Among the chemicals in weapons abandoned by Japan in China during World War II, 1,4-thioxane, a typical degradation product of mustard gas, has environmental persistence and potential ecological risks. However, its toxicity mechanism and efficient remediation strategy remain unclear. This study first employed multi-omics technologies (16S sequencing, metagenomics, and metabolomics) to analyze the toxic effects of 1,4-thioxane (0-100 mg·L-1, 120 days) on water microecology. Subsequently, an efficient degrader, Pseudomonas sp. M1, was screened, and transcriptome analysis revealed significant upregulation of Fe-S cluster assembly-related genes (sufB, sufU, sufS), which are key components of the SUF sulfur conversion system. These three genes were heterologously expressed in Escherichia coli to construct three engineered strains, each capable of degrading 1,4-thioxane via the SUF system. When mixed in equal proportions to form a synthetic microbiome, they completely degraded 100 mg·L-1 1,4-thioxane in culture medium within 16 h and achieved 100% removal in simulated polluted water within 15 days. Integrated multi-omics analysis demonstrated that 1,4-thioxane is highly persistent (residual rate > 98%) but significantly inhibits nitrogen cycling, manifested by NH4+ accumulation (1.5-3.1-fold increase) and NO3- depletion (24.9-87.6% decrease), along with reduced ammonia monooxygenase, nitrite oxidoreductase, and nitrate reductase activities (67.8-91.0%, 53.2-90.1%, and 42.8-80.9% reductions, respectively). Ionome analysis showed K and P accumulation and Mo depletion; 16S sequencing revealed reduced microbial diversity, suppression of nitrogen-cycling genera, and enrichment of Pseudomonas; metagenomics uncovered widespread suppression of nitrogen metabolism pathways, dysregulation of antibiotic resistance genes, and decreased viral abundance; and metabolomics confirmed global inhibition of the alanine-aspartate-glutamate pathway. This is the first study to combine multi-omics toxicity analysis with synthetic microbiome remediation based on the SUF sulfur conversion system. The findings provide a theoretical basis and technical support for ecological risk assessment and bioremediation of sites contaminated by relic Japanese chemical weapons.