Abstract
Giant viruses have remarkable genomic repertoires—blurring the line with cellular life—and act as top–down controls of eukaryotic plankton. However, to date only six cultured giant virus genomes are available from the pelagic ocean. We used at-sea flow cytometry with staining and sorting designed to target wild predatory eukaryotes, followed by DNA sequencing and assembly, to recover novel giant viruses from the Pacific Ocean. We retrieved four ‘PacV’ partial genomes that range from 421 to 1605 Kb, with 13 contigs on average, including the largest marine viral genomic assembly reported to date. Phylogenetic analyses indicate that three of the new viruses span a clade with deep-branching members of giant Mimiviridae, incorporating the Cafeteria roenbergensis virus, the uncultivated terrestrial Faunusvirus, one PacV from a choanoflagellate and two PacV with unclear hosts. The fourth virus, oPacV-421, is phylogenetically related to viruses that infect haptophyte algae. About half the predicted proteins in each PacV have no matches in NCBI nr (e-value < 10−5), totalling 1735 previously unknown proteins; the closest affiliations of the other proteins were evenly distributed across eukaryotes, prokaryotes and viruses of eukaryotes. The PacVs encode many translational proteins and two encode eukaryotic-like proteins from the Rh family of the ammonium transporter superfamily, likely influencing the uptake of nitrogen during infection. cPacV-1605 encodes a microbial viral rhodopsin (VirR) and the biosynthesis pathway for the required chromophore, the second finding of a choanoflagellate-associated virus that encodes these genes. In co-collected metatranscriptomes, 85% of cPacV-1605 genes were expressed, with capsids, heat shock proteins and proteases among the most highly expressed. Based on orthologue presence–absence patterns across the PacVs and other eukaryotic viruses, we posit the observed viral groupings are connected to host lifestyles as heterotrophs or phototrophs.This article is part of a discussion meeting issue ‘Single cell ecology’.
Highlights
Viruses have typically been characterized as ‘simple’ pathogens that are entirely dependent on cellular life for production of progeny
Giant viruses of eukaryotes belonging to the Nucleocytoplasmic Large double stranded DNA (dsDNA) viruses, NCLDV have led to a re-write of this definition owing to the discovery that they encode multiple functions previously thought to be unique to cellular life [2,3]
These giant viruses are a source of genetic novelty [4] and encode a variety of translational proteins such as translation initiation and elongation factors, tRNA synthetases and tRNAs that had been considered hallmarks of cellular life [3,5,6]
Summary
Viruses have typically been characterized as ‘simple’ pathogens that are entirely dependent on cellular life for production of progeny. The described viruses, ChoanoV1 and ChoanoV2 each encode three microbial rhodopsin proteins, adding to the one previously found in the genome of an algal virus, and two in metagenomic assemblies of putative algal viruses [42] Unlike the latter, the ChoanoViruses encode genes for the chromophore, retinal, and may confer phototrophic capacities to their heterotrophic hosts [25]. We assembled partial viral genome sequences that provide evidence for four deepbranching viruses within the Mimiviridae, with total assembly sizes from 421 to 1605 Kb, including the largest viral genome yet recovered from the pelagic ocean We characterize these assembled genome fragments, explore similarities with the other known NCLDV and analyse their transcriptional patterns from bulk metatranscriptomes to further understand the evolution and ecology of marine giant viruses
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