Multi-scale responses of soil nematode communities to mercury-associated mining contamination: from community restructuring to transcriptomic signatures of potential local adaptation.

Abstract

Mercury (Hg) is a persistent global pollutant that threatens soil ecosystem structure and function. However, for soil nematodes, most studies have focused on functional groups and model species, leaving a gap in our understanding of how community assembly processes are linked with molecular adaptive responses in field populations. Here, soil nematode communities were examined along a Hg pollution gradient (low, medium, high) in the Tongren mining area, using high-throughput sequencing and transcriptomics. While alpha diversity remained stable, beta diversity increased significantly in high-pollution zones, driven mainly by species turnover. High-pollution communities exhibited reduced niche breadth and overlap, a shift from stochastic (drift) to deterministic (homogeneous and heterogeneous selection) assembly, and increased compositional dispersion (AVD index). Heavy metals (Hg, Zn, Pb, As, Cd) and soil properties (pH, TC, TN, TS, MC) jointly shaped community variation, suggesting that Hg-associated contamination played a prominent role. Sensitive taxa (e.g., Dorylaimida) declined, while tolerant groups (e.g., Rhabditida, Enoplida) and key indicators included Acrobeloides sp. (ASV513 and ASV1143) increased. Further isolation, cultivation, and stress experiments on the dominant species Acrobeloides sp., present in both high- and low-pollution areas, revealed that high-pollution populations exhibited greater tolerance to acute ionic Hg stress, reduced ROS accumulation, and distinct baseline transcriptomic profiles, suggesting a pattern consistent with local adaptation. Tolerance was achieved through metabolic remodeling, enhancing core pathways (cysteine/methionine, ascorbate/aldarate, pyruvate metabolism). This multi-scale study reveals how Hg‑associated multi‑metal contamination restructures soil communities and drives adaptive response, providing insights for ecological risk assessment, bioindicator development, and exploration of biological resources in contaminated soils.