Principles of microbial PAH-degradation in soil

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Abstract

Interest in the biodegradation mechanisms and environmental fate of polycyclic aromatic hydrocarbons (PAHs) is motivated by their ubiquitous distribution, their low bioavailability and high persistence in soil, and their potentially deleterious effect on human health. Due to high hydrophobicity and solid–water distribution ratios, PAHs tend to interact with non-aqueous phases and soil organic matter and, as a consequence, become potentially unavailable for microbial degradation since bacteria are known to degrade chemicals only when they are dissolved in water. As the aqueous solubility of PAHs decreases almost logarithmically with increasing molecular mass, high-molecular weight PAHs ranging in size from five to seven rings are of special environmental concern. Whereas several reviews have focussed on metabolic and ecological aspects of PAH degradation, this review discusses the microbial PAH-degradation with special emphasis on both biological and physico-chemical factors influencing the biodegradation of poorly available PAHs.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are unique contaminants in the environment because they are generated continuously by the inadvertently incomplete combustion of organic matter, for instance in forest fires, home heating, traffic, and waste incineration. Massive soil contamination with PAH originated from extensive industrial coal gasification during most of the 20th century. As gas works were typically located in densely populated urban regions to facilitate the distribution of the coal gas, PAH contaminated sites are mostly found in or near cities, thus representing a considerable public health hazard. PAHs are composed of fused, aromatic rings whose biochemical persistence arises from dense clouds of π-electrons on both sides of the ring structures, making them resistant to nucleophilic attack. Besides this, they possess physical properties, such as low aqueous solubility and high solid–water distribution ratios, which stand against their ready microbial utilization and promote their accumulation in the solid phases of the terrestrial environment. As rules of thumb, the aqueous solubility and, as a consequence, the bioavailability of the PAHs decreases almost logarithmically with increasing molecular mass. Of environmental concern are primarily the PAHs ranging in size from naphthalene (two rings, C10H8) to coronene (seven rings, C24H12). This review discusses the microbial degradation of environmentally relevant PAHs with an emphasis on biological strategies to obtain poorly bioavailable, soil-sorbed or non aqueous phase PAHs.

Section snippets

Growth on PAHs as sole carbon sources

Microbial degradation of PAHs and other hydrophobic substrates is believed to be limited by the amounts dissolved in the water phase (Ogram et al., 1985, Rijnaarts et al., 1990, Volkering et al., 1992, Volkering et al., 1993, Harms and Bosma, 1997, Bosma et al., 1997), with sorbed, crystalline, and non-aqueous phase liquid (NAPL)-dissolved PAHs being unavailable to PAH-degrading organisms. Bioavailability is considered a dynamic process, determined by the rate of substrate mass-transfer to

Growth on PAH in soil

The growth curves discussed above are obtained under idealized conditions that are characterized by unlimited bacterial access to the crystals and fast substrate transport by convection and diffusion in a homogeneous, aqueous solution. Heterogeneous media, such as soil, do not have these characteristics. In soil, PAHs are heterogeneously distributed and may be absorbed inside of organic particles, located in small pores that are inaccessible for bacteria, or otherwise occluded by the multitude

PAH-metabolism

Since bacteria initiate PAH degradation by the action of intracellular dioxygenases, the PAHs must be taken up by the cells before degradation can take place. Bacteria most often oxidize PAHs to cis-dihydrodiols by incorporation of both atoms of an oxygen molecule. The cis-dihydrodiols are further oxidized, first to the aromatic dihydroxy compounds (catechols) and then channeled through the ortho- or meta cleavage pathways (Cerniglia, 1984, Smith, 1990).

The biological degradation of PAHs can

Bacterial adaptations that maximize the acquisition of sorbed and separate phase PAHs

In the following, the naturally occurring, rate limiting mass transfer processes will be analysed in terms of the possibilities of biological systems to optimize the PAH transfer.

PAH-degrading bacteria are well-adapted to oligotrophic conditions prevailing in soil

It has been observed that PAH degradation in soil is dominated by bacterial strains belonging to a very limited number of taxonomic groups such as Sphingomonas, Burkholderia, Pseudomonas and Mycobacterium (Kästner et al., 1994, Mueller et al., 1997, Ho et al., 2000, Bastiaens et al., 2000, Johnsen et al., 2002). Among these taxonomic groups a high proportion of the PAH-degrading isolates belong to the sphingomonads sensu lato (Mueller et al., 1997, Ho et al., 2000, Bastiaens et al., 2000,

Bacterial-eukaryotic consortia

It is tempting to take for real that PAH degradation in soil proceeds as in laboratory assays where a pure bacterial culture or defined mixed culture mineralizes a PAH to CO2 and water without much excretion of intermediates or interference of other substrates or other organisms. In a natural setting, however, various co-metabolic side-reactions will act on the PAHs and bring about a multitude of metabolites. These metabolites generally possess higher polarity than the mother compounds and one

Anaerobic PAH-degradation

It has been suggested that biodegradation of PAHs, both eukaryotic and prokaryotic, require the presence of molecular oxygen to initiate the enzymatic attack on the PAH molecules (Cerniglia, 1992). This would have wide implications for PAH-contamination of anaerobic sediments, water-logged soils and aquifers since contamination would practically last forever. Fortunately, there is increasing evidence of anaerobic PAH-degradation with nitrate and sulfate as terminal electron acceptors. It has

Implications for bioaugmentation of contaminated soil with PAH-degrading bacteria

Various studies have investigated the possibility of bioaugmentation of PAH-polluted soils with PAH-degrading consortia or pure strains, and enhanced PAH-degradation in soil slurries and soil-microcosms has indeed often been observed (Grosser et al., 1991, Madsen and Kristensen, 1997, Kästner et al., 1998). However, to our knowledge, enhanced PAH-biodegradation in large scale experiments as a result of inoculation with PAH-degrading lab-strains has never been demonstrated. It may be speculated

Acknowledgements

We are grateful to Ulrich Karlson and Parmely Pritchard for their critical revision of the manuscript, and to all the partners of the BIOVAB/BIOSTIMUL consortia. This work was supported by the European Commission (contracts BIO4-CT97-2015 and QLRT-1999-00326) and the Danish Strategic Environmental Research Program (BIOPRO).

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    1

    Present address: Geological Survey of Denmark and Greenland, Department of Geochemistry, Øster Voldgade 10, København K, 1350, Denmark.

    2

    Present address: UFZ Centre for Environmental Research, Department of Environmental Microbiology, Permoserstraße 15, D-04318 Leipzig, Germany. Tel.: +49-341-235-2225; fax: +49-341-235-2247.

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