As a prevalent congener of polybrominated diphenyl ethers (PBDEs), 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) poses significant environmental and health risks due to its persistence and bioaccumulation. However, the limited understanding of the microbial degradation mechanism of BDE-47 has hindered the development of effective bioremediation strategies. Here, we decipher an aerobic catabolic pathway of BDE-47 mediated by metabolic relay within a synthetic consortium composed of two environmental isolates, Rhizorhabdus wittichii YL-JM2C and Cupriavidus necator JMP134. Bioaugmentation with this consortium achieved complete removal of BDE-47 in real wastewater samples. The molecular basis underlying this cooperative degradation was elucidated through the heterologous expression and functional characterization of key enzymes involved. Namely, the dioxygenase TcsAaAb from strain YL-JM2C catalyzed the initial conversion of BDE-47 into 2,4-dibromophenol (2,4-DBP) and 3,5-dibromocatechol (3,5-DBC). As a dead-end intermediate in strain YL-JM2C, the former (2,4-DBP) was subsequently transformed into the latter (3,5-DBC) by the hydroxylase TfdB from strain JMP134. The resulting 3,5-DBC was catabolized through the downstream ortho-cleavage pathway present in both strains. These key enzymes for BDE-47 degradation coexist across diverse environments, including soil, seawater, and marine sediments. Global marine metagenomic profiling revealed a significant enrichment of these catabolic signatures in the Mariana Trench, implying that microorganisms in the hadal zone possess the genetic potential for PBDE catabolism. This study unveils previously unrecognized aerobic catabolic mechanisms for BDE-47 within natural ecosystems, offering promising bioremediation strategies for PBDE-contaminated environments.
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