Thiamethoxam (TH), a systemic neonicotinoid insecticide, poses food safety risks due to its persistence and uptake in crops. Microbial degradation during fermentation offers a promising decontamination strategy, but the underlying mechanisms and impact on food quality remain unclear. This study investigated TH and its toxic metabolite clothianidin biodegradation in Pixian broad bean paste (PBP) fermentation, assessed the impact of residue dissipation on product quality, and revealed microbial responses and metabolic adaptations under pesticide stress. Results demonstrated that TH and clothianidin were nearly completely degraded in the PBP fermentation system within 16 days, with a half-life of 3.25 days. Metagenomic analysis revealed that TH stress enriched pollutant-degrading microbes (e.g., Aspergillaceae, Desulfobacterota) and upregulated xenobiotic degradation genes (e.g., drug metabolism). However, volatile flavor compounds analysis indicated that TH treatment altered the flavor profile by reducing esters and phenols while increasing ketones and acids. Integrated metabolomics demonstrated that TH may disrupt organic acid metabolism during early fermentation, suppressing downstream flavonoid transformation and amino acid biosynthesis, ultimately compromising nutritional quality and flavor attributes. Multi-omics integration revealed that TH stress reshaped microbial community structure and enabled dual regulation of pesticide degradation and fermentation pathways through coordinated gene expression, ultimately altering PBP fermentation quality. Therefore, these findings demonstrate that the native microbial community in PBP efficiently degrades neonicotinoid pesticides, providing a novel strategy for the bioremediation of fermented foods and serving as an emerging reservoir of potential safe degrading bacteria, while highlighting the necessity for optimized microbial interventions to minimize adverse effects on product quality.
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