Nematode gut microbiota confers cadmium tolerance through microbial-dependent activation of detoxification and innate immune pathways.

INTRODUCTION: Soil heavy metal pollution, especially cadmium (Cd) contamination, represents a serious threat to ecosystem health and agricultural sustainability. Understanding how soil organisms and their associated microbiota respond to such stress is crucial for developing bioremediation strategies.

OBJECTIVES: This study aimed to investigate the response of the gut microbiota in the model soil nematodeCaenorhabditis elegansunder Cd(II) stress, identify key bacterial taxa involved in metal detoxification, and elucidate the underlying mechanisms of microbe-mediated host resistance.

METHODS: We employed an integrated multi-omics approach, combining 16S rRNA gene sequencing, transcriptomics, and culturomics. The structural and functional differences between the nematode gut microbiome and the soil microbial community were compared. A core Cd(II)-tolerant gut bacterium was isolated and used for colonization experiments inC. elegansunder Cd(II) exposure. Host responses were assessed via transcriptomic analysis, antioxidant enzyme activity assays, and physiological fitness measurements.

RESULTS: Nematode gut microbiota exhibited lower diversity but higher compositional stability compared to soil communities, with deterministic host selection (R2 = 0.480) overriding stochastic assembly. The gut community was dominated by Proteobacteria, particularly Pseudomonadaceae and Sphingomonadaceae, which maintained conserved abundances across cadmium gradients. Phenotype prediction and functional analysis revealed enhanced stress tolerance and enrichment of glutathione S-transferase (GST) in the gut microbiota. From 100 isolated colonies, we identified Brucella pseudogrignonensis (formerly Ochrobactrum) as a core gut symbiont with high Cd(II) tolerance. B. pseudogrignonensis successfully colonized the C. elegans gut, significantly improving host survival, reproduction, and growth under Cd(II) exposure. Transcriptomic analysis identified 1929 bacteria-Cd(II) interaction genes, with significant enrichment in glutathione metabolism, cytochrome P450 pathways, and lysosome function. Mechanistically, live bacteria primed host immunity (e.g., clec-67, lys-2) and activated a two-phase defense program: Phase I involved lysosome pathway activation and basal immune priming; Phase II featured GST-mediated detoxification (gst-4, gst-5, and gst-6) coordinated by transcription factors DAF-16 and SKN-1, with GSH-Px activity increasing 213% under Cd(II) stress while maintaining stable ROS levels.

CONCLUSION: Using C. elegans as a model system, we demonstrate that the gut bacterium B. pseudogrignonensis enhances host Cd(II) resistance through synergistic activation of detoxification and immune pathways. These findings provide mechanistic insights into microbe-mediated heavy metal tolerance in soil fauna and identify B. pseudogrignonensis as a promising microbial candidate for developing bioremediation strategies for cadmium contaminated soils.