Lytic viruses drive the decrease in polyphosphate-accumulating and phosphate-solubilizing potential of microbial...

River damming often leads to significant phosphorus enrichment in reservoir sediments and increases the risk of eutrophication with reservoir age. Microorganisms mediate critical steps of phosphorus cycling in ecosystems, and viruses are recognized as key regulators of microbial community structure and function. However, their influence on phosphorus-cycling microorganisms (PCMs) in freshwater environments remains poorly understood. In this study, surface sediment samples were collected from nine reservoirs (12-59 years old) of southwest China and analyzed using metagenomic and metatranscriptomic approaches to profile both PCMs and viral communities. The results demonstrated that the diversity of lytic viruses was the primary factor governing both shifts in the community stability of PCMs and the restructuring of P-cycling gene patterns with increasing reservoir age. Specifically, viral lysis reduced the relative abundance of dominant PCMs, thereby enhancing community diversity and stability. Concurrently, viral activity diminished PCMs' functional potential for phosphate solubilization and polyphosphate accumulation, while stimulating high-affinity inorganic phosphate (Pi) transport. Furthermore, viruses encoded auxiliary metabolic genes (AMGs) related to phosphate solubilization, mineralization, accumulation, and transport, underscoring the viral role in regulating phosphorus retention and release. Compared to polyphosphate-accumulating microorganisms, phosphate-solubilizing microorganisms may be more susceptible to viral infection. Additionally, viral activity was associated with an increase in the relative abundance of Cyanobacteria. Taken together, our results suggest viruses are key regulators of PCMs, highlighting that they should be incorporated into future strategies for assessing and mitigating reservoir eutrophication.IMPORTANCESediment microorganisms are regarded as the engine for endogenous phosphorus release in reservoirs. Therefore, understanding their dynamics and key driving factors is essential for effective eutrophication mitigation. Viral lysis and virus-encoded auxiliary metabolic genes (AMGs) may constitute a critical yet understudied mechanism influencing microbial phosphorus cycling. Our study provides unique, time-series-based mechanistic insights into how viral activity, in the context of large-scale artificial projects (river damming), restructures microbial phosphorus cycling and its potential ecological effects over decades.