Soil nutrient conditions alter viral lifestyle strategy and potential function in phosphorous and nitrogen metabolisms

As one of the most abundant members of microbial communities, viruses are considered to influence prokaryotic mortality and biogeochemical cycles. While extensive research has been conducted to explore viral diversity and community dynamics in marine ecosystems, our understanding of soil viruses, particularly within agroecosystems, remains limited. Here, we conducted metagenomics and viromics analyses in a paddy ecosystem subjected to four different levels of soil nutrient modification by pig manure applications (PM0: 0 kg ha−1, PM1: 1930 kg ha−1, PM2: 3860 kg ha−1 and PM3: 5790 kg ha−1) over a period of 9 years. We aimed to investigate viral community adaptation and virus-host interactions in response to varying soil nutrient conditions. Our findings revealed that the viral communities are more adaptable to changes in soil nutrient contents compared to prokaryotic communities. Specifically, the relative abundance of Caudoviricetes decreased significantly with increasing levels of soil available phosphorus and total nitrogen. The ratio of lytic-lysogenic cycles increased with higher manure application rates, accompanied by an elevated prevalence of functional genes related to cell processes and viral protein structure. Moreover, we identified several putative auxiliary metabolic genes (AMGs) associated with phosphorus and nitrogen cycles, including phoA, phoH, phoB, and gdh, with the first discovery of phoB and gdh as soil viral-encoded AMG. Notably, the association between viruses and phoB-encoding bacteria displayed greater similarity within nutrient-deficient environments compared to nutrient-enriched environments, while the converse interaction pattern emerged between viruses and gdh-encoding bacteria. Collectively, our study highlights the importance of soil nutrient conditions in driving the transition between lytic-lysogenic cycles, as well as the interaction patterns between viruses and key bacteria. The insights gleaned from our findings significantly enrich our understanding of viral ecology within agricultural ecosystems.