Nanoscale zero-valent iron coupled with microorganisms enhances the removal of organochlorine pesticides in groundwater: Insights from the role of cascading effects and horizontal gene transfer

Nanoscale zero-valent iron (nZVIs) represent a promising approach for the remediation of organic chlorine-contaminated groundwater. However, the interaction between nZVIs and indigenous dechlorinating microorganisms is complex, which may have unpredictable effects on the dechlorination of organic chlorine, necessitating further investigation. In this study, we investigated an abandoned pesticide factory in southwest China, combined with microcosm experiment to reconstruct the metabolic pathway of biological dechlorination, and quantified the functional contribution of dechlorination genes and microorganisms. The results showed that the combined treatment of nZVIs and microorganisms significantly enhanced the degradation efficiency of HCHs, DDTs, and their six isomers, achieving removal rates of up to 99% for HCHs and 87.73% for DDTs. The concentrations of Cl⁻ and Fe²⁺ had a direct positive effect on the enrichment of microbial communities harboring HCHs degradation genes. Haloalkane dehalogenase encoded by the dhaA gene was identified as a key enzyme in the degradation of β-HCH precursors, which not only promoted the growth of facultative dehalogenators (particularly Acidovorax and Methyloversatilis) but also enhanced overall dechlorination activity. Importantly, we successfully reconstructed 7 near-complete bacterial metagenome-assembled genomes (MAGs) carrying the dhaA gene, representing taxonomically diverse novel dechlorinating microorganisms. Additionally, nZVIs significantly increased the abundance of mobile genetic elements (MGEs), with 17 MGEs detected within scaffolds harboring dhaA in the 7 MAGs. Integrases and transposases were identified as key drivers facilitating the spread of dhaA. This finding was supported by the shift of dhaA-harboring hosts, and by the incongruent evolutionary patterns observed between the genome-based tree and the dhaA protein phylogenetic tree. To be specific, cascading effects and horizontal gene transfer synergistically promoted the proliferation of dechlorinating microbes, providing novel strategies for managing and remediating organic chlorine-contaminated ecosystems.