title: Viral tagging reveals discrete populations in Synechococcus viral genome sequence space.
abstract: Microbes and their viruses drive myriad processes across ecosystems ranging from oceans and soils to bioreactors and humans. Despite this importance, microbial diversity is only now being mapped at scales relevant to nature, while the viral diversity associated with any particular host remains little researched. Here we quantify host-associated viral diversity using viral-tagged metagenomics, which links viruses to specific host cells for high-throughput screening and sequencing. In a single experiment, we screened 10(7) Pacific Ocean viruses against a single strain of Synechococcus and found that naturally occurring cyanophage genome sequence space is statistically clustered into discrete populations. These population-based, host-linked viral ecological data suggest that, for this single host and seawater sample alone, there are at least 26 double-stranded DNA viral populations with estimated relative abundances ranging from 0.06 to 18.2%. These populations include previously cultivated cyanophage and new viral types missed by decades of isolate-based studies. Nucleotide identities of homologous genes mostly varied by less than 1% within populations, even in hypervariable genome regions, and by 42-71% between populations, which provides benchmarks for viral metagenomics and genome-based viral species definitions. Together these findings showcase a new approach to viral ecology that quantitatively links objectively defined environmental viral populations, and their genomes, to their hosts.
authors.affiliation: 1] Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85719, USA [2] Helmholtz Zentrum München-German Research Center for Environmental Health, Institute of Groundwater Ecology, Neuherberg 85764, Germany. [3].
authors.forename: Li
authors.initials: L
authors.lastname: Deng
authors.affiliation: 1] Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85719, USA [2].
authors.forename: J Cesar
authors.initials: JC
authors.lastname: Ignacio-Espinoza
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85719, USA.
authors.forename: Ann C
authors.initials: AC
authors.lastname: Gregory
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85719, USA.
authors.forename: Bonnie T
authors.initials: BT
authors.lastname: Poulos
authors.affiliation: 1] School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA [2] School of Physics, Georgia Institute of Technology, Atlanta, Georgia 30332, USA.
authors.forename: Joshua S
authors.initials: JS
authors.lastname: Weitz
authors.affiliation: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences &Institute for Molecular Bioscience, The University of Queensland, St Lucia QLB 4072, Australia.
authors.forename: Philip
authors.initials: P
authors.lastname: Hugenholtz
authors.affiliation: 1] Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85719, USA [2] Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85719, USA.
authors.forename: Matthew B
authors.initials: MB
authors.lastname: Sullivan
mesh_terms: D044822:Biodiversity; D004783:Environmental Microbiology; D016679:Genome, Viral / Q000235:genetics*; D054884:Host-Pathogen Interactions; D054892:Metagenome; D008969:Molecular Sequence Data; D010140:Pacific Ocean; D012623:Seawater / Q000821:virology*; D013045:Species Specificity; D046940:Synechococcus / Q000821:virology*