Gut microbiota and transcriptome response of earthworms (Metaphire guillelmi) to polymyxin B exposure

Abstract

Polymyxin B (PMB) has received widespread attention for its use as a last-line therapy against multidrug-resistant bacterial infection. However, the consequences of unintended PMB exposure on organisms in the surrounding environment remain inconclusive. Therefore, this study investigated the effects of soil PMB residue on the gut microbiota and transcriptome of earthworms (Metaphire guillelmi). The results indicated that the tested doses of PMB (0.01–100 mg/kg soil) did not significantly affect the richness and Shannon's diversity index of the earthworm gut microbiota, but PMB altered its community structure and taxonomic composition. Moreover, PMB significantly affected Lysobacter, Aeromonas, and Sphingomonas in the soil microbiota, whereas Pseudomonas was significantly impacted the earthworm gut microbiota. Furthermore, active bacteria responded more significantly to PMB than the total microbial community. Bacterial genera such as Acinetobacter and Bacillus were highly correlated with differential expression of some genes, including up-regulated genes associated with folate biosynthesis, sulphur metabolism, and the IL-17 signalling pathway, and downregulated genes involved in vitamin digestion and absorption, salivary secretion, other types of O-glycan biosynthesis, and the NOD-like receptor signalling pathway. These results suggest that adaptation to PMB stress by earthworms involves changes in energy metabolism, their immune and digestive systems, as well as glycan biosynthesis. The study findings help elucidate the relationship between earthworms and their microbiota, while providing a reference for understanding the environmental risks of PMB.