Ectomycoremediation of Heavy Metals

The contamination of soils with the nonradioactive metals arsenic (As), cadmium (Cd), copper (Cu), mercury (Hg), lead (Pb), and zinc (Zn) and the radioactive metals strontium (Sr), caesium (Cs), and uranium (U) represents a major environmental and human health problem (Raskin et al. 1997).

Suitable plant species for the phytoremediation of these sites should be able to extract and to tolerate high heavy metal concentrations and should accumulate these metals mainly in their shoot (phytoextraction). However, plants often accumulate heavy metals in their root system to protect the shoot from toxic heavy metal concentrations (Bucking and Heyser 1994). This is the reason why in the past, studies on the phytoremediation of heavy metal-contaminated soils were mainly conducted with hyperaccumulating plants, such as Thlaspi caerulescens, which are able to tolerate and to concentrate high heavy metal concentrations in the shoot (Robinson et al. 1998). However, the small biomass development of these species significantly reduces their potential to extract significant amounts of heavy metals from contaminated soils. Fast growing trees, such as Populus and Salix, could potentially be used for the phytoremediation of these sites, because (1) both are known to naturally colonize areas with high metal soil concentrations such as active and inactive smelter sites (Cripps 2003), (2) they are genetically transformable (Doty 2008), and (3) the high biomass development can compensate for the moderate heavy metal concentrations in the shoot (Pulford and Watson 2003; Tlustos et al. 2006).

Depending on the conditions, the utilization of mycorrhizal systems can assist the phytoremediation of heavy metal polluted soils by the positive effect of ECM fungi on plant tolerance, but could also limit the plants ability to extract heavy metals from the soil by reducing the uptake and the transfer into the shoot. The colonization of tree species with ECM fungi is often essential for the reforestation of old mine sites, because ECM fungi are able to ameliorate the toxicity of heavy metals (Marx 1975). On the other hand, ECM fungi have been shown to enhance the uptake of metals by plants particularly when the exogenous supply is low (Colpaert and Van Assche 1992), but can also reduce the uptake into the plant and the transport into the shoot when the external supply is high (Buucking and Heyser 1994; Krznaric et al. 2009). Several mechanisms have been described to be involved in the reduced heavy metal uptake of ECM plants (1) the larger cell wall surface that can bind heavy metals, (2) the filter function of the fungal sheath that restricts the apoplastic movement of heavy metals into the root cortex, (3) the extracellular precipitation of heavy metals, and (4) the intracellular chelation and compartmentation with, e.g., polyphosphates in the fungal vacuole (Hartley et al. 1997).

Whether ECM fungi are able to contribute to the phytoextraction of heavy metals from the soil despite their widely accepted effect on plant tolerance and uptake depends on the heavy metal, and the fungal and plant species involved. For instance, Sell et al. (2005) showed that by the ECM colonization with Paxillus involutus, the capability of Populus canadensis to extract Cd was increased, but that the same fungus had no effect on the Cd uptake by Salix viminalis. The effect of P. involutus on metal uptake and distribution in Salix varied depending on the fungal strain and its adaptation to heavy metals (Baum et al. 2006). However, the twofold increase in the capability of mycorrhizal Populus to extract Cd from the soil would substantially increase the potential of the plant to remove this metal from polluted soils (Sell et al. 2005).

Zimmer et al. (2009) showed that an ECM fungus can simultaneously increase the heavy metal tolerance of the plant and the accumulation of heavy metals in the plant biomass. An ECM colonization of Salix viminalis x caprea with Hebeloma crustuliniforme resulted in an increase in the plant biomass under metal stress, and increased the Cd and Zn accumulation in the stems. Interestingly, a dual inoculation of the root system with the bacterial strains Micrococcus luteus and Sphingomonas sp. 23L can further increase the effect of the ECM fungus on heavy metal accumulation (Zimmer et al. 2009). The increase by a factor of 4.7 and 3.4 for the Cd and Zn accumulation in the stem, respectively, suggests that a combination of ECM fungi and associated bacteria may represent a promising approach to increase the capability of plants to extract heavy metals from the soil. The bacteria could facilitate the ECM colonization (mycorrhiza helper bacteria) or could increase the bioavailability of heavy metals for the mycorrhizal plant.

Two thousand fungal strains belonging to 98 genera of fungi have been isolated from the Chernobyl Atomic Energy Station after its nuclear accident in 1986. Some isolates showed a growth promotion when exposed to ionizing radiation, and the hyphal growth was directed towards the radiation source (Zhdanova et al. 2004). By contrast, control isolates were inhibited or showed no response when exposed to ionizing radiation (Tugay et al. 2006). Particularly ECM basidiomycetes accumulate or hyperaccumulate radionuclides in their fruitbodies, and a directed growth would allow them to absorb radionuclides from radioactive hotspots in the soil. Fruitbodies are mainly formed when the fungus is in symbiosis with its host plant and could be collected from the site to extract radionuclides from the soil. However, the potential consumption of these fruitbodies by animals or humans also poses a substantial risk and could transfer these radionuclides into the food chain (Gray 1998).

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