Bacterial degradation of aromatic compounds via angular dioxygenation.

Abstract

Dioxygenation is one of the important initial reactions of the bacterial degradation of various aromatic compounds. Aromatic compounds, such as biphenyl, toluene, and naphthalene, are dioxygenated at lateral positions of the aromatic ring resulting in the formation of cis-dihydrodiol. This "normal" type of dioxygenation is termed lateral dioxygenation. On the other hand, the analysis of the bacterial degradation of fluorene (FN) analogues, such as 9-fluorenone, dibenzofuran (DF), carbazole (CAR), and dibenzothiophene (DBT)-sulfone, and DF-related diaryl ether compounds, dibenzo-p-dioxin (DD) and diphenyl ether (DE), revealed the presence of the novel mode of dioxygenation reaction for aromatic nucleus, generally termed angular dioxygenation. In this atypical dioxygenation, the carbon bonded to the carbonyl group in 9-fluorenone or to heteroatoms in the other compounds, and the adjacent carbon in the aromatic ring are both oxidized. Angular dioxygenation of DF, CAR, DBT-sulfone, DD, and DE produces the chemically unstable hemiacetal-like intermediates, which are spontaneously converted to 2,2,3-trihydroxybiphenyl, 2-aminobiphenyl-2,3-diol, 2,3-dihydroxybiphenyl-2-sulfinate, 2,2,3-trihydroxydiphenyl ether, and phenol and catechol, respectively. Thus, angular dioxygenation for these compounds results in the cleavage of the three-ring structure or DE structure. The angular dioxygenation product of 9-fluorenone, 1-hydro-1,1a-dihydroxy-9-fluorenone is a chemically stable cis-diol, and is enzymatically transformed to 2-carboxy-2,3-dihydroxybiphenyl. 2-Substituted 2,3-dihydroxybiphenyls formed by angular dioxygenation of FN analogues are degraded to monocyclic aromatic compounds by meta cleavage and hydrolysis. Thus, after the novel angular dioxygenation, subsequent degradation pathways are homologous to the corresponding part of that of biphenyl. Compared to the bacterial strains capable of catalyzing lateral dioxygenation, few bacteria having angular dioxygenase have been reported. Only a few degradation pathways, CARdegradation pathway of Pseudomonas resinovorans strain CA10, DF/DD-degradation pathway of Sphingomonas wittichii strain RW1, DF/DD/FN-degradation pathway of Terrabacter sp. strain DBF63, and carboxylated DE-degradation pathway of P. pseudoalcaligenes strain POB310, have been investigated at the gene level. As a result of the phylogenetic analysis and the comparison of substrate specificity of angular dioxygenase, it is suggested that this atypical mode of dioxygenation is one of the oxygenation reactions originating from the relaxed substrate specificity of the Rieske nonheme iron oxygenase superfamily. Genetic characterization of the degradation pathways of these compounds suggests the possibility that the respective genetic elements constituting the entire catabolic pathway have been recruited from various other bacteria and/or other genetic loci, and that these pathways have not evolutionary matured.

Biodiversity of Dioxin-Degrading Microorganisms and Potential Utilization in Bioremediation.

“…The metabolic pathway proposed for CAR in Pseudomonas resinovorans strain CA10 is homologous to the degradation route for DF which is initiated by angular dioxygenase attack. The biodegradation of dioxin-related compounds via angular dioxygenation and its biotechnological implications have recently been reviewed 133,136) .…”

“…Although bioremediation techniques for dioxin-polluted sites have remained undeveloped, basic information on the mechanism of microbial dioxin degradation as well as on the biodiversity and ecophysiology of dioxin-degrading microorganisms has accumulated, particularly during the past decade (for reviews, refs. 9, 23,133,136,198). The available information indicates that the ring structures of dioxins and dioxin-like compounds are degraded by aerobic bacteria that contain aromatic hydrocarbon dioxygenases having a broad substrate specificity.…”

Purification and Characterization of Carbazole 1,9a-Dioxygenase, a Three-Component Dioxygenase System of Pseudomonas resinovorans Strain CA10

“…As the initial degradation reaction, CAR is dioxygenated at the angular (C-9a) and adjacent (C-1) positions to yield the unstable cis-hydrodiol (25,27). The resultant cis-hydrodiol is spontaneously converted to 2Ј-aminobiphenyl-2,3-diol, which is further converted to anthranilate via meta cleavage and hydrolysis.…”

Identification and Characterization of Genes Encoding a Putative ABC-Type Transporter Essential for Utilization of γ-Hexachlorocyclohexane in Sphingobium japonicum UT26

“…Sphingomonas-related strains (sphingomonads) have broad catabolic abilities for natural and xenobiotic compounds, such as chlorinated phenols (5), polychlorinated biphenyls (42), polycyclic aromatic hydrocarbons (43), fluorene analogues (40), and azo dyes (51), and these bacterial strains are expected to have high potential for bioremediation of contaminated sites. Sphingomonads have glycosphingolipids in their outer membrane instead of lipopolysaccharides, which is characteristic of conventional gram-negative bacteria.…”