Biodegradation and bioaugmentation of tetracycline by Providencia stuartii TX2: Performance, degradation pathway, genetic background, key enzymes, and application risk assessment

The antibiotic tetracycline (TC) is an emerging pollutant frequently detected in various environments. Biodegradation is a crucial approach for eliminating TC contamination. However, only a few efficient TC-degrading bacteria have been isolated, and the molecular mechanisms of TC degradation, as well as their application potential, remain poorly understood. This study isolated a novel TC-degrading bacterium, Providencia stuartii TX2, from the intestine of black soldier fly larvae. TX2 exhibited remarkable performance, degrading 72.17 % of 400 mg/L TC within 48 h. Genomic analysis of TX2 unveiled the presence of antibiotic resistance genes and TC degradation enzymes. Transcriptomic analysis highlighted the roles of proteins related to efflux pumps, enzymatic transformation, adversity resistance, and unknown functions. Three TC degradation pathways were proposed, with TC being transformed into 27 metabolites through epimerization, hydroxylation, oxygenation, ring opening, and de-grouping, reducing TC toxicity. Additionally, TX2 significantly enhanced TC biodegradation in four TC-contaminated environmental samples and reduced antibiotic resistance genes and mobile genetic elements in chicken manure. This research provides insights into the survival and biodegradation mechanisms of Providencia stuartii TX2 and evaluates its potential for environmental bioremediation. [Display omitted] •A highly efficient TC degradation bacterium and its genomic information.•Novel TC biodegradation intermediates and their biotoxicity are proposed.•Three TC biodegradation pathways were discussed.•Possible TC-degrading mechanisms are characterized.•Successful bioaugmentation of tetracycline removal in various environments.