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Untapped potential: exploiting fungi in bioremediation of hazardous chemicals

Key Points

  • Fungi possess the biochemical and ecological capacity to degrade environmental organic chemicals and to decrease the risk associated with metals, metalloids and radionuclides, either by chemical modification or by influencing chemical bioavailability. However, to date, bioremediation has tended to disregard the ecological demands and ecophysiological strengths of fungi.

  • Unlike bacteria, fungi do not require continuous water phases for active dispersal. Their hyphae grow across air–water interfaces, bridge air-filled soil pores and grow into soil pores. Fungal mycelia also facilitate the movement of extra-hyphal bacteria, transport nutrients between spatially separated source and sink regions and transport hydrophobic organic contaminants.

  • Fungi co-metabolize many environmental chemicals and thus do not depend on the utilization of such compounds as carbon and energy sources. Pollutant-degrading fungal enzymes include several extracellular oxidoreductases primarily designed to decompose lignocellulose, as well as cell-bound enzymes, allowing fungi to act on a wide range of pollutants.

  • Fungal interactions with metals, metalloids and radionuclides include mobilization and immobilization in the mycosphere, sorption to cell walls and uptake into fungal cells. After being incorporated, such compounds can be chemically transformed, stored in different parts of the cell or translocated along fungal hyphae.

  • The use of filamentous fungi may be advantageous in cases for which translocation of essential factors (nutrients, water, the pollutant itself, and so on) is required for the transformation or detoxification of environmental chemicals.

  • Fungal degradation should be considered for those classes of pollutant that are inefficiently degraded by bacteria, including 'classical' pollutants such as dioxins and 2,4,6-trinitrotoluene, as well as human and veterinary drugs or endocrine-disrupting chemicals found in environmental matrices (water, aquatic sediments and soil).

  • Fungi are suitable for the treatment of organic or metal contaminants in surface soils, the treatment of concentrated or trace organic contaminants in water streams, the removal of metals from water streams, the removal of volatile organic chemicals from air streams, and the removal of organic pollutants using isolated extracellular enzymes instead of whole fungal organisms.

  • There is a trend towards energy- and cost-efficient passive remediation schemes, referred to as monitored natural attenuation, for the reclamation of contaminated land. The low degree of mechanical intervention in natural attenuation of soil probably favours the establishment of filamentous fungi.

Abstract

Fungi possess the biochemical and ecological capacity to degrade environmental organic chemicals and to decrease the risk associated with metals, metalloids and radionuclides, either by chemical modification or by influencing chemical bioavailability. Furthermore, the ability of these fungi to form extended mycelial networks, the low specificity of their catabolic enzymes and their independence from using pollutants as a growth substrate make these fungi well suited for bioremediation processes. However, despite dominating the living biomass in soil and being abundant in aqueous systems, fungi have not been exploited for the bioremediation of such environments. In this Review, we describe the metabolic and ecological features that make fungi suited for use in bioremediation and waste treatment processes, and discuss their potential for applications on the basis of these strengths.

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Figure 1: Typical habitats of terrestrial and aquatic fungi, and some of their ecological features.
Figure 2: Major organic chemicals degraded by various fungal phyla and subphyla.
Figure 3: Principal methods used by fungi to degrade organic chemicals.
Figure 4: Fungal interactions with recalcitrant organic contaminants and metals.

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Acknowledgements

The authors acknowledge support of the Helmholtz Centre For Environmental Research – UFZ (Leipzig, Germany) Research Topic Chemicals in the Environment (CITE).

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Supplementary information S1 (table)

Major classes of enzymes involved in the fungal catabolism of organic pollutants (extended version of TABLE 1) (PDF 478 kb)

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FURTHER INFORMATION

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The fungal kingdom: diverse and essential roles in Earth's ecosystem

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Glossary

Saprobe

A heterotrophic organism that feeds on dead or decaying organic material.

Water activity

A measure of the water (in a substrate) that is available for microbial growth, expressed as the decimal fraction of the amount of water present when the substrate is in equilibrium with a saturated atmosphere.

Matric potential

The force (measured in units of negative pressure) that the soil exerts on water owing to capillary and adsorptive forces.

Hydrophobin

One of a class of small, cysteine-rich proteins that are secreted by filamentous fungi and that self-assemble at hydrophilic–hydrophobic interfaces into an amphipathic membrane.

Exoenzyme

An enzyme that is secreted by a cell and that is usually used for breaking up large molecules that would otherwise be unable to enter the cell.

Photosynthate

A chemical (and its biogenic derivatives) that is produced by photosynthesis.

Meiosporic ascomycete

A member of the phylum Ascomycota that undergoes sexual reproduction, in which haploid meiospores produced by meiosis serve as propagules.

Mitosporic ascomycete

A member of the phylum Ascomycota that can exist in an asexual reproductive state (anamorph), using diploid mitospores produced by mitosis as propagules, or a sexual reproductive state (teleomorph).

Agaric basidiomycete

A basidiomycete of the order Agaricales, having a stem with an umbrella-like cap containing lamellae (gills) on the underside; commonly called a mushroom.

Axenic culture

A culture in which an organism grows alone, with no other organisms (hosts, symbionts or parasites) present.

One-electron abstraction

Oxidation of a compound (the electron-donating substrate) through the removal of one electron, which is then transferred to an electron acceptor.

Abiotic oxidative coupling

Spontaneous chemical oxidation of an organic compound (for example, by air oxygen or by oxidized forms of transition metals such as manganese and iron), leading to the formation of oligomeric or polymeric coupling products.

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Harms, H., Schlosser, D. & Wick, L. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9, 177–192 (2011). https://doi.org/10.1038/nrmicro2519

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