Genomic View of Mycobacterial High Molecular Weight Polycyclic Aromatic Hydrocarbon Degradation

Kweon, Ohgew; Kim, S. J.; Cerniglia, Carl E.

doi:10.1007/978-3-540-77587-4_81

Cited by 11 publications

(15 citation statements)

References 63 publications

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“…Since its isolation in 1986, M. vanbaalenii PYR-1 (10, 18) has been extensively studied with respect to the bacterial metabo- lism of HMW PAHs (19,27). The reconstruction of PAH-MN was essentially an effort to organize the dispersed data into an integrated resource for the multiscale mining of chemical and biological data.…”

Section: Discussionmentioning

confidence: 99%

Polycyclic Aromatic Hydrocarbon Metabolic Network in Mycobacterium vanbaaleniiPYR-1

et al. 2011

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This study investigated a metabolic network (MN) from Mycobacterium vanbaalenii PYR-1 for polycyclic aromatic hydrocarbons (PAHs) from the perspective of structure, behavior, and evolution, in which multilayer omics data are integrated. Initially, we utilized a high-throughput proteomic analysis to assess the protein expression response of M. vanbaalenii PYR-1 to seven different aromatic compounds. A total of 3,431 proteins (57.38% of the genome-predicted proteins) were identified, which included 160 proteins that seemed to be involved in the degradation of aromatic hydrocarbons. Based on the proteomic data and the previous metabolic, biochemical, physiological, and genomic information, we reconstructed an experiment-based system-level PAH-MN. The structure of PAH-MN, with 183 metabolic compounds and 224 chemical reactions, has a typical scale-free nature. The behavior and evolution of the PAH-MN reveals a hierarchical modularity with funnel effects in structure/function and intimate association with evolutionary modules of the functional modules, which are the ring cleavage process (RCP), side chain process (SCP), and central aromatic process (CAP). The 189 commonly upregulated proteins in all aromatic hydrocarbon treatments provide insights into the global adaptation to facilitate the PAH metabolism. Taken together, the findings of our study provide the hierarchical viewpoint from genes/proteins/metabolites to the network via functional modules of the PAH-MN equipped with the engineering-driven approaches of modularization and rationalization, which may expand our understanding of the metabolic potential of M. vanbaalenii PYR-1 for bioremediation applications.With the 2010 Deepwater Horizon BP oil spill in the Gulf of Mexico (http://www.epa.gov/BPSpill), concerns have been raised regarding the effect of polycyclic aromatic hydrocarbons (PAHs) on the environment. PAHs are a diverse class of organic compounds with two or more fused benzene rings (4). These compounds are highly hydrophobic and not easily bioavailable to microorganisms for degradation, and they pose a significant toxicological risk to human and environmental health (4). Microbial activities represent one of the primary processes by which PAHs are eliminated from the environment (4).Mycobacterium vanbaalenii PYR-1, originally isolated from oilcontaminated estuarine sediment, was the first bacterium reported to degrade high-molecular-weight (HMW) PAHs with four or more fused benzene rings (10, 18). 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...

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Section: Discussionmentioning

confidence: 99%

Polycyclic Aromatic Hydrocarbon Metabolic Network in Mycobacterium vanbaaleniiPYR-1

et al. 2011

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“…Because of its metabolic versatility to mineralize or degrade various polycyclic aromatic hydrocarbons (PAHs), including biphenyl, naphthalene, anthracene, fluoranthene, 1-nitropyrene, phenanthrene, benzo[a]pyrene, benz [a]anthracene, and 7,12-dimethylbenz [a]anthracene (5,6,8,9,(29)(30)(31), M. vanbaalenii PYR-1 has been extensively studied as a prototype organism for bacterial PAH metabolism, with special emphasis on high-molecular-weight (HMW) PAHs with four or more fused aromatic rings (13,14,23).…”

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Functional Robustness of a Polycyclic Aromatic Hydrocarbon Metabolic Network Examined in a nidA Aromatic Ring-Hydroxylating Oxygenase Mutant of Mycobacterium vanbaalenii PYR-1

Kim

Song

Kweon

et al. 2012

Appl Environ Microbiol

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ABSTRACTIn this study, we obtained over 4,000 transposon mutants ofMycobacterium vanbaaleniiPYR-1 and analyzed one of the mutants, 8F7, which appeared to lose its ability to degrade pyrene while still being able to degrade fluoranthene. This mutant was identified to be defective innidA, encoding an aromatic ring-hydroxylating oxygenase (RHO), known to be involved in the initial oxidation step of pyrene degradation. When cultured with pyrene as a sole source of polycyclic aromatic hydrocarbon (PAH), high-pressure liquid chromatography analysis revealed that thenidAmutant showed a significant decrease in the rate of pyrene degradation compared to the wild-type PYR-1, although pyrene was still being degraded. However, when incubated with PAH mixtures including pyrene, phenanthrene, and fluoranthene, the pyrene degradation rate of the mutant was higher than that of the mutant previously incubated with pyrene as a sole source of PAH. There was no significant difference between wild-type PYR-1 and the mutant in the rates of phenanthrene and fluoranthene degradation. From the whole-cell proteome analysis of mutant 8F7 induced by pyrene, we identified expression of a number of RHO enzymes which are suspected to be responsible for pyrene degradation in thenidAmutant, which had no expression of NidA. Taken together, results in this study provide direct evidence for thein vivofunctional role ofnidAin pyrene degradation at the level of the ring-cleavage-process (RCP) functional module but also for the robustness of the PAH metabolic network (MN) to such a genetic perturbation.

