Anaerobic metabolism of aromatic compounds

Aromatic compounds comprise a wide variety of low-molecular-mass natural compounds (amino acids, quinones, flavonoids, etc.) and biopolymers (lignin, melanin). They are almost exclusively degraded by microorganisms. Aerobic aromatic metabolism is characterised by the extensive use of molecular oxygen. Monoxygenases and dioxygenases are essential for the hydroxylation and cleavage of aromatic ring structures. Accordingly, the characteristic central intermediates of the aerobic pathways (e.g. catechol) are readily attacked oxidatively. Anaerobic aromatic catabolism requires, of necessity, a quite different strategy. The basic features of this metabolism have emerged from studies on bacteria that degrade soluble aromatic substrates to CO2 in the complete absence of molecular oxygen. Essential to anaerobic aromatic metabolism is the replacement of all the oxygen-dependent steps by an alternative set of novel reactions and the formation of different central intermediates (e.g. benzoyl-CoA) for breaking the aromaticity and cleaving the ring; notably, in anaerobic pathways, the aromatic ring is reduced rather than oxidised. The two-electron reduction of benzoyl-CoA to a cyclic diene requires the cleavage of two molecules of ATP to ADP and P1 and is catalysed by benzoyl-CoA reductase. After nitrogenase, this is the second enzyme known which overcomes the high activation energy required for reduction of a chemically stable bond by coupling electron transfer to the hydrolysis of ATP. The alicyclic product cyclohex-1,5-diene-1-carboxyl-CoA is oxidised to acetyl-CoA via a modified beta-oxidation pathway; the ring structure is opened hydrolytically. Some phenolic compounds are anaerobically transformed to resorcinol (1,3-dihydroxybenzene) or phloroglucinol (1,3,5-trihydroxybenzene). These intermediates are also first reduced and then as alicyclic products oxidised to acetyl-CoA. This review gives an outline of the anaerobic pathways which allow bacteria to utilize aromatics even in the absence of oxygen. We focus on previously unknown reactions and on the enzymes characteristic for such novel metabolism.