Seasonal succession, host associations, and biochemical roles of aquatic viruses in a eutrophic lake plagued by cyanobacterial blooms

Abstract

Viruses are implicated to play key roles as biogeochemical mediators and ecological drivers in freshwater ecosystems. However, the dynamics of viruses and host associations throughout the seasons and during blooming periods in eutrophic freshwater ecosystems remain poorly understood. From the water microbiomes of planktonic biomass from Lake Taihu, a large eutrophic freshwater lake in China that experiences annual Microcystis-dominated harmful algal blooms (HABs), we recovered 41,997 unique viral clusters spanning a wide taxonomic range, including 15,139 Caudovirales clusters targeting bacteria and 1,044 NCLDV clusters targeting eukaryotes. The viral community exhibited clear seasonal succession, driven primarily by microbial communities (particularly Cyanobacteria and Planctomycetes) and environmental factors (mainly nutrients and temperature). Host prediction revealed that viral infection had a more distinct impact on bacteria-driven nitrogen pathways than on phosphate cycling. HAB-induced variations in microbial composition and environmental conditions affected viral strategies including viral lifestyles, host range, and virus-encoded auxiliary metabolic genes (vAMGs) distributions. Viruses infecting Proteobacteria and Actinobacteria showed an enhanced lysogenic lifestyle and a narrower host range during HAB peak in summer, while viruses infecting Bacteroidota adopted an opposite strategy. Notably, vAMGs were most abundant before the HAB outbreak in spring, compensating for bacterial metabolic processes of their hosts such as carbohydrates metabolism, photosynthesis, and phosphate regulation. The findings highlight the intricate relationships between viruses, host microbes, and the bloom-associated environment, underscoring the important biochemical roles viruses play in eutrophic freshwater ecosystems.