Interactions of heavy metals with white-rot fungi
Introduction
White-rot fungi are characterized by their unique ability to degrade lignin. In addition to lignin degradation, white-rot fungi are also able to degrade a variety of structurally similar organic compounds. Various aspects of physiology, ecology and the biotechnological uses of these fungi have been studied. However, until now, there is only scattered information about the physiological effects of heavy metals on white-rot fungi. Only in recent years have the first studies concerning heavy metals effects on biotechnological processes performed by white-rot fungi appeared in literature.
Some heavy metals are essential for the fungal metabolism, whereas others have no known biological role. Both essential and nonessential heavy metals are toxic for fungi, when present in excess. Whereas fungi have metabolic requirements for trace metals, the same metals are often toxic at concentrations only a few times greater than those required [1]. The metals necessary for fungal growth include copper, iron, manganese, molybdenum, zinc, and nickel. Nonessential metals commonly encountered include chromium, cadmium, lead, mercury and silver [2]. The involvement of metal ions in the physiology of another group of wood-rotting fungi, the brown-rot fungi has currently been reviewed [3]. Metal ions are involved in the decomposition of cellulose and hemicelluloses by brown-rot fungi. In white-rot fungi, copper and manganese directly participate in the process of lignin degradation. Manganese participates in the reaction cycle of Mn-dependent peroxidase, and copper serves as a cofactor in the catalytic center of laccase. The role of Mn in lignin degradation has been the subject of numerous studies. In this review, attention will be paid mainly to the toxic heavy metals, that include all the nonessential metals and copper. In contrast with other essential metals, copper is toxic to most fungi even at very low concentrations.
The fungi must be able to sequester essential trace metal ions from various sources, where the metals can be present in concentrations ranging from trace to toxic levels. The concentration of heavy metal ions in their main source, wood, is usually low. In beech (Fagus sylvatica), Cd and Pb concentrations are usually below 1 ppm, Zn concentration can reach tens of parts per million. This is 10–100 times less than in soils at corresponding sites [4]. White-rot fungi have to cope with toxic levels of metal ions often during their growth in soil. The concentration and availability of heavy metal ions in soil are generally higher than in wood, and the concentration can be greatly elevated as a result of industrial pollution on specific sites. Near motorways, gaswork sites, incineration plants and other industrial facilities, soil contamination with heavy metal ions is often accompanied by the presence of high levels of polycyclic aromatic hydrocarbons (PAHs) [5]. The in situ degradation of organic pollutants in such places by white-rot fungi poses a specific problem [6], because the fungal growth can be inhibited by some heavy metal ions. Fungal decomposition of wood treated with different metal-based preservatives is also problematic. Last, but not least, the fruit bodies of white-rot fungi receive significant amounts of heavy metals from the atmosphere.
Section snippets
Uptake of heavy metals
Heavy metals present in the environment can directly interact with extracellular enzymes of fungi. However, to cause a physiological response, heavy metals must be taken up by the fungus. The uptake from liquid environment is the most simple situation, not only under laboratory conditions, but also in the case of water-containing substrates. White-rot fungi can concentrate metals taken up from substrate in their mycelia. Pleurotus ostreatus was able to accumulate 20 mg g−1 dry weight Cd from
Growth and metabolic activity
After heavy metals enter the fungal cell, they affect both individual reactions and complex metabolic processes. Growth is the most popular complex phenomenon, that was studied from the viewpoint of heavy metals toxicity. Cd and Hg are in general the most toxic metals for all white-rot fungi. In S. commune, addition of only 0.1–0.2 mM Cd led to severe growth inhibition [22], addition of 0.05–0.25 mM mercury to growing cultures of Phanerochaete chrysosporium led to decrease of growth rate and in
Ecology of metal–fungus interactions
It is clear, that the interference of heavy metals with physiological, enzymatic and reproductive processes of white-rot fungi has its ecological consequences. The limitations in growth or reproduction in the presence of metals leads to the changes of community structure and the effects of heavy metals on enzymatic activities influences the energy flux in the ecosystem.
It is therefore not surprising, that different species of white-rot fungi differ in the degree of their heavy metal tolerance.
Use of metals in antifungal compounds
The fact that heavy metals are toxic to fungi has been widely used in the fight against fungal deterioration of materials including timber. Due to its high toxicity, the early preparations of biocides were based mostly on mercury. However, the toxicity of mercury to living organisms was also the case for ending the use of mercuric antifungals. The much less environmentally problematic copper was also found to exhibit good biocidal activity [115], but the major requirement of any formulation of
Effects of metals on fungal biodegradation processes
From biotechnological viewpoint, the occurrence of heavy metals poses a serious problem for the use of white-rot fungi to degrade persistent organic compounds including, e.g. synthetic textile dyes, PAHs or pesticides. Effluents from textile dyeing facilities contain metals used in dyes production technologies or in the molecule of textile dyes. Soil containing persistent organic compounds to be degraded by fungi is often contaminated by toxic levels of heavy metals.
Since the effect of heavy
Biosorption of heavy metals from solutions
The use of microbial biomass for the biosorption of metals from industrial and municipal waste water has been proposed as a promising alternative to conventional heavy metal management strategies. Although the mechanism of metal sorption and uptake by microorganisms is still not completely understood, the sorption to polysaccharides, proteins or other molecules occurring in the outer layer of the cell wall probably plays the most important role. Experiments with chemically modified cell walls
Conclusions
The interactions of white-rot fungi and toxic heavy metals have several physiological, ecological and technological consequences. The essential metals are necessary for fungal growth and development, but they are toxic when present in excess. The presence of heavy metals in the environment of fungi can lead to the changes in the structure and function of microbial communities in decaying wood or affect the decomposition process and nutrients turnover in soil. These processes as well as the
Acknowledgements
This work was supported by the Grant Agency of the Czech Republic (204/02/P100), by the Grant Agency of the Czech Academy of Sciences (B5020202) and by the Institutional Research Concept no. AV0Z5020903 of the Institute of Microbiology, ASCR.
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