Metabolism of fluoranthene by mycobacterial strains isolated by their ability to grow in fluoranthene or pyrene

Abstract

Mycobacterium sp. strains CP1, CP2, CFt2 and CFt6 were isolated from creosote-contaminated soil due to their ability to grow in pyrene (CP1 and CP2) or fluoranthene (CFt2 and CFt6). All these strains utilized fluoranthene as a sole source of carbon and energy. Strain CP1 exhibited the best growth, with a cellular assimilation of fluoranthene carbon of approximately 45%. Identification of the metabolites accumulated during growth in fluoranthene, the kinetics of metabolites, and metabolite feeding studies, indicated that all these isolates oxidized fluoranthene by the following two routes: the first involves dioxygenation at C-1 and C-2, meta cleavage, and a 2-carbon fragment excision to produce 9-fluorenone-1-carboxylic acid. An angular dioxygenation of the latter yields cis-1,9a-dihydroxy-1-hydrofluorene-9-one-8-carboxylic acid, which is further degraded via 8-hydroxy-3,4-benzocoumarin-1-carboxylic acid, benzene-1,2,3-tricarboxylic acid, and phthalate; the second route involves dioxygenation at C-2 and C-3 and ortho cleavage to give Z-9-carboxymethylenefluorene-1-carboxylic acid. In addition, the pyrene-degrading strains CP1 and CP2 possess a third route initiated by dioxygenation at positions C-7 and C-8, which--following meta cleavage, an aldolase reaction, and a C(1)-fragment excision--yields acenaphthenone. Monooxygenation of this ketone to the corresponding quinone, and its subsequent hydrolysis, produces naphthalene-1,8-dicarboxylic acid. The results obtained in this study not only complete and confirm the three fluoranthene degradation routes previously proposed for the pyrene-degrading strain Mycobacterium sp. AP1, but also suggest that such routes represent general microbial processes for environmental fluoranthene removal.

A Polyomic Approach To Elucidate the Fluoranthene-Degradative Pathway in Mycobacterium vanbaalenii PYR-1

“…However, in Mycobacterium sp. strains AP1, CP1, CP2, CFt2, and CFt6, (9E)-9-carboxymethylenefluorene-1-carboxylic acid (VI) was suggested to be a dead-end product in fluoranthene metabolism (37,38).…”

Actions of Mycobacterium sp. Strain AP1 on the Saturated- and Aromatic-Hydrocarbon Fractions of Fuel Oil in a Marine Medium

“…The GC-MS analytical conditions used for detection of metabolites were those described previously (45). When possible, oxidation products were identified by comparison of their MS spectra and GC retention times with those obtained for authentic commercial standards or for metabolites isolated and identified in previous biodegradation studies with single PAHs (29,30,45). When commercial products were not available, identification was performed by comparison of the MS spectra with those in databases (National Institute of Standards and Technology).…”

“…The pathways for the complete degradation of hydrocarbons containing two and three aromatic rings by gram-negative bacteria are well characterized for such conditions (7,22). Conversely, degradation of hydrocarbons containing four or more fused aromatic rings, such as pyrene, has been reported only for soil actinomycetes (20,25,29,30,36,45), which use multibranched pathways involving both classical dioxygenation and meta-cleavage reactions and novel ortho-cleavage mechanisms uncommon in gram-negative organisms (23). Due to the relaxed specificity of some degradative enzymes, mainly dioxygenases (15,37), PAH-degrading strains have a wide range of substrates, being able to act simultaneously on a number of structural analogs and to oxidize them to different extents (18,37).…”

Complete and Integrated Pyrene Degradation Pathway in Mycobacterium vanbaalenii PYR-1 Based on Systems Biology

“…Pyrene has been used as a model compound to study biodegradation of HMW PAHs since it is structurally similar to several carcinogenic PAHs (24). Although a number of bacterial isolates have been reported to grow on or mineralize pyrene, the majority of these isolates are nocardioform actinomycetes, such as members of the genera Mycobacterium (4,12,19,26,40,48,56,60) and Rhodococcus (6,61).…”