Active prophages as key drivers of microbial adaptation in global soil ecosystems.

Soils harbor the most complex microbial diversity on Earth, in which bacteria are ubiquitously infected by temperate phages. While integrated prophages often enhance host fitness, active (inducible) prophages are traditionally perceived as "molecular time bombs" due to their intrinsic lysis threat. This dual nature has raised fundamental questions about the true contribution of temperate phages to microbial adaptation and ecosystem stability. To address this gap, we conducted a global-scale integrative analysis by synthesizing 123,207 high-quality bacterial genomes, 183 soil-specific viromic data sets, and 3,749 metagenomes. We established the Global Soil Active Prophage Database (GSAPD), comprising 21,397 high-confidence active prophages, which we found to represent 34.3% of the total soil viral population within our analytical framework. Our comparative genomic analysis reveals that active prophages possess significantly larger genomes and greater genetic complexity compared with their dormant counterparts. Crucially, by mapping phage-encoded auxiliary metabolic genes (AMGs) across diverse biomes, we found that active prophages are disproportionately enriched in key pathways for carbon, nitrogen, and sulfur cycling, as well as specialized resistance mechanisms against heavy metal toxicity. These findings suggest that active prophages act as dynamic reservoirs of functional diversity. We demonstrate that their lytic potential is not merely a survival risk, but a sophisticated mechanism underpinning host environmental adaptation and niche expansion. Ultimately, this study provides a comprehensive global catalog of soil viral pathways and redefines the role of temperate phages as pivotal drivers of microbial evolution and biogeochemical cycling in terrestrial ecosystems.IMPORTANCESoils contain immense microbial diversity, yet the ecological role of temperate phages-especially their active (inducible) forms-remains poorly understood. This study provides the first global-scale assessment of active prophages in soils, revealing that they are widespread and functionally distinct from dormant forms. By building a comprehensive database and integrating multi-omics data, we show that active prophages are enriched in genes linked to key biogeochemical processes and stress resistance. These findings challenge the traditional view of active prophages as purely harmful agents and instead highlight their role as dynamic contributors to microbial function and adaptation. Our work offers new insights into how viruses shape ecosystem processes and provides a valuable resource for future studies on soil microbial ecology and nutrient cycling.