Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene

Abstract

Over the past 30 years, research on the microbial degradation of polycyclic aromatic hydrocarbons (PAHs) has resulted in the isolation of numerous genera of bacteria, fungi and algae capable of degrading low molecular weight PAHs (compounds containing three or less fused benzene rings). High molecular weight PAHs (compounds containing four or more fused benzene rings) are generally recalcitrant to microbial attack, although some fungi and algae are capable of transforming these compounds. Until recently, only a few genera of bacteria have been isolated with the ability to utilise four-ring PAHs as sole carbon and energy sources while cometabolism of five-ring compounds has been reported. The focuss of this review is on the high molecular weight PAH benzo[a]pyrene (BaP). There is concern about the presence of BaP in the environment because of its carcinogenicity, teratogenicity and toxicity. BaP has been observed to accumulate in marine organisms and plants which could indirectly cause human exposure through food consumption. This review provides an outline of the occurrence of BaP in the environment and the ability of bacteria, fungi and algae to degrade the compound, including pathways for BaP degradation by these organisms. In addition, approaches for improving microbial degradation of BaP are discussed.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are one class of toxic environmental pollutants that have accumulated in the environment due to a variety of anthropogenic activities. Since the 1970s, research on the biological degradation of PAHs has demonstrated that bacteria, fungi and algae possess catabolic abilities that may be utilised for the remediation of PAH-contaminated soil and water. Presently, bioremediation has been shown to be effective in remediating soils contaminated with low molecular weight PAHs (Mueller et al., 1991a, Kastner and Mahro, 1996, Banerjee et al., 1995); however, the high molecular weight PAHs are generally recalcitrant to microbial attack (Park et al., 1990, Erickson et al., 1993, Cerniglia, 1992). Although the lack of microbial activity towards high molecular weight PAHs may be attributed to site specific environmental factors, such as bioavailability of the contaminant, nutrients, redox potential, etc., the limiting factor may be the scarcity of micro-organisms capable of degrading the more highly condensed compounds. For bioremediation to be an effective tool for the clean up of PAH-contaminated soils, a greater understanding of the processes involved, and those that limit the degradation of high molecular weight PAHs, is required.

One such high molecular weight PAH is benzo[a]pyrene (BaP), a five-ring compound. BaP has been classified by the US Environmental Protection Agency (USEPA) as a priority pollutant: a compound selected on the basis of its known or suspected carcinogenicity, teratogenicity or acute toxicity. Multiple animal studies in many species have demonstrated the carcinogenicity of BaP following administration by numerous routes. In addition, BaP has been shown to cause genotoxic effects in a broad range of prokaryotic and mammalian cell assays, and as such, its occurrence in the environment is of great concern. The level of BaP in the environment forms the basis for the development of environmental assessment and cleanup regulations throughout the world. Although there is a great diversity of organisms capable of degrading low molecular weight PAH, such as naphthalene, acenaphthene and phenanthrene, relatively few genera have been observed to degrade the high molecular weight PAHs, such as BaP. The subject of this review is the microbial degradation of BaP, factors limiting the compounds degradation and options for its remediation.