Novel Cell-Virus-Virophage Tripartite Infection Systems Discovered in the Freshwater Lake Dishui Lake in Shanghai, China

Abstract

Virophages are small parasitizing viruses of large/giant viruses. To our knowledge, the few isolated virophages all parasitize giant protozoan viruses ( Mimiviridae ) for propagation and form a tripartite infection system with hosts, here named the cell-virus-virophage (CVv) system. However, the CVv system remains largely unknown in environmental metagenomic data sets. In this study, we systematically investigated the metagenomic data set from the freshwater lake Dishui Lake, Shanghai, China. Consequently, four novel large alga viruses and seven virophages were discovered to coexist in Dishui Lake. Surprisingly, a novel CVv tripartite infection system comprising green algae, large green alga viruses ( Phycodnaviridae - and Mimiviridae -related), and virophages was identified based on genetic link, genomic signature, and CRISPR system analyses. Meanwhile, a nonhomologous CRISPR-like system was found in Dishui Lake large alga viruses, which appears to protect the virus host from the infection of Dishui Lake virophages (DSLVs). These findings are critical to give insight into the potential significance of CVv in global evolution and ecology.