Effects of Heavy Metals on Fungal Physiology

Metals exert toxic effects in many ways: they can (1) inhibit enzymes by the interactions with proteins; (2) displace or substitute for essential metal ions; (3) cause disruption of membranes, and; (4) cause oxidative stress or interact with systems that normally protect against the harmful effects of free radicals.

Growth reduction is a typical response of fungi to the toxicity of heavy metals (Baldrian 2003). It has been demonstrated that this reduction is dependent on nutrient availability, and that higher nutrient content can alleviate metal toxicity (Gadd et al. 2001). The growth of cord-forming saprotrophic basidiomycetes in the soil environment represents the colonization of nutrient-poor space in the search for nutrients. This growth is supported from the colonized bulky substrate, e.g., wood pieces or litter patches. This type of colonization of nutrient-limited soil regions was significantly reduced for Pleurotus ostreatus in the presence of Cd or Hg (Baldrian et al. 2000), and Pb exhibited the same effect on several litter-decomposing fungi (Tuomela et al. 2005; Kahkonen et al. 2008).

The morphological changes induced by heavy metals are common among all groups of fungi (Baldrian 2003). Changes in mycelial morphology were observed in Mucor rouxii in the presence of a high copper concentration (Gardea-Torresdey et al. 1997). In the ectomycorrhizal fungus P. involutus, the addition of Cd led to an increase in hyphal density caused by increasing numbers of laterals per branch point and a decrease in the distance between branch points (Darlington and Rauser 1988). Furthermore, the morphologies of whole fungal colonies are affected by heavy metals. This is the case for Trichoderma viride and Rhizopus arrhizus, which show biomass redistribution within colonies (Gadd et al. 2001).

Metal-contaminated soils usually contain a spatially heterogeneous distribution of metal concentrations and available nutritional resources, and the morphology of whole fungal colonies can reflect this heterogeneity. During the growth of fungi in metal-containing agar tiles, a wide range of morphological changes and growth responses occurred (Fomina et al. 2000, 2003). In the gap between metal-free and metal-containing tiles, the presence of copper or cadmium led to negative chemot-ropism in Geotrichum candidum, Clonostachys rosea, Humicola grisea, and Trichoderma virens, as well as the cessation of growth, swelling, or lysis of some hyphal tips.

In addition to growth reduction, there are detectable markers of metal toxicity in fungi. In the ectomycorrhizal fungus Paxillus involutus, Zn induced changes in vacuolar motility and tubularity, caused reversible mitochondrial fragmentation (Tuszynska et al. 2006), and interfered with the biosynthesis of polyamines (Zarb and Walters 1995). In fruitbodies of Boletus edulis collected in soils with a gradient of Cd, Zn, Cu, and Hg contamination, the extent of DNA and lipid damage was related to the metal concentration as a result of metal-induced oxidative stress (Collin-Hansen et al. 2005a).

Heavy metals in general are potent inhibitors of enzymatic reactions. Mercury exerts its toxic effect mainly by binding to sulfhydryl groups present in the active or regulatory sites of enzymes, thereby causing irreversible inactivation. Copper and cadmium - in addition to binding to aromatic amino acid residues in enzyme molecules - can also cause oxidative damage to proteins through the induction of oxidative stress associated with the production of reactive oxygen species such as hydroxyl or superoxide radicals (Baldrian 2003). In Paxillus involutus, cadmium stress leads to the expression of superoxide dismutase, an intracellular enzyme alleviating oxidative stress, and also increases the transcription of laccase, aconitase, and metallothionein (Jacob et al. 2001, 2004). Increased amounts of superoxide dismutase as well as catalase and HSP70 were also found in Boletus edulis fruitbodies exposed to higher concentrations of heavy metals in forest soils in a smelter area (Collin-Hansen et al. 2005b).

In different taxonomic groups of fungi, it was found that heavy metals are harmful to reproduction. In saprotrophic and mycorrhizal soil fungi, the reproductive stages of development (spore formation and germination) are much more sensitive to heavy metals than mycelial growth (Baldrian 2003). The litter-decomposing fungus Agrocybe perfecta failed to produce fruitbodies during growth on straw with 0.05-1 mM Cd or when metal-free straw was overlaid with soil containing 50 ppm of the metal; Pleurotus ostreatus was much less sensitive (Gabriel et al. 1996).

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