Metagenomic analysis reveals global landscape of viruses in biogeochemical cycles and microbial resistance in paddy soils and wetlands.
Paddy soils and wetlands form a critical soil-water interface that supports global crop production and biogeochemical cycling. Understanding the role of viruses in these ecosystems is vital for predicting ecosystem resilience. Considering the significance of viruses in microbial community structure and environmental pollution, we analyzed 163 metagenomes from 18 countries in Asia, Europe, America, and Australia. We characterized the global distribution and potential ecological functions of viruses through viral auxiliary metabolic genes (vAMGs), antibiotic resistance genes (vARGs), and metal(loid) resistance genes (vMRGs). We found viruses with globally consistent compositions and host profiles, characterized by high richness and a dominance of lysogenic families. We identified 497 vAMGs associated with carbon, phosphorus, nitrogen, and sulfur cycling, and detected 279 vARGs (conferring resistance to 10 antibiotic) and 141 vMRGs (against 7 metal(loids)). These genes exhibited strong co-localization and co-selection patterns, and their transduction can promote the emergence of multi-resistant microbes, reshaping microbial communities. Therefore, viruses are key mobile vectors for the environmental spread of these genes. By quantifying these pathways, we provide a crucial advancement for ecological risk identification and assessment. This meta-analysis provides a comprehensive overview of virus-mediated biogeochemical processes and resistance gene propagation. We demonstrate that viruses can disseminate antibiotic and metal(loid) resistance, a pollution-driven process that poses potential health risks. Furthermore, by regulating key metabolic pathways, viruses can influence greenhouse gas fluxes. Our findings underscore the necessity of integrating viruses into climate models, pollution mitigation strategies, and One Health policies to assess ecological risks and to protect ecosystem and public health.