Nutrient‐Dependent Viral Lifestyle Shifts Drive Microbial Turnover and Soil Organic Carbon Accrual

ABSTRACT Viruses are increasingly recognized as active agents in soil biogeochemistry, yet their responses to decades‐long nutrient management remain poorly understood. Leveraging a 39‐year, fully replicated field experiment in a double‐rice system, we integrated virus‐enriched metagenomics, 16S rRNA amplicon sequencing, and structural equation modelling (SEM) to unravel how long‐term fertilization shapes virus–host dynamics and carbon cycling in paddy soil. Treatments ( n = 5) comprised an unfertilized control, full chemical nitrogen fertilization (180 kg ha −1 yr. −1 ), and manure substitutions of 30%, 50% and 70%. Manure inputs significantly increased bacterial and viral abundances, mitigated the diversity loss caused by chemical fertilization, and enriched copiotrophic hosts. Caudoviricetes , Malgrandaviricetes , and Faserviricetes constituted the dominant viral taxa across all samples (3 treatments × 3 replicates). The viral community composition and lifestyle strategy shifted markedly along the fertility gradient. Manure amendments increased soil nutrient availability and host abundance and coincided with higher viral counts (causing an increase in virus‐to‐bacterium ratios), and we observed a shift toward predicted virulent lifestyles (69% in M50 vs. 61% in control). In contrast, the unfertilized nutrient‐poor control contained the highest proportion of temperate phages and the greatest abundance of carbon‐related auxiliary metabolic genes (AMGs), suggesting that the lysogenic conversion provided “metabolic rescue” to hosts by supplementing key metabolic functions under oligotrophic stress. SEM revealed that these viral community attributes, including lifestyle, diversity, and AMGs, were positively associated with microbial biomass carbon and soil organic carbon under manure amendment. By integrating viral ecology into the context of nutrient management and field‐scale agroecosystem dynamics, our findings highlight viruses as an overlooked biological dimension in the design of fertilization strategies for sustainable agroecosystems.