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Published on: September 13, 2022
Gut microbiota and transcriptome response of earthworms (Metaphire guillelmi) to polymyxin B exposure
Jun Zhao1, Guilan Duan1, Yongguan Zhu2
1State Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; University of Chinese Academy of Sciences, Beijing 100049, China.
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.
Insights
Polymyxin B (PMB) residue in soil alters earthworm gut microbial structure and gene expression, impacting energy metabolism and immunity. This study highlights potential environmental risks of PMB exposure to soil ecosystems.
Area of Science:
- Environmental Science
- Microbiology
- Toxicology
Background:
- Polymyxin B (PMB) is a critical last-line antibiotic for multidrug-resistant bacterial infections.
- Environmental impacts of PMB residue, particularly on soil organisms, are not well understood.
- Earthworms are vital soil ecosystem engineers, making them ideal models for assessing environmental contaminants.
Purpose of the Study:
- To investigate the effects of soil Polymyxin B (PMB) residue on the gut microbiota and transcriptome of earthworms (Metaphire guillelmi).
- To identify specific microbial and molecular responses of earthworms to PMB exposure.
- To assess the ecological risks associated with PMB contamination in soil environments.
Main Methods:
- Earthworms (Metaphire guillelmi) were exposed to varying doses of PMB in soil (0.01-100 mg/kg).
- Earthworm gut microbiota composition and diversity were analyzed using sequencing techniques.
- Earthworm gene expression was profiled to identify molecular pathways affected by PMB.
Main Results:
- PMB exposure altered the community structure and taxonomic composition of earthworm gut microbiota, though richness and diversity were not significantly affected.
- Specific bacterial genera in soil (Lysobacter, Aeromonas, Sphingomonas) and earthworm gut (Pseudomonas) were significantly impacted.
- PMB exposure correlated with differential gene expression in earthworms, including pathways related to energy metabolism, immune response (IL-17, NOD-like receptor), and digestion.
Conclusions:
- Earthworm adaptation to PMB stress involves significant alterations in energy metabolism, immune function, and digestive processes.
- Active soil bacteria are more sensitive to PMB than the total microbial community.
- Findings provide insights into earthworm-microbiota interactions and the environmental risks of PMB in soil ecosystems.
