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Anaerobic catabolism of aromatic compounds: a genetic and genomic view.

ABSTRACT: 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.

SUBMITTER: Carmona M

PROVIDER: S-EPMC2650882 | biostudies-literature | 2009 Mar

REPOSITORIES: biostudies-literature

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Anaerobic catabolism of aromatic compounds: a genetic and genomic view.

Carmona Manuel M Zamarro María Teresa MT Blázquez Blas B Durante-Rodríguez Gonzalo G Juárez Javier F JF Valderrama J Andrés JA Barragán María J L MJ García José Luis JL Díaz Eduardo E

Microbiology and molecular biology reviews : MMBR 20090301 1

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 anaerobi ...[more]

PMID: 19258534

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Project description:Members of the genus Aromatoleum thrive in diverse habitats and use a broad range of recalcitrant organic molecules coupled to denitrification or O2 respiration. To gain a holistic understanding of the model organism A. aromaticum EbN1T, we studied its catabolic network dynamics in response to 3-(4-hydroxyphenyl)propanoate, phenylalanine, 3-hydroxybenzoate, benzoate, and acetate utilized under nitrate-reducing versus oxic conditions. Integrated multi-omics (transcriptome, proteome, and metabolome) covered most of the catabolic network (199 genes) and allowed for the refining of knowledge of the degradation modules studied. Their substrate-dependent regulation showed differing degrees of specificity, ranging from high with 3-(4-hydroxyphenyl)propanoate to mostly relaxed with benzoate. For benzoate, the transcript and protein formation were essentially constitutive, contrasted by that of anoxia-specific versus oxia-specific metabolite profiles. The matrix factorization of transcriptomic data revealed that the anaerobic modules accounted for most of the variance across the degradation network. The respiration network appeared to be constitutive, both on the transcript and protein levels, except for nitrate reductase (with narGHI expression occurring only under nitrate-reducing conditions). The anoxia/nitrate-dependent transcription of denitrification genes is apparently controlled by three FNR-type regulators as well as by NarXL (all constitutively formed). The resequencing and functional reannotation of the genome fostered a genome-scale metabolic model, which is comprised of 655 enzyme-catalyzed reactions and 731 distinct metabolites. The model predictions for growth rates and biomass yields agreed well with experimental stoichiometric data, except for 3-(4-hydroxyphenyl)propanoate, with which 4-hydroxybenzoate was exported. Taken together, the combination of multi-omics, growth physiology, and a metabolic model advanced our knowledge of an environmentally relevant microorganism that differs significantly from other bacterial model strains. IMPORTANCE Aromatic compounds are abundant constituents not only of natural organic matter but also of bulk industrial chemicals and fuel components of environmental concern. Considering the widespread occurrence of redox gradients in the biosphere, facultative anaerobic degradation specialists can be assumed to play a prominent role in the natural mineralization of organic matter and in bioremediation at contaminated sites. Surprisingly, differential multi-omics profiling of the A. aromaticum EbN1T studied here revealed relaxed regulatory stringency across its four main physiological modi operandi (i.e., O2-independent and O2-dependent degradation reactions versus denitrification and O2 respiration). Combining multi-omics analyses with a genome-scale metabolic model aligned with measured growth performances establishes A. aromaticum EbN1T as a systems-biology model organism and provides unprecedented insights into how this bacterium functions on a holistic level. Moreover, this experimental platform invites future studies on eco-systems and synthetic biology of the environmentally relevant betaproteobacterial Aromatoleum/Azoarcus/Thauera cluster.

Project description:Emergent strategies to valorize lignin, an abundant but underutilized aromatic biopolymer, include tandem processes that integrate chemical depolymerization and biological catalysis. To date, aromatic monomers from C-O bond cleavage of lignin have been converted to bioproducts, but the presence of recalcitrant C-C bonds in lignin limits the product yield. A promising chemocatalytic strategy that overcomes this limitation involves phenol methyl protection and autoxidation. Incorporating this into a tandem process requires microbial cell factories able to transform the p-methoxylated products in the resulting methylated lignin stream. In this study, we assessed the ability of Rhodococcus jostii RHA1 to catabolize the major aromatic products in a methylated lignin stream and elucidated the pathways responsible for this catabolism. RHA1 grew on a methylated pine lignin stream, catabolizing the major aromatic monomers: p-methoxybenzoate (p-MBA), veratrate, and veratraldehyde. Bioinformatic analyses suggested that a cytochrome P450, PbdA, and its cognate reductase, PbdB, are involved in p-MBA catabolism. Gene deletion studies established that both pbdA and pbdB are essential for growth on p-MBA and several derivatives. Furthermore, a deletion mutant of a candidate p-hydroxybenzoate (p-HBA) hydroxylase, ΔpobA, did not grow on p-HBA. Veratraldehyde and veratrate catabolism required both vanillin dehydrogenase (Vdh) and vanillate O-demethylase (VanAB), revealing previously unknown roles of these enzymes. Finally, a ΔpcaL strain grew on neither p-MBA nor veratrate, indicating they are catabolized through the β-ketoadipate pathway. This study expands our understanding of the bacterial catabolism of aromatic compounds and facilitates the development of biocatalysts for lignin valorization.IMPORTANCELignin, an abundant aromatic polymer found in plant biomass, is a promising renewable replacement for fossil fuels as a feedstock for the chemical industry. Strategies for upgrading lignin include processes that couple the catalytic fractionation of biomass and biocatalytic transformation of the resulting aromatic compounds with a microbial cell factory. Engineering microbial cell factories for this biocatalysis requires characterization of bacterial pathways involved in catabolizing lignin-derived aromatic compounds. This study identifies new pathways for lignin-derived aromatic degradation in Rhodococcus, a genus of bacteria well suited for biocatalysis. Additionally, we describe previously unknown activities of characterized enzymes on lignin-derived compounds, expanding their utility. This work advances the development of strategies to replace fossil fuel-based feedstocks with sustainable alternatives.

Dataset Information

Anaerobic catabolism of aromatic compounds: a genetic and genomic view.

Publications

Anaerobic catabolism of aromatic compounds: a genetic and genomic view.

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