Multi-metal contamination is associated with microbial network simplification and functional adaptation in paddy...

The spatial heterogeneity of multi-metal contamination and its ecological consequences for soil microbial communities remain poorly characterized on a national scale, particularly within paddy ecosystems. This study investigated microbial ecological and genomic responses to heavy metal stress across 48 paddy soils from major rice-growing regions in China, categorized into low (LMS), moderate (MMS), and high (HMS) contamination levels. Our results indicate that multi-metal contamination triggered a significant restructuring of microbial communities, which was accompanied by increased alpha diversity and the enrichment of metal-tolerant taxa (e.g., Planctomycetes and Cyanobacteria). Conversely, microbial co-occurrence networks exhibited systematic simplification as contamination levels increased, characterized by reduced connectivity and a significant loss of keystone taxa. This suggests a transition from functionally redundant communities to modularized, survival-oriented network configurations. Metagenomic analysis revealed positive correlations between metal contamination and the abundance of nitrogen, phosphorus, and sulfur-cycling genes, while carbon-cycling genes remained relatively stable. Furthermore, genome-resolved metagenomics demonstrated widespread co-localization of metal resistance genes (MRGs) and nutrient cycling genes within metagenome-assembled genomes, particularly among key taxa (e.g., Burkholderiaceae, MBNT15). Collectively, these findings elucidate the mechanistic basis of microbial adaptation to multi-metal stress in paddy soils, providing critical insights for optimizing soil health management, developing targeted bioremediation strategies, and enhancing environmental risk assessment frameworks for contaminated agricultural ecosystems.