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Journal of Bacteriology, July 2007, p. 4635-4647, Vol. 189, No. 13
0021-9193/07/$08.00+0     doi:10.1128/JB.00128-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

A Polyomic Approach To Elucidate the Fluoranthene-Degradative Pathway in Mycobacterium vanbaalenii PYR-1{triangledown} ,{dagger}

Ohgew Kweon,1,{ddagger} Seong-Jae Kim,1,{ddagger} Richard C. Jones,2,{ddagger} James P. Freeman,3 Michael D. Adjei,1,§ Ricky D. Edmondson,2 and Carl E. Cerniglia1*

Division of Microbiology,1 Division of Systems Toxicology,2 Division of Biochemical Toxicology, National Center for Toxicological Research/FDA, Jefferson, Arkansas 720793

Received 25 January 2007/ Accepted 12 April 2007

Mycobacterium vanbaalenii PYR-1 is capable of degrading a wide range of high-molecular-weight polycyclic aromatic hydrocarbons (PAHs), including fluoranthene. We used a combination of metabolomic, genomic, and proteomic technologies to investigate fluoranthene degradation in this strain. Thirty-seven fluoranthene metabolites including potential isomers were isolated from the culture medium and analyzed by high-performance liquid chromatography, gas chromatography-mass spectrometry, and UV-visible absorption. Total proteins were separated by one-dimensional gel and analyzed by liquid chromatography-tandem mass spectrometry in conjunction with the M. vanbaalenii PYR-1 genome sequence (http://jgi.doe.gov), which resulted in the identification of 1,122 proteins. Among them, 53 enzymes were determined to be likely involved in fluoranthene degradation. We integrated the metabolic information with the genomic and proteomic results and proposed pathways for the degradation of fluoranthene. According to our hypothesis, the oxidation of fluoranthene is initiated by dioxygenation at the C-1,2, C-2,3, and C-7,8 positions. The C-1,2 and C-2,3 dioxygenation routes degrade fluoranthene via fluorene-type metabolites, whereas the C-7,8 routes oxidize fluoranthene via acenaphthylene-type metabolites. The major site of dioxygenation is the C-2,3 dioxygenation route, which consists of 18 enzymatic steps via 9-fluorenone-1-carboxylic acid and phthalate with the initial ring-hydroxylating oxygenase, NidA3B3, oxidizing fluoranthene to fluoranthene cis-2,3-dihydrodiol. Nonspecific monooxygenation of fluoranthene with subsequent O methylation of dihydroxyfluoranthene also occurs as a detoxification reaction.

* Corresponding author. Mailing address: Division of Microbiology, NCTR/US FDA, 3900 NCTR Road, Jefferson, AR 72079. Phone: (870) 543-7341. Fax: (870) 543-7307. E-mail: carl.cerniglia{at}fda.hhs.gov

{triangledown} Published ahead of print on 20 April 2007.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

{ddagger} O.K., S.-J.K., and R.C.J. contributed equally to this work.

§ Present address: Norfolk Department of Public Health, 830 Southampton Ave., Norfolk, VA 23510.

Journal of Bacteriology, July 2007, p. 4635-4647, Vol. 189, No. 13
0021-9193/07/$08.00+0     doi:10.1128/JB.00128-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.





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