Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases

Hug, Laura; Maphosa, Farai; Leys, D.; Löffler, Frank E.; Smidt, Hauke; Edwards, Elizabeth A.; Adrian, Lorenz

doi:10.1098/rstb.2012.0322

Cited by 272 publications

(299 citation statements)

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“…According to this, the electron-donating and electron-accepting reactions are orientated toward the periplasmic and cytoplasmic faces, respectively, thereby creating a proton motive force driving ATP synthesis (4,6,12). The cprA gene, however, like other reductive dehalogenase-encoding genes, codes for a preprotein with a TAT signal sequence, strongly suggesting that CprA is exported across the cytoplasmic membrane (3,56). In Desulfitobacterium hafniense strain Y51 and Sulfurospirillum multivorans, PceA is constitutively expressed.…”

Section: Discussionmentioning

confidence: 99%

Genomic, Proteomic, and Biochemical Analysis of the Organohalide Respiratory Pathway in Desulfitobacterium dehalogenans

et al. 2015

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g Desulfitobacterium dehalogenans is able to grow by organohalide respiration using 3-chloro-4-hydroxyphenyl acetate (Cl-OHPA) as an electron acceptor. We used a combination of genome sequencing, biochemical analysis of redox active components, and shotgun proteomics to study elements of the organohalide respiratory electron transport chain. The genome of Desulfitobacterium dehalogenans JW/IU-DC1 T consists of a single circular chromosome of 4,321,753 bp with a GC content of 44.97%. The genome contains 4,252 genes, including six rRNA operons and six predicted reductive dehalogenases. One of the reductive dehalogenases, CprA, is encoded by a well-characterized cprTKZEBACD gene cluster. Redox active components were identified in concentrated suspensions of cells grown on formate and Cl-OHPA or formate and fumarate, using electron paramagnetic resonance (EPR), visible spectroscopy, and high-performance liquid chromatography (HPLC) analysis of membrane extracts. In cell suspensions, these components were reduced upon addition of formate and oxidized after addition of Cl-OHPA, indicating involvement in organohalide respiration. Genome analysis revealed genes that likely encode the identified components of the electron transport chain from formate to fumarate or Cl-OHPA. Data presented here suggest that the first part of the electron transport chain from formate to fumarate or Cl-OHPA is shared. Electrons are channeled from an outward-facing formate dehydrogenase via menaquinones to a fumarate reductase located at the cytoplasmic face of the membrane. When Cl-OHPA is the terminal electron acceptor, electrons are transferred from menaquinones to outward-facing CprA, via an as-yet-unidentified membrane complex, and potentially an extracellular flavoprotein acting as an electron shuttle between the quinol dehydrogenase membrane complex and CprA.

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Section: Discussionmentioning

confidence: 99%

Genomic, Proteomic, and Biochemical Analysis of the Organohalide Respiratory Pathway in Desulfitobacterium dehalogenans

et al. 2015

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“…Although in situ bioremediation is already a well-established remediation approach, greater understanding of new microbial capabilities is important for optimization of this strategy (1,2). Some of the most interesting dechlorinating organisms are organohalide-respiring bacteria (OHRB), which couple dehalogenation with a respiration process required for growth (3)(4)(5). The most studied genus of OHRB is Dehalococcoides because of the ability of members of this genus to respire the most common chlorinated solvent contaminants, trichloroethene (TCE) and perchloroethene (PCE).…”

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Dehalogenimonas sp. Strain WBC-2 Genome and Identification of Its trans -Dichloroethene Reductive Dehalogenase, TdrA

Molenda

Quaile

Edwards

2016

Appl Environ Microbiol

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The Dehalogenimonas population in a dechlorinating enrichment culture referred to as WBC-2 was previously shown to be responsible for trans-dichloroethene (tDCE) hydrogenolysis to vinyl chloride (VC). In this study, blue native polyacrylamide gel electrophoresis (BN-PAGE) followed by enzymatic assays and protein identification using liquid chromatography coupled with mass spectrometry (LC-MS/MS) led to the functional characterization of a novel dehalogenase, TdrA. This new reductive dehalogenase (RDase) catalyzes the dechlorination of tDCE to VC. A metagenome of the WBC-2 culture was sequenced, and a complete Dehalogenimonas genome, only the second Dehalogenimonas genome to become publicly available, was closed. The tdrA dehalogenase found within the Dehalogenimonas genome appears to be on a genomic island similar to genomic islands found in Dehalococcoides. TdrA itself is most similar to TceA from Dehalococcoides sp. strain FL2 with 76.4% amino acid pairwise identity. It is likely that the horizontal transfer of rdhA genes is not only a feature of Dehalococcoides but also a feature of other Dehalococcoidia, including Dehalogenimonas. A set of primers was developed to track tdrA in WBC-2 subcultures maintained on different electron acceptors. This newest dehalogenase is an addition to the short list of functionally defined RDases sharing the usual characteristic motifs (including an AB operon, a TAT export sequence, two iron-sulfur clusters, and a corrinoid binding domain), substrate flexibility, and evidence for horizontal gene transfer within the Dehalococcoidia. Industrial, military, and agricultural practices have resulted in the release of a growing number of chemical compounds hazardous to human health and the environment. Contamination of soil and groundwater with chlorinated ethenes and ethanes is of concern due to their known toxicity and/or carcinogenicity. Although in situ bioremediation is already a well-established remediation approach, greater understanding of new microbial capabilities is important for optimization of this strategy (1, 2). Some of the most interesting dechlorinating organisms are organohalide-respiring bacteria (OHRB), which couple dehalogenation with a respiration process required for growth (3-5). The most studied genus of OHRB is Dehalococcoides because of the ability of members of this genus to respire the most common chlorinated solvent contaminants, trichloroethene (TCE) and perchloroethene (PCE). As recently as 2009, Dehalogenimonas was identified to be a new genus of OHRB most similar to Dehalococcoides. Dehalogenimonas lykanthroporepellens and Dehalogenimonas alkenigignens are the only two species of Dehalogenimonas described to date; they are capable of dihaloelimination of polychlorinated aliphatic alkanes (6-8), although Dehalogenimonas-like organisms are known to be widely distributed (9). The West Branch Canal Creek Consortium (WBC-2) culture was derived from sediments contaminated with 1,1,2,2-tetrachloroethane (1,1,2,2-TeCA) (10). In this consortium, 1,1,2,2-TeCA d...

