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

Abstract

In this study, a total of 41,997 viral clusters were identified in surface water metagenomes from China’s eutrophic Lake Taihu. We delineated significant fluctuations in various viral characteristics throughout the year with the outbreak and decline of HABs. These fluctuations encompassed alterations in viral community structure, virus-host interactions, viral lifecycles, host ranges, and vAMGs. The observed dynamics underscored viruses as one of the crucial ecological drivers in eutrophic water environments, and untangled the ecological links between viruses, host microbes and water environment in the eutrophic freshwater ecosystem with cyanobacterial HABs. • The viral community in Lake Taihu underwent distinct seasonal succession. • Environmental factors and microbial hosts co-drove the viral community structure. • Water viruses could affect the bacteria-driven nitrogen and phosphate cycling through infection. • Viral strategies could be affected by bloom-induced environmental variations. • Viruses in Lake Taihu encoded auxiliary metabolic genes involved in central carbon metabolism. Viruses are implicated as important biogeochemical mediators and ecological drivers in freshwater ecosystems. However, the dynamics of viruses and host associations over the seasons and blooming periods in eutrophic freshwater ecosystems remain elusive. From the water microbiomes of planktonic biomass from Lake Taihu, a large and eutrophic lake that suffered from yearly Microcystis -dominated harmful algal blooms (HABs) in China, 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 distinct seasonal succession driven by microbial communities (mainly Cyanobacteria and Planctomycetes) and environmental factors (mainly nutrients and temperature). Host prediction highlighted a more distinct viral impact on bacteria-driven nitrogen pathways than phosphate cycling through infection. HAB-induced microbial and environmental variations affected viral strategies including lifestyles, host range, and virus-encoded auxiliary metabolic genes (vAMGs) distributions. Viruses infecting Proteobacteria and Actinobacteria showed enhanced lysogenic lifestyle and condensed host ranges during HAB peak in summer, while viruses infecting Bacteroidota selected the opposite strategy. Notably, vAMGs were most abundant before HAB outbreak in spring, compensating for host bacterial metabolism including carbohydrates metabolism, photosynthesis, and phosphate regulation. The elucidated relationship between viruses, host microbes, and bloom-associated environment suggested prominent biochemical roles in the eutrophic freshwater ecosystems.