Allyl chloride respiration by Dehalobacter shapes the fate of 1,2,3-trichloropropane

The synthetic compound 1,2,3-trichloropropane (1,2,3-TCP) is a persistent groundwater contaminant and probable human carcinogen for which effective detoxification pathways remain limited. Under anoxic conditions, microbial transformation of 1,2,3-TCP typically stalls at the intermediate allyl chloride, preventing complete detoxification. Here, we report the enrichment and characterization of Dehalobacter restrictus strain XRTCP, a bacterium capable of coupling dichloroelimination of 1,2,3-TCP with subsequent hydrogenolysis of allyl chloride to propene. While dichloroelimination to allyl chloride has been previously observed, the ability to utilize allyl chloride as a respiratory electron acceptor represents a previously unrecognized metabolic capability. This transformation was linked to microbial growth, with cell densities increasing by up to 74-fold during 1,2,3-TCP reduction and 15.8-fold during allyl chloride transformation. Metagenomic and metaproteomic analyses revealed a diverse repertoire of reductive dehalogenases (RDases), with expression patterns that differed between 1,2,3-TCP and allyl chloride amendments. Notably, a tcpA-like RDase was expressed under both 1,2,3-TCP and allyl chloride conditions, while distinct RDases were preferentially expressed under each substrate, indicating functional specialization within the dechlorination pathway. Despite this metabolic capability, propene formation remained limited due to rapid abiotic transformation of allyl chloride, primarily via reactions with reduced sulfur species, highlighting a critical branching point between biotic and abiotic pathways. These findings demonstrate that allyl chloride can function as a growth-supporting respiratory electron acceptor. More broadly, this work reveals how interactions between microbial metabolism and geochemical processes govern contaminant fate, with implications for improving both monitored natural attenuation and engineered bioremediation strategies for chlorinated solvents.