Genomic analysis of polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1

Abstract

Mycobacterium vanbaalenii PYR-1 is well known for its ability to degrade a wide range of high-molecular-weight (HMW) polycyclic aromatic hydrocarbons (PAHs). The genome of this bacterium has recently been sequenced, allowing us to gain insights into the molecular basis for the degradation of PAHs. The 6.5 Mb genome of PYR-1 contains 194 chromosomally encoded genes likely associated with degradation of aromatic compounds. The most distinctive feature of the genome is the presence of a 150 kb major catabolic region at positions 494 approximately 643 kb (region A), with an additional 31 kb region at positions 4,711 approximately 4,741 kb (region B), which is predicted to encode most enzymes for the degradation of PAHs. Region A has an atypical mosaic structure made of several gene clusters in which the genes for PAH degradation are complexly arranged and scattered around the clusters. Significant differences in the gene structure and organization as compared to other well-known aromatic hydrocarbon degraders including Pseudomonas and Burkholderia were revealed. Many identified genes were enriched with multiple paralogs showing a remarkable range of diversity, which could contribute to the wide variety of PAHs degraded by M. vanbaalenii PYR-1. The PYR-1 genome also revealed the presence of 28 genes involved in the TCA cycle. Based on the results, we proposed a pathway in which HMW PAHs are degraded into the beta-ketoadipate pathway through protocatechuate and then mineralized to CO2 via TCA cycle. We also identified 67 and 23 genes involved in PAH degradation and TCA cycle pathways, respectively, to be expressed as proteins.

Polycyclic Aromatic Hydrocarbon Metabolic Network in Mycobacterium vanbaaleniiPYR-1

“…Through the ␤-ketoadipate pathway, which consists of reactions of partial RCP and SCP, protocatechuate is converted to TCA cycle intermediates. The proteome shows a coordinated expression of CAP genes arranged as pcaHGBLIJ (21), enhancing the linearity of the metabolic route. The paralogs of ␤-ketoadipylCoA thiolase (pcaF), catalyzing the last step of the pathway, transforming ␤-ketoadipyl-CoA to succinyl-CoA and acetylCoA, also were identified in the proteome ( Fig.…”

“…Such functional association generally leads to a strong genomic association and evolutionary cohesion, resulting in coexpression or genetic linkage (3). In this respect, of particular interest are the RHO enzymes, due to their extremely low evolutionary cohesiveness and significant numerical imbalance between oxygenases and ETC (21,26). In M. vanbaalenii PYR-1, 21 genes encoding oxygenase components were identified, whereas only one copy of the type V ETC genes (phtAcAd) was found.…”

“…Since it has the ability to mineralize or degrade various kinds of PAHs, such as phenanthrene, anthracene, fluoranthene, pyrene, benzo[a]pyrene, benz [a]anthracene, and 7,12-dimethylbenz[a]anthracene (10, 11, 15-17, 24, 34-38), strain PYR-1 has been studied extensively as a prototype organism to elucidate pathways (19) and has been used to remediate PAH-contaminated soils (31). Recently, with the completion of the genome sequence of M. vanbaalenii PYR-1, efforts to elucidate the molecular background for the metabolism of PAHs have been initiated (21,22,26).Recently, a global biodegradation network has been reconstructed from public resources independently of the microbial hosts (40). In this study, we conducted research on the metabolism of PAHs by M. vanbaalenii PYR-1 from the standpoint of a metabolic network (MN).…”

“…We used high-throughput one-dimensional (1D) gel electrophoresis coupled to nanoflow-liquid chromatography-tandem mass spectrometry (nano-LC-MS/MS) approaches to yield large-scale proteome data for the response of strains PYR-1 to seven aromatic hydrocarbons, phthalate, fluorene, acenaphthylene, anthracene, phenanthrene, pyrene, and benzo[a]pyrene, which well represent characteristics of aromatic hydrocarbons degraded by strain PYR-1 in terms of their structure and metabolism. The whole-cell proteome results then were combined with previous metabolic, biochemical, physiological, and genomic information (20)(21)(22)29) to reconstruct an experimental evidence-driven PAH-MN for M. vanbaalenii PYR-1. We analyzed the network from the viewpoints of structure, behavior, and evolution, which provided a system-wide perspective on the biodegradation of PAHs and insights on how M. vanbaalenii PYR-1 satisfies the demands for unusual metabolic capability toward HMW PAHs.…”

Assessment of the Hydrocarbon Degrading Abilities of Three Bioaugmentation Agents for the Bioremediation of Crude Oil Tank Bottom Sludge Contaminated Libyan Soil

“…Compared to other bacterial degraders, Pseudomonas is unique in its ability to metabolize hydrocarbons (single fractions and mixtures) rapidly and efficiently even at high hydrocarbon concentrations [50,51]. Pseudomonas was tested for its ability of growth on a different of hydrocarbons including various PAHs, n-alkanes and complex hydrocarbon mixture.…”