Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine

The effects of pharmaceuticals as emerging contaminants in soil on the gut microbiome and antibiotic resistome in nontarget soil fauna are largely elusive. In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the model soil collembolan (Folsomia candida) upon antiepileptic drug carbamazepine (CBZ) and antibiotic tetracycline (TC) exposure. Results showed that, individually or in combination, exposure to TC or CBZ significantly altered the gut community structure of F. candida, causing some enrichment of the bacteria associated with xenobiotic metabolism, such as Arthrobacter, Achromobacter, Gordonia, and Shinella. More importantly, oral exposure to the nonantibiotic drug CBZ enhanced the abundance and diversity of ARGs in the gut of F. candida, especially for the beta-lactams and multidrug resistance genes. Our results revealed that the most likely hosts of ARGs in the gut of F. candida were Proteobacteria and Actinobacteria. The significant positive correlation between mobile genetic elements (MGEs) and ARGs indicated the potential risk of ARGs transmission in the gut of F. candida. Overall, the nonantibiotic CBZ is likely to disturb the gut microbiota of nontarget soil fauna such as collembolans, thereby enhancing the dissemination of ARGs.