Microbial Anaerobic Demethylation and Dechlorination of Chlorinated Hydroquinone Metabolites Synthesized by Basidiomycete Fungi

Milliken, Charles E.; Meier, Gregor; Watts, Joy E. M.; Sowers, Kevin R.; May, Harold D.

doi:10.1128/aem.70.1.385-392.2004

Cited by 30 publications

(18 citation statements)

References 52 publications

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“…In these methanogenic methyltransferases, the methyl group is transferred to coenzyme M. Desulfitobacteria are most commonly described as reductively dehalogenating bacteria (12,35). The O-demethylation was proposed previously to be an intermediary reaction in the dehalogenation of methoxylated chlorinated aromatics (5,24). In 2004, it was shown that two strains of Desulfitobacterium hafniense (strains DBC-2 and PCE-S) were able to utilize a variety of phenyl methyl ethers as growth substrates when an appropriate electron acceptor (e.g., fumarate) was provided (26).…”

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Characterization of anO-Demethylase of Desulfitobacterium hafniense DCB-2

2012

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Besides acetogenic bacteria, only Desulfitobacterium has been described to utilize and cleave phenyl methyl ethers under anoxic conditions; however, no ether-cleaving O-demethylases from the latter organisms have been identified and investigated so far. In this study, genes of an operon encoding O-demethylase components of Desulfitobacterium hafniense strain DCB-2 were cloned and heterologously expressed in Escherichia coli. Methyltransferases I and II were characterized. Methyltransferase I mediated the ether cleavage and the transfer of the methyl group to the superreduced corrinoid of a corrinoid protein. Desulfitobacterium methyltransferase I had 66% identity (80% similarity) to that of the vanillate-demethylating methyltransferase I (OdmB) of Acetobacterium dehalogenans. The substrate spectrum was also similar to that of the latter enzyme; however, Desulfitobacterium methyltransferase I showed a higher level of activity for guaiacol and used methyl chloride as a substrate. Methyltransferase II catalyzed the transfer of the methyl group from the methylated corrinoid protein to tetrahydrofolate. It also showed a high identity (ϳ70%) to methyltransferases II of A. dehalogenans. The corrinoid protein was produced in E. coli as cofactor-free apoprotein that could be reconstituted with hydroxocobalamin or methylcobalamin to function in the methyltransferase I and II assays. Six COG3894 proteins, which were assumed to function as activating enzymes mediating the reduction of the corrinoid protein after an inadvertent oxidation of the corrinoid cofactor, were studied with respect to their abilities to reduce the recombinant reconstituted corrinoid protein. Of these six proteins, only one was found to catalyze the reduction of the corrinoid protein.A cetogenic bacteria were the first anaerobes described to utilize phenyl methyl ethers as energy substrates (2). These organisms mediate the cleavage of the substrate ether bond and utilize the methyl group, which is oxidized to CO 2 in the oxidative part of catabolism. The reducing equivalents derived from methyl group oxidation are transferred to CO 2 upon the formation of an enzyme-bound carbon monoxide, which is then combined with further methyl groups to finally yield acetate (6). The key enzymes in the methylotrophic phenyl methyl ether metabolism of acetogens such as Acetobacterium dehalogenans (23) and Moorella thermoacetica (13) are the O-demethylases. These inducible enzyme systems mediate the ether cleavage and transfer of the methyl group to tetrahydrofolate (FH 4 ). Until now, three of these acetogenic O-demethylase systems were purified and characterized (7,14,25). In general, they consist of four protein components: two methyltransferases (MTs) (MT I and MT II), a corrinoid protein (CP), and an activating enzyme (AE). Both MTs and CP are involved in the catalytic cycle (Fig. 1) (Fig. 1). In A. dehalogenans, the genes encoding MT I, MT II, and CP are usually organized into an operon (31). Only one AE gene has been detected so far; this gene is not part of a...

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Characterization of anO-Demethylase of Desulfitobacterium hafniense DCB-2

2012

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“…Among the biosynthesized organohalides are the extensively chlorinated hydroquinone metabolites (CHMs) that are produced by basidiomycete fungi (5), such as the prevalent metabolite 2,3,5,6-tetrachloro-4-methoxyphenol (TCMP) (3,17). The primary pathway for the biodegradation of TCMP by desulfitobacteria is the removal of the two chlorines adjacent to the hydroxylated carbon, followed by demethylation and, finally, full dechlorination (11). However, an examination of mixed microbial communities from estuarine sediment and a pure culture of Desulfitobacterium sp.…”

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“…The 2,3,5,6-TCP was purchased from Supelco, the 2,3,6-TriCP was purchased from Sigma-Aldrich, and the 2,3,5-TriCP was purchased from Acros. All other compounds were synthesized as described previously (11).…”

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“…Inocula for the mixed cultures were prepared by transferring the supernatant from a sediment-containing culture, initiated with sediment from either Baltimore Harbor (39°16.8ЈN, 76°36.1ЈW) or a freshwater pond in the Cumberland Mountains (36°21.72ЈN, 84°42.07ЈW), as described previously (11). Seven Desulfitobacterium sp.…”

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“…Seven Desulfitobacterium sp. strains (DSM11544, ATCC 51507, DSM10664, DSM13498, ATCC 700357, DSM12704, and DSM10344) and Sulfurospirillum multivorans (DSM12446; previously Dehalospirillum multivorans) were grown in DSMZ medium 720 (German Collection of Microorganisms and Cell Cultures [www.dsmz.de]), which is a basic mineral medium plus 0.1% (wt/vol) pyruvate and 0.1% (wt/vol) yeast extract, and transfers were made as described previously (11). Organochlorides were added to separate cultures to achieve a final concentration of 173 M TCMP, a 183 M concentration of each 2,3,5,6-tetrachlorohydroquinone (TCHQ) and 2,3,5,6-tetrachlorophenol (2,3,5,6-TCP), a 202 M concentration of each trichlorohydroquinone (TriCHQ) and 2,3,5-trichlorophenol (2,3,5-TriCP), a 239 M concentration of each dichlorohydroquinone (DCHQ), a 155 M concentration of monochlorohydroquinone, and a 205 M concentration of 1,4-dihydroquinone.…”

