title: Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean.
abstract: Metagenomics has revealed the existence of numerous uncharacterized viral lineages, which are referred to as viral "dark matter." However, our knowledge regarding viral genomes is biased toward culturable viruses. In this study, we analyzed 1,600 (1,352 nonredundant) complete double-stranded DNA viral genomes (10 to 211 kb) assembled from 52 marine viromes. Together with 244 previously reported uncultured viral genomes, a genome-wide comparison delineated 617 genus-level operational taxonomic units (OTUs) for these environmental viral genomes (EVGs). Of these, 600 OTUs contained no representatives from known viruses, thus putatively corresponding to novel viral genera. Predicted hosts of the EVGs included major groups of marine prokaryotes, such as marine group IIEuryarchaeotaand SAR86, from which no viruses have been isolated to date, as well asFlavobacteriaceaeand SAR116. Our analysis indicates that marine cyanophages are already well represented in genome databases and that one of the EVGs likely represents a new cyanophage lineage. Several EVGs encode many enzymes that appear to function for an efficient utilization of iron-sulfur clusters or to enhance host survival. This suggests that there is a selection pressure on these marine viruses to accumulate genes for specific viral propagation strategies. Finally, we revealed that EVGs contribute to a 4-fold increase in the recruitment of photic-zone viromes compared with the use of current reference viral genomes.IMPORTANCEViruses are diverse and play significant ecological roles in marine ecosystems. However, our knowledge of genome-level diversity in viruses is biased toward those isolated from few culturable hosts. Here, we determined 1,352 nonredundant complete viral genomes from marine environments. Lifting the uncertainty that clouds short incomplete sequences, whole-genome-wide analysis suggests that these environmental genomes represent hundreds of putative novel viral genera. Predicted hosts include dominant groups of marine bacteria and archaea with no isolated viruses to date. Some of the viral genomes encode many functionally related enzymes, suggesting a strong selection pressure on these marine viruses to control cellular metabolisms by accumulating genes.
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan; Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Yosuke
authors.initials: Y
authors.lastname: Nishimura
authors.affiliation: Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Hiroyasu
authors.initials: H
authors.lastname: Watai
authors.affiliation: Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Honda
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan.
authors.forename: Tomoko
authors.initials: T
authors.lastname: Mihara
authors.affiliation: Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Kimiho
authors.initials: K
authors.lastname: Omae
authors.affiliation: Department of Microbiology, the Ohio State University, Columbus, Ohio, USA.
authors.forename: Simon
authors.initials: S
authors.lastname: Roux
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan.
authors.forename: Romain
authors.initials: R
authors.lastname: Blanc-Mathieu
authors.affiliation: Research Institute of Environment, Agriculture and Fisheries, Osaka Prefecture, Osaka, Japan.
authors.forename: Keigo
authors.initials: K
authors.lastname: Yamamoto
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan; CNRS, IGS UMR 7256, Aix Marseille Université, Marseille, France.
authors.forename: Pascal
authors.initials: P
authors.lastname: Hingamp
authors.affiliation: Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Yoshihiko
authors.initials: Y
authors.lastname: Sako
authors.affiliation: Department of Microbiology, the Ohio State University, Columbus, Ohio, USA; Department of Civil, Environmental and Geodetic Engineering, the Ohio State University, Columbus, Ohio, USA.
authors.forename: Matthew B
authors.initials: MB
authors.lastname: Sullivan
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan.
authors.forename: Susumu
authors.initials: S
authors.lastname: Goto
authors.affiliation: Institute for Chemical Research, Kyoto University, Uji, Kyoto, Japan.
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Ogata
authors.affiliation: Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Yoshida
keywords: genome; marine ecosystem; metabolism; metagenomics; virus