Anaerobic degradation of non-substituted aromatic hydrocarbons

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Aromatic hydrocarbons are among the most prevalent organic pollutants in the environment. Their removal from contaminated systems is of great concern because of the high toxicity effect on living organisms including humans. Aerobic degradation of aromatic hydrocarbons has been intensively studied and is well understood. However, many aromatics end up in habitats devoid of molecular oxygen. Nevertheless, anaerobic degradation using alternative electron acceptors is much less investigated. Here, we review the recent literature and very early progress in the elucidation of anaerobic degradation of non-substituted monocyclic (i.e. benzene) and polycyclic aromatic hydrocarbons (PAH such as naphthalene and phenanthrene). A focus will be on benzene and naphthalene as model compounds. This review concerns the microbes involved, the biochemistry of the initial activation and subsequent enzyme reactions involved in the pathway.

Highlights

► Anaerobic benzene and naphthalene degradation is performed by microbes belonging to different phyla. ► Metabolite analysis of cultures suggest as initial activation reaction either methylation, hydroxylation, or carboxylation for benzene, and methylation or carboxylation for naphthalene. ► Proteogenomic studies indicate carboxylation of benzene and naphthalene. ► Non-substitute aromatic hydrocarbons are most likely activated by a novel carboxylation reaction.

Introduction

Anaerobic degradation of aromatic hydrocarbons is an important bioremediation process in the environment, where they can stem from not only hydrocarbon spills but also natural production, for example [1]. Owing to the low oxygen solubility in water (8 mg/l = 250 μM at 25 °C) saturated systems such as lake and sea sediments or aquifers turn anoxic upon rather small carbon loads (e.g. 33 μM benzene). Degradation has therefore to proceed in the absence of molecular oxygen which is essential for biochemical activation reactions because reactive oxygen is lacking as a cosubstrate. Molecular oxygen as electron acceptor for respiration can be easily replaced by nitrate, sulphate, etc. For alkylated aromatic hydrocarbons such as toluene, xylene, ethylbenzene, and methylnaphthalene degradation pathways have been well studied and described to the enzyme mechanism level which is summarized in several excellent reviews [2, 3]. However, enzymatic reactions contributing to the degradation of non-substituted aromatic hydrocarbons, are much less understood. They are especially interesting because, so far, there are no biochemical reactions known that could attack these extremely stable aromatic C–C or C–H-bonds in the absence of molecular oxygen [4]. The energy of dissociation of the C–H bond of naphthalene in position 1 or 2 is approximately the same as the first bond dissociation energy for benzene (about 480 kJ mol−1) [5], making such compounds difficult to activate in the absence of molecular oxygen.

Section snippets

Organisms involved in anaerobic benzene degradation

Anaerobic degradation of benzene has been reported for all of the important terminal electron acceptors for anaerobic respiration, that is, nitrate [6, 7•, 8], sulphate [9, 10, 11], ferric iron [12••, 13••], and even fermentation coupled to methanogenesis [14, 15] which agrees with thermodynamic calculations. Two pure cultures belonging to the genera Dechloromonas [7] and Azoarcus [8] have been reported to oxidise benzene with nitrate as electron acceptor. Furthermore, the dominating member in

Anaerobic degradation of non-substituted polycyclic aromatic hydrocarbons

Polycyclic aromatic hydrocarbons are ubiquitous environmental contaminants of natural and anthropogenic origin. Their high hydrophobicity and low bioavailability increase with the molecular masses and contribute to their persistence in the environment. Owing to toxicity properties of several of these compounds, there is a serious concern about their presence in the environment. They can bioaccumulate in food chains leading to ecological and human health risks. A carcinogenic potential due to

Molecular mechanism of benzene and naphthalene activation

So far, there are no enzyme assays or purified proteins available that would allow a detailed mechanistic study of the initial activation reaction of benzene or naphthalene. Nevertheless, hints for the reaction mechanisms stem from stable isotope fractionation studies [64, 65] (Bergmann et al., Unpublished data). The stable isotope fractionation factors for carbon obtained in growth experiments by several laboratories were in the range between a radical mediated C–H bond cleavage and a

Summary

Anaerobic degradation of non-substituted aromatic hydrocarbons such as benzene and naphthalene are widely distributed among several phyla and classes of bacteria. Although the detailed mechanism of the initial activation reactions remains to be clarified the biochemical steps involved slowly approach elucidation. More and more lines of evidence are collected from different culture studies supporting a direct carboxylation of both benzene and naphthalene. The further breakdown proceeds by the

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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