Identification of Reductive Dehalogenases That Mediate Complete Debromination of Penta- and Tetrabrominated Diphenyl Ethers in Dehalococcoides spp

Polybrominated diphenyl ethers (PBDEs) are persistent, highly toxic, and widely distributed environmental pollutants. The microbial populations and functional reductive dehalogenases (RDases) responsible for PBDE debromination in anoxic systems remain poorly understood, which confounds bioremediation of PBDE-contaminated sites. Here, we report a PBDE-debrominating enrichment culture dominated by a previously undescribed Dehalococcoides mccartyi population. A D. mccartyi strain, designated TZ50, whose genome contains 25 putative RDase-encoding genes, was isolated from the debrominating enrichment culture. Strain TZ50 dehalogenated a mixture of pentabrominated diphenyl ether (penta-BDE) and tetra-BDE congeners (total BDEs, 1.48 μM) to diphenyl ether within 2 weeks (0.58 μM Br-/day) via ortho- and meta-bromine elimination; strain TZ50 also dechlorinated tetrachloroethene (PCE) to vinyl chloride and ethene (260.2 μM Cl-/day). Results of native PAGE, proteomic profiling, and in vitro enzymatic activity assays implicated the involvement of three RDases in PBDE and PCE dehalogenation. TZ50_0172 (PteATZ50) and TZ50_1083 (TceATZ50) were responsible for the debromination of penta- and tetra-BDEs to di-BDE. TZ50_0172 and TZ50_1083 were also implicated in the dechlorination of PCE to trichloroethene (TCE) and of TCE to vinyl chloride/ethene, respectively. The other expressed RDase, TZ50_0090 (designated BdeA), was associated with the debromination of di-BDE to diphenyl ether, but its role in PCE dechlorination was unclear. Comparatively few RDases are known to be involved in PBDE debromination, and the identification of PteATZ50, TceATZ50, and BdeA provides additional information for evaluating debromination potential at contaminated sites. Moreover, the ability of PteATZ50 and TceATZ50 to dehalogenate both PBDEs and PCE makes strain TZ50 a suitable candidate for the remediation of cocontaminated sites. IMPORTANCE The ubiquity, toxicity, and persistence of polybrominated diphenyl ethers (PBDEs) in the environment have drawn significant public and scientific interest to the need for the remediation of PBDE-contaminated ecosystems. However, the low bioavailability of PBDEs in environmental compartments typically limits bioremediation of PBDEs and has long impeded the study of anaerobic microbial PBDE removal. In the current study, a novel Dehalococcoides mccartyi strain, dubbed strain TZ50, that expresses RDases that mediate organohalide respiration of both PBDEs and chloroethenes was isolated and characterized. Strain TZ50 could potentially be used to remediate multiple cooccurring organohalides in contaminated systems.