This study leveraged 20 years of monitoring data from Lake Mendota to investigate viral ecological and evolutionary dynamics using metagenomic and metatranscriptomic analyses. Over 1.3 million viral genomes were analyzed to reveal patterns driven by temporal, seasonal, and environmental changes. More than 140,000 viral auxiliary metabolic genes (AMGs), involved in carbon, nitrogen, and sulfur cycling, were identified across a broad range of functional categories. High-abundance AMGs such as psbA, pmoC, and katG showed stable distributions and displayed two distinct patterns: "broad host" and "narrow host". Broad host AMGs, less influenced by environmental variability, were involved in sulfur metabolism and folate synthesis, while narrow host AMGs targeted specific host functions—for example, photosynthesis gene psbA in cyanophages, and gnd and zwf related to the pentose phosphate pathway. The study uncovered correlations between virus-host interactions and seasonal changes, along with ecological niche differentiation. High-frequency viral populations exhibited both gene-specific and genome-wide selection. This included positive selection of adaptive genes, temporal reduction in genome-wide SNP heterogeneity, and the emergence of dominant subpopulations with enhanced replication and transcriptional regulation capacities. These dominant viruses—termed “royal family” viruses—maintain ecological stability and dominance through genomic evolution, consistent with the "kill-the-winner" model. Additionally, viral abundance was linked to environmental variables such as inorganic carbon and ammonium, highlighting complex interactions between nutrient availability and predator-prey dynamics.

Freshwater Lake,Viruses