Abstract
Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. While two types of virophages have been isolated, their genomic diversity and ecology remain largely unknown. Here we use time series metagenomics to identify and study the dynamics of 25 uncultivated virophage populations, 17 of which represented by complete or near-complete genomes, in two North American freshwater lakes. Taxonomic analysis suggests that these freshwater virophages represent at least three new candidate genera. Ecologically, virophage populations are repeatedly detected over years and evolutionary stable, yet their distinct abundance profiles and gene content suggest that virophage genera occupy different ecological niches. Co-occurrence analyses reveal 11 virophages strongly associated with uncultivated Mimiviridae, and three associated with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups. Together, these findings significantly augment virophage databases, help refine virophage taxonomy, and establish baseline ecological hypotheses and tools to study virophages in nature.
Highlights
Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate
All were associated with a giant virus from the Mimiviridae, a group of nucleo-cytoplasmic large DNA viruses (NCLDV) that are “giant” both by capsid and genome size, with genome complexity often rivaling that of small bacteria[6, 8,9,10,11]
We explored a 5- and 3-year metagenomic time series collected from Lake Mendota and Trout Bog Lake, respectively, to help refine taxonomy and establish baseline ecological data for virophages
Summary
Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. All were associated with a giant virus from the Mimiviridae, a group of nucleo-cytoplasmic large DNA viruses (NCLDV) that are “giant” both by capsid and genome size, with genome complexity often rivaling that of small bacteria[6, 8,9,10,11] For both Sputnik and Mavirus, virophage and NCLDV co-infection leads to reduced host cell lysis compared to infection by NCLDV alone, which highlights the peculiar role of virophages as “viral parasites of a virus”[1, 11]. Comparison of isolate genomes has revealed that 6 genes are shared by all canonical virophages (i.e., all but the virophage-like element), and virophages appear evolutionary related to other eukaryotic mobile genetic elements such as the Maverick/Polinton class of DNA transposons[5, 12, 13] This has resulted in establishment of a new family (the Lavidaviridae, for large virus-dependent or -associated virus), and two new genera (Sputnikvirus and Mavirus) to classify known virophages[14]. Co-occurrence analyses reveal putative giant viruses hosts for 11 virophages, seemingly affiliated to the ‘extended Mimiviridae’ clade, as well as three virophages co-occurring with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups
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