Anaerobic Catabolism of Aromatic Compounds: a Genetic and Genomic View

Abstract

SUMMARY Aromatic compounds belong to one of the most widely distributed classes of organic compounds in nature, and a significant number of xenobiotics belong to this family of compounds. Since many habitats containing large amounts of aromatic compounds are often anoxic, the anaerobic catabolism of aromatic compounds by microorganisms becomes crucial in biogeochemical cycles and in the sustainable development of the biosphere. The mineralization of aromatic compounds by facultative or obligate anaerobic bacteria can be coupled to anaerobic respiration with a variety of electron acceptors as well as to fermentation and anoxygenic photosynthesis. Since the redox potential of the electron-accepting system dictates the degradative strategy, there is wide biochemical diversity among anaerobic aromatic degraders. However, the genetic determinants of all these processes and the mechanisms involved in their regulation are much less studied. This review focuses on the recent findings that standard molecular biology approaches together with new high-throughput technologies (e.g., genome sequencing, transcriptomics, proteomics, and metagenomics) have provided regarding the genetics, regulation, ecophysiology, and evolution of anaerobic aromatic degradation pathways. These studies revealed that the anaerobic catabolism of aromatic compounds is more diverse and widespread than previously thought, and the complex metabolic and stress programs associated with the use of aromatic compounds under anaerobic conditions are starting to be unraveled. Anaerobic biotransformation processes based on unprecedented enzymes and pathways with novel metabolic capabilities, as well as the design of novel regulatory circuits and catabolic networks of great biotechnological potential in synthetic biology, are now feasible to approach.

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

“…Many of the genes associated with benzoate metabolism are localized within two gene clusters, whereas genes associated with phenol metabolism are found in a third cluster (Figure 4). This gene organization resembles those previously described in bacteria (Carmona et al, 2009). Since F. placidus is the only hyperthermophilic archaeon known to degrade aromatic compounds, it was of interest to study these pathways in more detail.…”

“…Duplicate Azoarcus evansii and A. aromaticum, one associated with aerobic metabolism and another with anaerobic metabolism of benzoate (Gescher et al, 2002;Rabus et al, 2005;Carmona et al, 2009). However, F. placidus is a strict anaerobe (Hafenbradl et al, 1996), and no genes for aerobic metabolism of benzoate via hydroxylation or the BOX pathway (Zaar et al, 2001;Gescher et al, 2002;Risso et al, 2009) were apparent in the genome.…”

“…Two slightly different versions of these reactions have been described (Figure 2): the BadK-BadH-BadI pathway found in the phototroph R. palustris Gibson and Harwood, 2002) and the Dch-Had-Oah pathway (Breese et al, 1998) found in all other benzoate-degrading organisms studied to date (Carmona et al, 2009). The ultimate fate of this C 7 -dicarboxyl-CoA compound is to be converted into acetyl-CoA by b-oxidation, either to be fully oxidized to CO 2 by the tricyclic acids cycle or to be used in anabolic reactions.…”

“…The metabolism of benzoate has been studied intensively in members of mesophilic Bacteria Gibson and Harwood, 2002;Boll, 2005;Carmona et al, 2009). In all anaerobic benzoate-degrading bacteria that have been studied to date, the enzyme benzoate-CoA (coenzyme A) ligase (BCL) first catalyzes the conversion of benzoate to benzoyl-CoA.…”

“…The anaerobic degradation of aromatic compounds other than benzoate requires a series of reactions that convert them into the central metabolite of the pathway, benzoyl-CoA Carmona et al, 2009). In the case of phenol, two different pathways have been proposed (Figure 3).…”