Abstract
Virophages replicate within viral factories inside the Acanthamoeba cytoplasm, and decrease the infectivity and replication of their associated giant viruses. Culture isolation and metagenome analyses have suggested that they are common in our environment. By screening metagenomic databases in search of amoebal viruses, we detected virophage-related sequences among sequences generated from the same non-aerated bioreactor metagenome as recently screened by another team for virophage capsid-encoding genes. We describe here the assembled partial genome of a virophage closely related to Zamilon, which infects Acanthamoeba with mimiviruses of lineages B and C but not A. Searches for sequences related to amoebal giant viruses, other Megavirales representatives and virophages were conducted using BLAST against this bioreactor metagenome (PRJNA73603). Comparative genomic and phylogenetic analyses were performed using sequences from previously identified virophages. A total of 72 metagenome contigs generated from the bioreactor were identified as best matching with sequences from Megavirales representatives, mostly Pithovirus sibericum, pandoraviruses and amoebal mimiviruses from three lineages A–C, as well as from virophages. In addition, a partial genome from a Zamilon-like virophage, we named Zamilon 2, was assembled. This genome has a size of 6716 base pairs, corresponding to 39% of the Zamilon genome, and comprises partial or full-length homologs for 15 Zamilon predicted open reading frames (ORFs). Mean nucleotide and amino acid identities for these 15 Zamilon 2 ORFs with their Zamilon counterparts were 89% (range, 81–96%) and 91% (range, 78–99%), respectively. Notably, these ORFs included two encoding a capsid protein and a packaging ATPase. Comparative genomics and phylogenetic analyses indicated that the partial genome was that of a new Zamilon-like virophage. Further studies are needed to gain better knowledge of the tropism and prevalence of virophages in our biosphere and in humans.
Highlights
Mimivirus was the first amoeba-associated giant virus described in 2003 (La Scola et al, 2003)
We found sequences related to various Megavirales members, most of which being giant viruses of Acanthamoeba including mimiviruses, the known Zamilon hosts
Comparative genomics and phylogenetic analyses based upon 4 genes clearly showed that the Zamilon 2 genome was that from a Zamilonclose relative, and Zamilon 2 and Zamilon comprised a sister group to Sputnik virophages
Summary
Mimivirus was the first amoeba-associated giant virus described in 2003 (La Scola et al, 2003). Five virophages have been isolated from Acanthamoeba spp. in water samples collected from distinct geographical locations (La Scola et al, 2008; Fischer and Suttle, 2011; Gaia et al, 2013, 2014) (Table 1). Their genomes are 17.2–26.4 kilobase pairs (kbp) in length and encode 16–24 proteins. Eight additional genome sequences from virophages named YSLV1-7 and ALM were retrieved from Yellowstone Lake, USA, and Ace Lake, Antarctica, respectively (Zhou et al, 2013, 2015) Five of these virophages (YSLV1-4 and 6) were related to OLV, ALM was related to Mavirus and YSLV5 and 7 represented a novel lineage. Phylogeny reconstruction showed that MCPs from activated sludge and bioreactor metagenomes were clustered with Sputnik/Zamilon virophages, whereas those from Sargasso sea metagenome were clustered with Organic Lake/Yellowstone Lake virophages
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