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Chlorophenol Production by Anaerobic Microorganisms: Transformation of a Biogenic Chlorinated Hydroquinone Metabolite

Milliken

Meier

Sowers

et al. 2004

Appl Environ Microbiol

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Appl. Environ. Microbiol. 70: [385][386][387][388][389][390][391][392] 2004). In the present study, mixed microbial communities from Baltimore Harbor sediment and a pure culture of Desulfitobacterium sp. strain PCE1 were discovered to demethylate, reductively dehydroxylate, and dechlorinate chlorinated hydroquinones into chlorophenols. Mixed microbial cultures from a freshwater source and several other desulfitobacteria in pure culture did not perform these reactions. Desulfitobacterium sp. strain PCE1 degraded 2,3,5,6-tetrachloro-4-methoxyphenol, a metabolite of basidiomycete fungi, to 2,3,5,6-tetrachlorophenol and 2,3,5-trichlorophenol, recalcitrant compounds that are primarily synthesized anthropogenically.The presence of halogenated compounds in the environment is due primarily to anthropogenic activity, but recent investigations have demonstrated that a significant number of organohalides are biologically synthesized (5, 7) and degraded within the global halogen cycle (see reviews in references 8 and 12). Among the biosynthesized organohalides are the extensively chlorinated hydroquinone metabolites (CHMs) that are produced by basidiomycete fungi (5), such as the prevalent metabolite 2,3,5,6-tetrachloro-4-methoxyphenol (TCMP) (3, 17). The primary pathway for the biodegradation of TCMP by desulfitobacteria is the removal of the two chlorines adjacent to the hydroxylated carbon, followed by demethylation and, finally, full dechlorination (11). However, an examination of mixed microbial communities from estuarine sediment and a pure culture of Desulfitobacterium sp. strain PCE1 revealed a novel route of biodegradation ending with the accumulation of chlorophenols. Chlorophenols in the environment are present primarily due to anthropogenic activity. The U.S. Environmental Protection Agency has documented chlorophenols at many National Priority Sites (Superfund sites), and the Environmental Protection Agency and the U.S. Agency for Toxic Substances and Disease Registry list chlorophenols as priority pollutants (1, 2; see also www.atsdr.cdc.gov).Mixed cultures and several pure cultures of anaerobic bacteria were examined in this study. Inocula for the mixed cultures were prepared by transferring the supernatant from a sediment-containing culture, initiated with sediment from either Baltimore Harbor (39°16.8ЈN, 76°36.1ЈW) or a freshwater pond in the Cumberland Mountains (36°21.72ЈN, 84°42.07ЈW), as described previously (11). Seven Desulfitobacterium sp. strains (DSM11544, ATCC 51507, DSM10664, DSM13498, ATCC 700357, DSM12704, and DSM10344) and Sulfurospirillum multivorans (DSM12446; previously Dehalospirillum multivorans) were grown in DSMZ medium 720 (German Collection of Microorganisms and Cell Cultures [www.dsmz.de]), which is a basic mineral medium plus 0.1% (wt/vol) pyruvate and 0.1% (wt/vol) yeast extract, and transfers were made as described previously (11). Organochlorides were added to separate cultures to achieve a final concentration of 173 M TCMP, a 183 M concentration of each 2,3,5,6-tetrachlorohydroq...

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Biochemical and genetic bases of dehalorespiration

Futagami

Goto

Furukawa

2008

The Chemical Record

105

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Some anaerobic bacteria can effi ciently eliminate one or more halide atoms from halogenated compounds such as chlorophenols and chloroethenes through reductive dehalogenation. During this process, the bacteria utilize halogenated compounds as the terminal electron acceptors in their anaerobic respiration, called dehalorespiration, to yield energy for growth. Currently the genera of Desulfi tobacterium and Dehalococcoides occupy the major part of the dehalorespiring isolates. The former can acquire energy not only by dehalorespiration but also by other respirations utilizing organic compounds and metals. In sharp contrast, the latter is specialized in dehalorespiration and plays a crucial role in the detoxifi cation of chlorinated compounds in nature. From these bacteria, various reductive dehalogenases, which catalyze the dehalogenation reaction, were purifi ed and their corresponding genes were identifi ed. Most reductive dehalogenases exhibit similar features such as the presences of a Tat (twin arginine translocation) signal sequence, two Fe-S clusters, and a corrinoid cofactor. Some of dehalogenase-encoding genes are found to be fl anked by insertion sequences. Thus, dehalogenase genes act as a catabolic transposon, and genetic rearrangements mediated by transposable elements occur well in dehalorespirers. Moreover, the genome sequences of some dehalorespiring bacteria provide many insights into the mechanism of dehalorespiration and the evolution of a dehalogenase gene.

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Microbial Anaerobic Demethylation and Dechlorination of Chlorinated Hydroquinone Metabolites Synthesized by Basidiomycete Fungi

Cited by 30 publications

References 52 publications

Characterization of anO-Demethylase of Desulfitobacterium hafniense DCB-2

Characterization of anO-Demethylase of Desulfitobacterium hafniense DCB-2

Chlorophenol Production by Anaerobic Microorganisms: Transformation of a Biogenic Chlorinated Hydroquinone Metabolite

Biochemical and genetic bases of dehalorespiration

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