, A. V. (1999). Biodeterioration of Stone in Tropical Environments: An Overview. USA: The J. Paul Getty Trust.
Lesage, E., Meers, E., Vervaeke, P., Lamsal, S., Hopgood, M., Tack, F. & Verloo, M. (2005). Enhanced phytoextraction: II. Effect of EDTA and citric acid on heavy metal uptake by Helianthus annuus from a calcareous soil. International Journal of Phytoremediation, 7, 143–52.
Leyval, C. & Joner, E. J. (2001). Bioavailability of heavy metals in the mycorrhizosphere. In Trace Elements in the Rhizosphere, ed. Gobran, G. R., Wenzel, W. W. & Lombi, E.. Boca Raton, FLA: CRC Press, pp. 165–85.
Lima, I. M., Marshall, W. E. and Wartelle, I. Y. H. (2004). Hardware-based granular activated carbon for metals remediation. Journal of the American Water Works Association, 96, 95–102.
Martino, E., Perotto, S., Parsons, R. & Gadd, G. M. (2003). Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biology and Biochemistry, 35, 133–41.
Meers, E., Lesage, E., Lamsal, S., Hopgood, M., Vervaeke, P., Tack, F. & Verloo, M. (2005). Enhanced phytoextraction: I. Effect of EDTA and citric acid on heavy metal mobility in a calcareous soil. International Journal of Phytoremediation, 7, 129–42.
Meharg, A. A. (2003). The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycological Research, 107, 1253–65.
Meharg, A. A. & Cairney, J. W. G. (2000). Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Advances in Ecological Research, 30, 69–112.
Money, N. P. (2004). The fungal dining habit – a biomechanical perspective. Mycologist, 18, 71–6.
Morley, G. F. & Gadd, G. M. (1995). Sorption of toxic metals by fungi and clay minerals. Mycological Research, 99, 1429–38.
Olsson, P. A., Wallander, H. (1998). Interactions between ectomycorrhizal fungi and the bacterial community in soils amended with various primary minerals. FEMS Microbiology Ecology, 27, 195–205.
Panfili, F. R., Manceau, A., Sarret, G., Spadini, L., Kirpichtchikova, T., Bert, V., Laboudigue, A., Marcus, M. A., Ahamdach, N. & Libert, M.-F. (2005). The effect of phytostabilization on Zn speciation in a dredged contaminated sediment using scanning electron microscopy, X-ray fluorescence, EXAFS spectroscopy, and principal components analysis. Geochimica et Cosmochimica Acta, 69, 2265–84.
Paris, F., Bonnaud, P., Ranger, J. & Lapeyrie, F. (1995). In vitro weathering of phlogopite by ectomycorrhizal fungi I. Effect of K+ and Mg2 + deficiency on phyllosilicate evolution. Plant and Soil, 177, 191–201.
Perotto, S. & Martino, E. (2001). Molecular and cellular mechanisms of heavy metal tolerance in mycorrhizal fungi: what perspectives for bioremediation?Minerva Biotechnologica, 13, 55–63.
Prasad, M. N. V. & Freitas, H. M. (2003). Metal hyperaccumulation in plants – biodiversity prospecting for phytoremediation technology. Electronic Journal of Biotechnology, 6, 285–321.
Ryan, J. A., Zhang, P., Hesterberg, D., Chou, L. & Sayers, D. E. (2001). Formation of chloropyromorphite in a lead-contaminated soil amended with hydroxyapatite. Environmental Science and Technology, 35, 3798–803.
Raskin, I., Smith, R. D. & Salt, D. E. (1997). Phytoremediation of metals: using plants to remove pollutants from the environment. Current Opinion in Biotechnology, 8, 221–6.
Sarret, G., Manceau, A., Cuny, D., Haluwyn, C., Deruelle, S., Hazemann, J.-L., Soldo, Y., Eybert-Berard, L. & Menthonnex, J.-J. (1998). Mechanisms of lichen resistance to metallic pollution. Environmental Science and Technology, 32, 3325–30.
