Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway

Aromatic compounds are important growth substrates for microorganisms. They form a large group of diverse compounds including lignin monomers, amino a cids, quinones, and flavonoids. Aerobic aromatic metabolism is characterize d by the extensive use of molecular oxygen which is essential for the hydro xylation and cleavage of aromatic ring structures. The anaerobic metabolism of low molecular mass soluble aromatic compounds requires, of necessity, a quite different strategy. In most known cases, aromaticity is broken by re duction and the ring is subsequently opened hydrolytically. A small number of different central aromatic intermediates can be reduced, the most common of which is benzoyl-CoA, a compound that is formed as a central intermedia te in the degradation of a large number of aromatic growth substrates. This review concentrates on the anaerobic aromatic metabolism via the benzoyl-C oA pathway. The peripheral pathways that transform growth substrates to ben zoyl-CoA include various types of novel reactions, for example carboxylatio n of phenolic compounds, reductive elimination of ring substituents like hy droxyl or amino groups, oxidation of methyl substituents, O-demethylation r eactions and shortening of aliphatic side chains. The central benzoyl-CoA p athway differs in several aspects in the denitrifying, phototrophic and fer menting bacteria studied. In denitrifying and phototrophic bacteria it star ts with the two-electron reduction of benzoyl-CoA to a cyclic dienoyl-CoA d riven by the hydrolysis of two molecules of ATP to ADP+P-i. This ring reduc tion is catalyzed by benzoyl-CoA reductase and requires a low-potential fer redoxin as an electron donor. In Rhodopseudomonas palustris the cyclic dien e is further reduced to cyclohex-1-ene-1-carboxyl-CoA. In the denitrifying species Thauera aromatica, the cyclic diene is hydrated to give 6-hydroxycy clohex-1-ene-1-carboxyl-CoA. Subsequent beta-oxidation results in the forma tion of a cyclic beta-oxo compound, followed by hydrolytic carbon ring open ing yielding 3-hydroxypimelyl-CoA in the case of T. aromatica and pimelyl-C oA in the case of R. palustris. These intermediates are further beta-oxidiz ed via glutaryl-CoA; final products are 3 acetyl-CoA and 1 CO2. In fermenti ng bacteria benzoyl-CoA may possibly be reduced to the level of cyclohex-1- ene-1-carboxyl-CoA in an ATP-independent reaction. The genes coding for the enzymes of the central benzoyl-CoA pathway have been cloned and sequenced from R. palustris, T. aromatica, and Azoarcus evansii. Sequence analyses of the genes support the concept that phototrophic and denitrifying bacteria use two slightly different pathways to metabolize benzoyl-CoA. The gene seq uences have in some cases been very helpful for the identification of possi ble catalytic mechanisms that were not obvious from initial characterizatio ns of purified enzymes. (C) 1999 Federation of European Microbiological Soc ieties. Published by Elsevier Science B.V. All rights reserved.