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“…Dehalococcoides mccartyi strain DCMB5 was enriched from these microcosms and was isolated initially using 1,2,3,4-tetrachlorodibenzo-p-dioxin (TeCDD) or 1,2,4-trichlorodibenzo-p-dioxin (TrCDD) and subsequently 1,2,3-trichlorobenzene (TCB) as electron acceptors, hydrogen as the electron donor, and acetate and CO 2 as carbon sources (6). Recently, the genome of strain DCMB5 was sequenced and revealed the presence of 23 rdhAB genes encoding the catalytic subunit A and the putative membrane anchor subunit B, respectively, of reductive dehalogenases (or reductive dehalogenase homologous proteins, Rdh proteins, if not yet biochemically characterized) (7). This finding suggests that the bacterium has a high capacity for organohalide respiration with a broad range of pollutants (8).…”

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Dehalococcoides mccartyi Strain DCMB5 Respires a Broad Spectrum of Chlorinated Aromatic Compounds

Pöritz

Schiffmann

Hause

et al. 2015

Appl Environ Microbiol

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f Polyhalogenated aromatic compounds are harmful environmental contaminants and tend to persist in anoxic soils and sediments. Dehalococcoides mccartyi strain DCMB5, a strain originating from dioxin-polluted river sediment, was examined for its capacity to dehalogenate diverse chloroaromatic compounds. Strain DCMB5 used hexachlorobenzenes, pentachlorobenzenes, all three tetrachlorobenzenes, and 1,2,3-trichlorobenzene as well as 1,2,3,4-tetra-and 1,2,4-trichlorodibenzo-p-dioxin as electron acceptors for organohalide respiration. In addition, 1,2,3-trichlorodibenzo-p-dioxin and 1,3-, 1,2-, and 1,4-dichlorodibenzo-p-dioxin were dechlorinated, the latter to the nonchlorinated congener with a remarkably short lag phase of 1 to 4 days following transfer. Strain DCMB5 also dechlorinated pentachlorophenol and almost all tetra-and trichlorophenols. Tetrachloroethene was dechlorinated to trichloroethene and served as an electron acceptor for growth. To relate selected dechlorination activities to the expression of specific reductive dehalogenase genes, the proteomes of 1,2,3-trichlorobenzene-, pentachlorobenzene-, and tetrachloroethene-dechlorinating cultures were analyzed. Dcmb_86, an ortholog of the chlorobenzene reductive dehalogenase CbrA, was the most abundant reductive dehalogenase during growth with each electron acceptor, suggesting its pivotal role in organohalide respiration of strain DCMB5. Dcmb_1041 was specifically induced, however, by both chlorobenzenes, whereas 3 putative reductive dehalogenases, Dcmb_1434, Dcmb_1339, and Dcmb_1383, were detected only in tetrachloroethene-grown cells. The proteomes also harbored a type IV pilus protein and the components for its assembly, disassembly, and secretion. In addition, transmission electron microscopy of DCMB5 revealed an irregular mode of cell division as well as the presence of pili, indicating that pilus formation is a feature of D. mccartyi during organohalide respiration.

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Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases

Cited by 272 publications

References 100 publications

Genomic, Proteomic, and Biochemical Analysis of the Organohalide Respiratory Pathway in Desulfitobacterium dehalogenans

Genomic, Proteomic, and Biochemical Analysis of the Organohalide Respiratory Pathway in Desulfitobacterium dehalogenans

Dehalogenimonas sp. Strain WBC-2 Genome and Identification of Its trans -Dichloroethene Reductive Dehalogenase, TdrA

Dehalococcoides mccartyi Strain DCMB5 Respires a Broad Spectrum of Chlorinated Aromatic Compounds

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