Sarret, G., Manceau, A., Spadini, L., Roux, J. R., Hazemann, J. L., Soldo, Y., Eybert-Berard, L., Monthennex, J. J. (1999). Structural determination of Pb binding sites in Penicillium chrysogenum cell walls by EXAFS spectroscopy and solution chemistry. Journal of Synchrotron Radiation, 6, 414–16.
Sarret, G., Saumitou-Laprade, P., Bert, V., Proux, O., Hazemann, J.-L., Traverse, A., Marcus, M. A. & Manceau, A. (2002). Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiology, 130, 1815–26.
Sayer, J. A., Kierans, M. & Gadd, G. M. (1997). Solubilization of some naturally occurring metal-bearing minerals, limescale and lead phosphate by Aspergillus niger. FEMS Microbiology Letters, 154, 29–35.
Sayer, J. A., Cotter-Howells, J. D., Watson, C., Hillier, S. & Gadd, G. M. (1999). Lead mineral transformation by fungi. Current Biology, 9, 691–4.
Sersen, F., Cik, G., Havranek, E. & Sykorova, M. (2005). Bio-remediation by natural zeolite on plants cultivated in a heavy metal-contaminated medium. Fresenius Environmental Bulletin, 14, 13–17.
Smith, S. E. & Read, D. J. (1997). Mycorrhizal Symbiosis. London, UK: Academic Press.
Sterflinger, K. (2000). Fungi as geologic agents. Geomicrobiology Journal, 17, 97–124.
Tandy, S., Bossart, K., Mueller, R., Ritschel, J., Hauser, L., Schulin, R. & Nowack, B. (2004). Extraction of heavy metals from soils using biodegradable chelating agents. Environmental Science and Technology, 38, 937–44.
Terzano, R., Spagnuolo, M., Medici, L., Tateo, F. & Ruggiero, P. (2005). Copper stabilization by zeolite synthesis in polluted soils treated with coal fly ash. Environmental Science and Technology, 39, 6280–7.
Tichelen, K. K., Colpaert, J. V. & Vangronsveld, J. (2001). Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytologist, 150, 203–13.
Tobin, J. M. (2001). Fungal metal biosorption. In Fungi in Bioremediation, ed. Gadd, G. M.. Cambridge: Cambridge University Press, pp. 424–44.
Turnau, K., Kottke, I. & Dexheimer, J. (1996). Toxic element filtering in Rhizopogon roseolus/Pinus sylvestris mycorrhizas collected from calamine dumps. Mycological Research, 100, 16–22.
Verrecchia, E. P. (2000). Fungi and sediments. In Microbial Sediments, eds. Riding, R. E. & Awramik, S. M.. Berlin: Springer Verlag, pp. 69–75.
Watanabe, M. E. (1997). Phytoremediation on the brink of commercialization. Environmental Science and Technology, 31, 182–6.
Wenzel, W. W., Lombi, E. & Adriano, D. C. (2004). Biogeochemical processes in the rhizosphere: role in phytoremediation of metal-polluted soils. In Heavy Metal Stress in Plants: From Biomolecules to Ecosystems, eds. Prasad, M. & Hagemeyer, J.. Berlin, Heidelberg, New York: Springer Verlag, pp. 273–303.
Whitelaw, M. A., Harden, T. J. & Helyar, K. R. (1999). Phosphate solubilization in solution culture by the soil fungus Penicillium radicum. Soil Biology and Biochemistry, 31, 655–65.
Wu, L. H., Luo, Y. M., Xing, X. R. & Christie, P. (2004). EDTA-enhanced phytoremediation of heavy metal contaminated soil with Indian mustard and associated potential leaching risk. Agriculture, Ecosystems and Environment, 102, 307–18.
Zhang, P. C., Ryan, J. A. & Bryndzia, L. T. (1997). Pyromorphite formation from goethite adsorbed lead. Environmental Science and Technology, 31, 2673–8.