Phosphorus Enrichment Rewires Viral-Mediated Phosphorus Cycling in Freshwater Ecosystems via Auxiliary Metabolic Genes

Abstract

While phosphorus (P) enrichment is a well-recognized driver of eutrophication in freshwater ecosystems, the effect of phosphorus enrichment on viral communities and functions remains poorly understood. Here we conducted microcosm experiments manipulating P availability using water from an oligotrophic plateau lake, integrating amplicon sequencing/viromics and direct experimentation. The results reveal that P enrichment induces niche partitioning in prokaryotic communities, favoring copiotrophic taxa such as Cyanobacteria while maintaining α-diversity. Concurrently, viral communities exhibited β-diversity shifts, with specific lineages (e.g., Tequatrovirus, Lambdavirus) enriched and several P-related auxiliary metabolic genes (AMGs, purL, phnO and pyrE) involved in purine/pyrimidine metabolism and phosphonate utilization were identified bioinformatically in P-enriched viral metagenomes. Furthermore, viral-host interaction networks structure was changed, with cyanobacteria and Alphaproteobacteria emerging as crucial taxa. Notably, viral AMGs may accelerate P turnover rates, driven by viral-mediated production of labile organic phosphorus compounds. These findings bridge viral ecology and eutrophication science by demonstrating that viral AMGs act as metabolic catalysts, amplifying P cycling under nutrient stress. This work underscores the necessity of integrating viral processes into predictive models of eutrophication and identifies viral AMGs as potential early-warning indicators for mitigating P-driven cyanobacterial blooms and restoring ecosystem balance.

Keywords

P enrichment / prokaryotic communities / viral communities / virus-host interaction / auxiliary metabolic genes / environment geology

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