Anaerobic bacterial metabolism of hydrocarbons

Abstract

The capacity of some bacteria to metabolize hydrocarbons in the absence of molecular oxygen was first recognized only about ten years ago. Since then, the number of hydrocarbon compounds shown to be catabolized anaerobically by pure bacterial cultures has been steadily increasing. This review summarises the current knowledge of the bacterial isolates capable of anaerobic mineralization of hydrocarbons, and of the biochemistry and molecular biology of enzymes involved in the catabolic pathways of some of these substrates. Several alkylbenzenes, alkanes or alkenes are anaerobically utilized as substrates by several species of denitrifying, ferric iron‐reducing and sulfate‐reducing bacteria. Another group of anaerobic hydrocarbon degrading bacteria are ‘proton reducers’ that depend on syntrophic associations with methanogens. For two alkylbenzenes, toluene and ethylbenzene, details of the biochemical pathways involved in anaerobic mineralization are known. These hydrocarbons are initially attacked by novel, formerly unknown reactions and oxidized further to benzoyl‐CoA, a common intermediate in anaerobic catabolism of many aromatic compounds. Toluene degradation is initiated by an unusual addition reaction of the toluene methyl group to the double bond of fumarate to form benzylsuccinate. The enzyme catalyzing this first step has been characterized at both the biochemical and molecular level. It is a unique type of glycyl‐radical enzyme, an enzyme family previously represented only by pyruvate‐formate lyases and anaerobic ribonucleotide reductases. Based on the nature of benzylsuccinate synthase as a radical enzyme, a hypothetical reaction mechanism for the addition of toluene to fumarate is proposed. The further catabolism of benzylsuccinate to benzoyl‐CoA and succinyl‐CoA appears to occur via reactions of a modified β‐oxidation pathway. Ethylbenzene is first oxidized at the methylene carbon to 1‐phenylethanol and subsequently to acetophenone, which is then carboxylated to 3‐oxophenylpropionate and converted to benzoyl‐CoA and acetyl‐CoA. Anaerobic mineralization of alkanes involves an oxygen‐independent oxidation to fatty acids, followed by β‐oxidation. In one strain of an alkane‐mineralizing sulfate‐reducing bacterium, the activation appears to proceed via a chain‐elongation, possibly by addition of a C1‐group at the terminal methyl group of the alkane. Finally, aspects concerned with the regulation and ecological significance of anaerobic hydrocarbon catabolic pathways are discussed.

Anaerobic toluene-catabolic pathway in denitrifying Thauera aromatica: activation and β-oxidation of the first intermediate, (R)-(+)-benzylsuccinate

“…Stereospecific formation of (R)-(j)-benzylsuccinate was also recently reported in a different toluene-degrading denitrifying bacterium (Beller & Spormann, 1998). Thus, the reaction of benzylsuccinate synthase proceeds highly stereospecifically, despite the probable involvement of radical intermediates in the reaction mechanism (Heider et al, 1999). The enantiomer specificity of the CoA-transferase catalysing the activation of benzylsuccinate to benzylsuccinyl-CoA was assayed by HPLC analysis.…”

“…Organisms capable of anaerobic hydrocarbon mineralization and available in pure culture include denitrifying, ferric iron-and sulfate-reducing bacteria. The metabolic pathways involved in the catabolism of some hydrocarbons in the absence of oxygen are currently being investigated (for a review see Heider et al, 1999). The simplest alkylbenzene, toluene, appears to be one of the most readily degradable hydrocarbons under anaerobic conditions : it is preferentially catabolized from crude oil in anaerobic enrichment cultures (Rabus et al, 1996(Rabus et al, , 1999.…”

Anaerobic utilization of toluene by marine alpha- and gammaproteobacteria reducing nitrate

“…Austin et al, 1977;Gibson & Subramanian, 1984;Teramoto et al, 2009). Even though hydrocarbons are among the least chemically reactive molecules, microbial-mediated degradation has also been demonstrated under anoxic conditions and several anaerobic phototrophic, nitrate-, iron-, sulphatereducing and fermenting bacteria have been isolated or enriched in recent decades (Heider et al, 1998;Widdel et al, 2010). The activity of sulphate-reducing bacteria in oil reservoirs and in onshore and offshore oil operation has been of great interest from an industrial perspective, as detrimental souring (production of sulphide) has been associated with this group of bacteria.…”

Plant litter and soil type drive abundance, activity and community structure of alkB harbouring microbes in different soil compartments

“…Although the chemically inert alkanes are activated by the addition of fumarate (Heider et al, 1999;Widdel and Rabus, 2001;Wilkes et al, 2003) during anoxia, aerobic activation is accomplished by the terminal (Sepic et al, 1995;Koma et al, 2001;Van Hamme et al, 2003) or subterminal (Whyte et al, 1998;Kotani et al, 2006Kotani et al, , 2007 introduction of oxygen. For alkanes with a chain length oC 30 , which can be considered as typical for plant waxes, terminal oxygen introduction is mainly catalysed by the membrane bound, rubredoxin-dependent di-iron alkane monooxygenase (AlkB), which is found among Actinobacteria, a-, b-and g-Proteobacteria (van Beilen et al, 2003;van Beilen and Funhoff, 2007).…”