Fungal Communities in Hydrocarbon Degradation

Abstract

The present chapter reviews and discusses recent advances in the ecophysiology, phylogeny, and biotechnological applications of fungi with respect to their ability to degrade hydrocarbons. There is a very wide fungal biodiversity with diverse enzymatic mechanisms that transform different hydrocarbon chemical structures, from short chain aliphatics to heavy weight polycyclic aromatics. Alkanes and alkylbenzenes are generally metabolized as the sole source of carbon and energy via specialized metabolic pathways that start with the substrate oxidation through cytochrome P450 monoxygenases. Unsaturated alkenes and alkynes, as well as alicyclics, are more recalcitrant to fungal degradation and are often converted to partly oxidized metabolites. Aromatic hydrocarbons ranging from the single benzene ring to the high-molecular-weight polycyclics are generally degraded via one or more of three independent enzymatic systems. The intracellular P450 monooxygenases that detoxify harmful chemicals are universally present in the microsomes of eukaryotic cells, while lignin-degrading fungi specifically produce extracellular peroxidases and laccases that biodegrade aromatic hydrocarbons. Laccases are not exclusively active in lignin biodegradation: other functions have been reported for these enzymes in nonligninolytic fungi. The low functional specificity and high redox potential of peroxidases and laccases enables the oxidation of a broad range of aromatic hydrocarbons and other recalcitrant contaminants. Such co-incidental biodegradation processes often result in partially degraded compounds that do not support fungal growth and that might be more toxic than the parent substrates.

Relevant hydrocarbonoclastic fungal strains deposited in culture collections have been identified and their phylogenies revised and reassessed when necessary. The capacity to assimilate hydrocarbons in fungi may have evolved in the context of biotrophic interactions in environments that are rich in naturally biosynthesized alkanes and volatile alkylbenzenes. The ability to utilize hydrocarbons seems to correlate with virulence toward humans, as seen in phylogenetically unrelated genera of hydrocarbonoclastic fungi, e.g., Scedosporium (Microascales) and Exophiala-Cladophialophora (Chaetothyriales). Applied research on hydrocarbonoclastic fungi includes studies dedicated to preventing biodeterioration as well as on potential use of the same enzymatic capabilities for bioremediation purposes. Fungal contamination of fuels is a long-standing problem that has acquired new dimensions as new biofuel blends have emerged. Recent improvements in phylogenetic understanding of fungal biodeteriogens may provide enhanced biocontrol opportunities. In work related to restoration of ecosystems, the ability of hydrocarbonoclastic fungi to form extended mycelial networks, in combination with the broad capabilities of their catabolic enzymes, makes these fungi well suited for the bioremediation of hydrocarbon-polluted soils. However, some cases of unsatisfactory biodegradation efficiency in operations conducted at field scale and cases in which toxic intermediates were generated have turned research efforts towards synergistic biodegradation processes mediated by complex microbial populations (i.e., fungal-bacterial mixtures). The assimilatory biodegradation of volatile alkanes and alkylbenzenes by certain fungal species makes them ideal candidates for the biofiltration of air polluted with these compounds. However, the potential correlation between hydrocarbon utilization and capacity for human infection must be taken into account in the design of biofiltration systems in order to prevent unintended production of biohazardous conditions. Ongoing research is focusing on the precise delimitation of genetic mechanisms that underlie these two apparently converging ecological traits.