Substrate Specificity and Structural Characteristics of the Novel Rieske Nonheme Iron Aromatic Ring-Hydroxylating Oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1

Kweon, Ohgew; Kim, Seong-Jae; Freeman, James P.; Song, Jaekyeong; Baek, Songjoon; Cerniglia, Carl E.

doi:10.1128/mbio.00135-10

Title: Substrate Specificity and Structural Characteristics of the Novel Rieske Nonheme Iron Aromatic Ring-Hydroxylating Oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1

Journal Article · 15 June 2010 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.00135-10 · OSTI ID:1626089

Kweon, Ohgew ^[1]; Kim, Seong-Jae ^[2]; Freeman, James P. ^[3]; Song, Jaekyeong ^[4]; Baek, Songjoon ^[5]; Cerniglia, Carl E. ^[2]

U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). Divisions of Microbiology; DOE/OSTI
U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). Divisions of Microbiology
U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). Biochemical Toxicology
U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). Divisions of Microbiology; U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). National Center for Toxicological Research. Division of Biosafety; National Institute of Agricultural Biotechnology, Suwon (Korea, Republic of)
National Institutes of Health (NIH), Bethesda, MD (United States). National Cancer Inst. Lab. of Receptor Biology and Gene Expression

The Rieske nonheme iron aromatic ring-hydroxylating oxygenases (RHOs) NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1 have been implicated in the initial oxidation of high-molecular-weight (HMW) polycyclic aromatic hydrocarbons (PAHs), forming cis-dihydrodiols. To clarify how these two RHOs are functionally different with respect to the degradation of HMW PAHs, we investigated their substrate specificities to 13 representative aromatic substrates (toluene, m-xylene, phthalate, biphenyl, naphthalene, phenanthrene, anthracene, fluoranthene, pyrene, benz[a]anthracene, benzo[a]pyrene, carbazole, and dibenzothiophene) by enzyme reconstitution studies of Escherichia coli. Both Nid systems were identified to be compatible with type V electron transport chain (ETC) components, consisting of a [3Fe-4S]-type ferredoxin and a glutathione reductase (GR)-type reductase. Metabolite profiles indicated that the Nid systems oxidize a wide range of aromatic hydrocarbon compounds, producing various isomeric dihydrodiol and phenolic compounds. NidAB and NidA3B3 showed the highest conversion rates for pyrene and fluoranthene, respectively, with high product regiospecificity, whereas other aromatic substrates were converted at relatively low regiospecificity. Structural characteristics of the active sites of the Nid systems were investigated and compared to those of other RHOs. The NidAB and NidA3B3 systems showed the largest substrate-binding pockets in the active sites, which satisfies spatial requirements for accepting HMW PAHs. Spatially conserved aromatic amino acids, Phe-Phe-Phe, in the substrate-binding pockets of the Nid systems appeared to play an important role in keeping aromatic substrates within the reactive distance from the iron atom, which allows each oxygen to attack the neighboring carbons.

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Research Organization:: Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: SC0014664

OSTI ID:: 1626089

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 2 Vol. 1; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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