Genetic clues on the evolution of anaerobic catabolism of aromatic compounds

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Abstract
In contrast to the aerobic catabolism of aromatic compounds for which so much information is available, only very little is known about the genes involved in the anaerobic catabolism of aromatics in bacteria. The genes of the central pathway responsible for the anaerobic catabolism of benzoate have been only described in the denitrifying β-Proteobacteria Azoarcus evansii and Thauera aromatica (Breese et al., 1998; Harwood et al., 1999) and in the photosynthetic α-proteobacterium Rhodopseudomonas palustris (Egland et al., 1997; Harwood et al., 1999), and they are organized in catabolic clusters. In all three bacteria, the anaerobic degradation of benzoate begins with its activation to benzoyl-CoA by a benzoate–CoA ligase. However, the subsequent ring reduction to a non-aromatic compound, which is carried out by a four-subunit benzoyl-CoA reductase, and the β-oxidation system that transforms the de-aromatized intermediate by the action of a hydratase, dehydrogenase and ring-cleavage hydrolase, differ between a denitrifying bacterium, T. aromatica, and the photosynthetic bacterium R. palustris. Thus, whereas the T. aromatica pathway converts benzoyl-CoA to 3-hydroxypimelyl-CoA in just four enzymic steps, seven steps are needed through the R. palustris pathway (Harwood et al., 1999; Gibson & Harwood, 2002). The benzoate pathway of A. evansii appears to be similar to that of T. aromatica (Ebenau-Jehle et al., 2003; Harwood et al., 1999). At this point, some questions arise. Is the Thauera-type pathway and the Rhodopseudomonas-type pathway a landmark of anaerobic benzoate catabolism in bacteria with denitrifying and photosynthetic metabolism, respectively? Or, on the contrary, is there a relationship between the type of benzoate degradation pathway and the phylogenetic mark of the organism? To provide some clues as to the answers to the above questions, we decided to expand our knowledge on the genetic determinants responsible for the anaerobic degradation of benzoate in bacteria. We performed an in silico search on the (un)finished microbial genome database at NCBI (http://www.ncbi.nlm.nih.gov/blast/) for genes homologous to those responsible for benzoyl-CoA catabolism in Thauera (Breese et al., 1998), Azoarcus (Schühle et al., 2003) and Rhodopseudomonas (Egland et al., 1997) strains. The only significant match was found with the unfinished genome sequence of Magnetospirillum magnetotacticum MS-1T, which was a surprising finding since this denitrifying strain has not been reported to degrade aromatic compounds (Blakemore et al., 1979). The whole set of genes encoding the putative benzoyl-CoA reductase (bcrCBAD), ferredoxin (fdx), hydratase (dch), dehydrogenase (had), ring-cleavage hydrolase (oah), ferredoxin-reducing enzyme (korAB) and benzoate–CoA ligase (bclA) proteins (Breese et al., 1998; Dörner & Boll, 2003; Schühle et al., 2003) were found in the genome of M. magnetotacticum MS-1T (Fig. 1a⇓). It is worth noting that korAB and oah–had are located at the ends of two different contigs in the current genome sequence of M. magnetotacticum and, therefore, it could be possible that such genes are, as in T. aromatica, adjacent to the dch and bcr genes once the complete genome sequence becomes assembled. Interestingly, although the gene encoding the benzoate–CoA ligase is not physically associated with the rest of the genes of the cluster in T. aromatica and M. magnetotacticum, this gene is located within the cluster in R. palustris and A. evansiiThis work was supported by Grants 07M/0076/2002 and 07M/0127/2000 from the Comunidad Autónoma de Madrid and by Grants BIO2000-1076, BIO2003-01482 and VEM2003-20075-C02-02 from the Comisión Interministerial de Ciencia y Tecnología. M. J. L. B. is a recipient of a predoctoral fellowship from the Plan Nacional de Formación de Personal Investigador-MCYT, and M. C. is a holder of the Ramón y Cajal Program of the Spanish Ministerio de Ciencia y TecnologíaPeer Reviewe

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