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“…Because of its versatile PAH degradation ability, M. vanbaalenii PYR-1 has been extensively studied as a model at both the laboratory and field scales (16, 17). These efforts have produced considerable information on its metabolic, biochemical, physiological, and molecular characteristics, which are also found in other aromatic-compound-degrading bacteria (16)(17)(18)(19)(20)(21)(22).A global PAH metabolic network (MN) in M. vanbaalenii PYR-1 has been proposed on the basis of genomic, proteomic, metabolic, and biochemical information (23). The PAH-MN describes the biochemical pathways for the biodegradation of 10 PAHs with 183 metabolites and 224 chemical reactions, providing systematic insight into the structure, behavior, and evolution of bacterial PAH metabolism.…”

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confidence: 99%

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confidence: 99%

“…This bacterium also degrades other HMW PAHs (fluoranthene, benzo [a]pyrene, benz[a]anthracene, and 7,12-dimethylbenz[a]anthracene) and lowmolecular-weight (LMW) PAHs (naphthalene, fluorene, phenanthrene, and anthracene), primarily via dioxygenation to isomeric cis-dihydrodiols (2,(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15). Because of its versatile PAH degradation ability, M. vanbaalenii PYR-1 has been extensively studied as a model at both the laboratory and field scales (16,17). These efforts have produced considerable information on its metabolic, biochemical, physiological, and molecular characteristics, which are also found in other aromatic-compound-degrading bacteria (16)(17)(18)(19)(20)(21)(22).…”

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Pleiotropic and Epistatic Behavior of a Ring-Hydroxylating Oxygenase System in the Polycyclic Aromatic Hydrocarbon Metabolic Network from Mycobacterium vanbaalenii PYR-1

Kweon

Kim

et al. 2014

J Bacteriol

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bDespite the considerable knowledge of bacterial high-molecular-weight (HMW) polycyclic aromatic hydrocarbon (PAH) metabolism, the key enzyme(s) and its pleiotropic and epistatic behavior(s) responsible for low-molecular-weight (LMW) PAHs in HMW PAH-metabolic networks remain poorly understood. In this study, a phenotype-based strategy, coupled with a spray plate method, selected a Mycobacterium vanbaalenii PYR-1 mutant (6G11) that degrades HMW PAHs but not LMW PAHs. Sequence analysis determined that the mutant was defective in pdoA2, encoding an aromatic ring-hydroxylating oxygenase (RHO). A series of metabolic comparisons using high-performance liquid chromatography (HPLC) analysis revealed that the mutant had a lower rate of degradation of fluorene, anthracene, and pyrene. Unlike the wild type, the mutant did not produce a color change in culture media containing fluorene, phenanthrene, and fluoranthene. An Escherichia coli expression experiment confirmed the ability of the Pdo system to oxidize biphenyl, the LMW PAHs naphthalene, phenanthrene, anthracene, and fluorene, and the HMW PAHs pyrene, fluoranthene, and benzo[a]pyrene, with the highest enzymatic activity directed toward three-ring PAHs. Structure analysis and PAH substrate docking simulations of the Pdo substrate-binding pocket rationalized the experimentally observed metabolic versatility on a molecular scale. Using information obtained in this study and from previous work, we constructed an RHO-centric functional map, allowing pleiotropic and epistatic enzymatic explanation of PAH metabolism. Taking the findings together, the Pdo system is an RHO system with the pleiotropic responsibility of LMW PAH-centric hydroxylation, and its epistatic functional contribution is also crucial for the metabolic quality and quantity of the PAH-MN. Mycobacterium vanbaalenii PYR-1 was originally isolated from oil-contaminated estuarine sediment in Redfish Bay, Texas, in 1986 (1-4). It was the first bacterium shown to degrade pyrene, a high-molecular-weight (HMW) polycyclic aromatic hydrocarbon (PAH) with four fused benzene rings. This bacterium also degrades other HMW PAHs (fluoranthene, benzo[a]pyrene, benz[a]anthracene, and 7,12-dimethylbenz[a]anthracene) and lowmolecular-weight (LMW) PAHs (naphthalene, fluorene, phenanthrene, and anthracene), primarily via dioxygenation to isomeric cis-dihydrodiols (2, 5-15). Because of its versatile PAH degradation ability, M. vanbaalenii PYR-1 has been extensively studied as a model at both the laboratory and field scales (16, 17). These efforts have produced considerable information on its metabolic, biochemical, physiological, and molecular characteristics, which are also found in other aromatic-compound-degrading bacteria (16)(17)(18)(19)(20)(21)(22).A global PAH metabolic network (MN) in M. vanbaalenii PYR-1 has been proposed on the basis of genomic, proteomic, metabolic, and biochemical information (23). The PAH-MN describes the biochemical pathways for the biodegradation of 10 PAHs with 183 metabolites and 224 chemical rea...

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Genomic View of Mycobacterial High Molecular Weight Polycyclic Aromatic Hydrocarbon Degradation

Cited by 11 publications

References 63 publications

Polycyclic Aromatic Hydrocarbon Metabolic Network in Mycobacterium vanbaaleniiPYR-1

Polycyclic Aromatic Hydrocarbon Metabolic Network in Mycobacterium vanbaaleniiPYR-1

Functional Robustness of a Polycyclic Aromatic Hydrocarbon Metabolic Network Examined in a nidA Aromatic Ring-Hydroxylating Oxygenase Mutant of Mycobacterium vanbaalenii PYR-1

Pleiotropic and Epistatic Behavior of a Ring-Hydroxylating Oxygenase System in the Polycyclic Aromatic Hydrocarbon Metabolic Network from Mycobacterium vanbaalenii PYR-1

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