A legacy pollutant deciphered by multiomics toxicology and targeted remediation by a synthetic microbial consortium: a case study of 2-chloroacetophenone from abandoned chemical weapons.

Abstract

2-Chloroacetophenone (2-CA) is a typical organic poison found in abandoned Japanese chemical weapons, yet systematic research on its ecological risks and bioremediation strategies in aquatic environments remains scarce. Through a 120-day exposure experiment across three concentration gradients (10, 50, and 100 mg·L-1) coupled with multiomics analysis (physicochemical profiling, ionomics, 16S rRNA sequencing, metagenomics, and metabolomics), we systematically characterized the toxic effects of 2-CA on aquatic microbial communities and their molecular response mechanisms. The glutathione (GSH) metabolic pathway was identified as the core defense hub against 2-CA-induced oxidative stress, with multiomics data revealing its transition from compensatory activation to irreversible collapse. Guided by these mechanistic insights, we directionally isolated three cascade-degrading bacteria (Pseudomonas abietaniphila, Bacillus sp., and Arthrobacter agilis) harboring the key genes hapA, yjfP, and catA, which encode the three consecutive steps of Baeyer-Villiger oxidation, ester bond hydrolysis, and aromatic ring cleavage. The synthetic microbiome assembled from these three wild-type strains achieved 100% removal of 100 mg·L-1 2-CA within 24 h in vitro and within 10 days in simulated contaminated water, with the sequential detection of predicted intermediates (phenyl 2-chloroacetate, phenol, and pyruvic acid) confirming the operation of the cascade pathway. This study establishes a "toxicology diagnosis-functional deconstruction-synthetic reconstruction" paradigm, providing mechanistic understanding and a potential bioremediation strategy for organic toxicants at sites contaminated by relic Japanese chemical weapons, although direct ecotoxicological validation of detoxification remains to be confirmed.