Unraveling metabolic fate of a veterinary antibiotic thiamphenicol via the multi-omic approach

Thiamphenicol (TAP), a typical veterinary antibiotic, is emerging as a contaminant in livestock, poultry, and aquaculture environments. Addressing this concern, this study domesticated a TAP-degrading consortium in a lab-scale activated sludge bioreactor, demonstrating efficient degradation of up to 200 mg/L TAP within 50 h and elimination of antimicrobial activity. The microbial compositions, cross-feeding interactions, and underlying metabolic mechanisms were unveiled through multi-omics. TAP was modified at two hydroxyl groups for the initial step in three pathways including oxidation at C3-OH, dehydrogenation at both C1-OH and C3-OH, and acetylation at C3-OH. Hydrogenophaga (MAG1 and MAG2) and Bosea (MAG9) were implicated in oxidation and acetylation of TAP, respectively. Aromatic compounds and 2,2-dichloroacetic acid (DCA) were the principal downstream metabolites of TAP. MAG9 (Bosea), MAG10 (Rubrivivax), and MAG13 (Hyphomicrobium) were predicted as DCA degraders, while MAG4 (Xanthobacteraceae, Ga0077548) and MAG10 (Rubrivivax) conducted the catabolism of aromatic compounds. Therefore, consortium members collaborated to efficiently reduce and detoxify TAP. Furthermore, the co-metabolism of TAP and extracellular substrates supported the microbial populations' growth. Genomic traits and transcriptional profiles suggested that the dominant Hydrogenophaga (MAG1) could store carbon and nitrogen by synthesizing cyanophycin and polyhydroxybutyrate biopolymers. Ultimately, this comprehensive understanding of TAP biodegradation will aid in formulating efficient biotreatment strategies for TAP-contaminated environments.