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      Single-virus genomics reveals hidden cosmopolitan and abundant viruses

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          Abstract

          Microbes drive ecosystems under constraints imposed by viruses. However, a lack of virus genome information hinders our ability to answer fundamental, biological questions concerning microbial communities. Here we apply single-virus genomics (SVGs) to assess whether portions of marine viral communities are missed by current techniques. The majority of the here-identified 44 viral single-amplified genomes (vSAGs) are more abundant in global ocean virome data sets than published metagenome-assembled viral genomes or isolates. This indicates that vSAGs likely best represent the dsDNA viral populations dominating the oceans. Species-specific recruitment patterns and virome simulation data suggest that vSAGs are highly microdiverse and that microdiversity hinders the metagenomic assembly, which could explain why their genomes have not been identified before. Altogether, SVGs enable the discovery of some of the likely most abundant and ecologically relevant marine viral species, such as vSAG 37-F6, which were overlooked by other methodologies.

          Abstract

          Viruses play an important role in microbial communities but, due to limitations of available techniques, our understanding of viral diversity is limited. Here, the authors use SVGs and identify highly abundant viruses in marine communities that have been previously overlooked.

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          Most cited references37

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          Explaining microbial population genomics through phage predation.

          The remarkable differences that have been detected by metagenomics in the genomes of strains of the same bacterial species are difficult to reconcile with the widely accepted paradigm that periodic selection within bacterial populations will regularly purge genomic diversity by clonal replacement. We have found that many of the genes that differ between strains affect regions that are potential phage recognition targets. We therefore propose the constant-diversity dynamics model, in which the diversity of prokaryotic populations is preserved by phage predation. We provide supporting evidence for this model from metagenomics, mathematical analysis and computer simulations. Periodic selection and phage predation dynamics are not mutually exclusive; we compare their predictions to shed light on the ecological circumstances under which each type of dynamics could predominate.
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            Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus.

            Extensive genomic diversity within coexisting members of a microbial species has been revealed through selected cultured isolates and metagenomic assemblies. Yet, the cell-by-cell genomic composition of wild uncultured populations of co-occurring cells is largely unknown. In this work, we applied large-scale single-cell genomics to study populations of the globally abundant marine cyanobacterium Prochlorococcus. We show that they are composed of hundreds of subpopulations with distinct "genomic backbones," each backbone consisting of a different set of core gene alleles linked to a small distinctive set of flexible genes. These subpopulations are estimated to have diverged at least a few million years ago, suggesting ancient, stable niche partitioning. Such a large set of coexisting subpopulations may be a general feature of free-living bacterial species with huge populations in highly mixed habitats.
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              Viral dark matter and virus–host interactions resolved from publicly available microbial genomes

              The ecological importance of viruses is now widely recognized, yet our limited knowledge of viral sequence space and virus–host interactions precludes accurate prediction of their roles and impacts. In this study, we mined publicly available bacterial and archaeal genomic data sets to identify 12,498 high-confidence viral genomes linked to their microbial hosts. These data augment public data sets 10-fold, provide first viral sequences for 13 new bacterial phyla including ecologically abundant phyla, and help taxonomically identify 7–38% of ‘unknown’ sequence space in viromes. Genome- and network-based classification was largely consistent with accepted viral taxonomy and suggested that (i) 264 new viral genera were identified (doubling known genera) and (ii) cross-taxon genomic recombination is limited. Further analyses provided empirical data on extrachromosomal prophages and coinfection prevalences, as well as evaluation of in silico virus–host linkage predictions. Together these findings illustrate the value of mining viral signal from microbial genomes. DOI: http://dx.doi.org/10.7554/eLife.08490.001
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                23 June 2017
                2017
                : 8
                : 15892
                Affiliations
                [1 ]Department of Physiology, Genetics, and Microbiology, University of Alicante, Carretera San Vicente del Raspeig , San Vicente del Raspeig, Alicante 03690, Spain
                [2 ]Centre for Genomic Regulation (CRG), The Barcelona Institute for Science and Technology (BIST) , Carrer del Doctor Aiguader, 88, PRBB Building, Barcelona 08003, Spain
                [3 ]Universitat Pompeu Fabra (UPF) , Carrer del Doctor Aiguader, 88, PRBB Building, Barcelona 08003, Spain
                [4 ]Department of Microbiology, The Ohio State University , 105 Biological Sciences Building, 484 West 12th Avenue Columbus, Ohio 43210, USA
                [5 ]Bigelow Laboratory for Ocean Sciences , 60 Bigelow Drive, PO Box 380, East Boothbay, Maine 04544, USA
                [6 ]Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM) , CSIC, Passeig Marítim, 47, Barcelona 08003, Spain
                [7 ]Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández , Campus San Juan, San Juan, Alicante 03550, Spain
                [8 ]Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, The Ohio State University , 105 Biological Sciences Building, 484 West 12th Avenue Columbus, Ohio 43210, USA
                Author notes
                Article
                ncomms15892
                10.1038/ncomms15892
                5490008
                28643787
                0670d0ea-fbd7-4a67-9396-cebdf937e7b6
                Copyright © 2017, The Author(s)

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 19 December 2016
                : 10 May 2017
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