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      Viruses in the Oceanic Basement

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          ABSTRACT

          Microbial life has been detected well into the igneous crust of the seafloor (i.e., the oceanic basement), but there have been no reports confirming the presence of viruses in this habitat. To detect and characterize an ocean basement virome, geothermally heated fluid samples (ca. 60 to 65°C) were collected from 117 to 292 m deep into the ocean basement using seafloor observatories installed in two boreholes (Integrated Ocean Drilling Program [IODP] U1362A and U1362B) drilled in the eastern sediment-covered flank of the Juan de Fuca Ridge. Concentrations of virus-like particles in the fluid samples were on the order of 0.2 × 10 5 to 2 × 10 5 ml −1 ( n = 8), higher than prokaryote-like cells in the same samples by a factor of 9 on average (range, 1.5 to 27). Electron microscopy revealed diverse viral morphotypes similar to those of viruses known to infect bacteria and thermophilic archaea. An analysis of virus-like sequences in basement microbial metagenomes suggests that those from archaeon-infecting viruses were the most common (63 to 80%). Complete genomes of a putative archaeon-infecting virus and a prophage within an archaeal scaffold were identified among the assembled sequences, and sequence analysis suggests that they represent lineages divergent from known thermophilic viruses. Of the clustered regularly interspaced short palindromic repeat (CRISPR)-containing scaffolds in the metagenomes for which a taxonomy could be inferred (163 out of 737), 51 to 55% appeared to be archaeal and 45 to 49% appeared to be bacterial. These results imply that the warmed, highly altered fluids in deeply buried ocean basement harbor a distinct assemblage of novel viruses, including many that infect archaea, and that these viruses are active participants in the ecology of the basement microbiome.

          IMPORTANCE

          The hydrothermally active ocean basement is voluminous and likely provided conditions critical to the origins of life, but the microbiology of this vast habitat is not well understood. Viruses in particular, although integral to the origins, evolution, and ecology of all life on earth, have never been documented in basement fluids. This report provides the first estimate of free virus particles (virions) within fluids circulating through the extrusive basalt of the seafloor and describes the morphological and genetic signatures of basement viruses. These data push the known geographical limits of the virosphere deep into the ocean basement and point to a wealth of novel viral diversity, exploration of which could shed light on the early evolution of viruses.

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          Most cited references57

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          tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence

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            CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea.

            Sequence-directed genetic interference pathways control gene expression and preserve genome integrity in all kingdoms of life. The importance of such pathways is highlighted by the extensive study of RNA interference (RNAi) and related processes in eukaryotes. In many bacteria and most archaea, clustered, regularly interspaced short palindromic repeats (CRISPRs) are involved in a more recently discovered interference pathway that protects cells from bacteriophages and conjugative plasmids. CRISPR sequences provide an adaptive, heritable record of past infections and express CRISPR RNAs - small RNAs that target invasive nucleic acids. Here, we review the mechanisms of CRISPR interference and its roles in microbial physiology and evolution. We also discuss potential applications of this novel interference pathway.
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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

                Contributors
                Role: Editor
                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                7 March 2017
                Mar-Apr 2017
                : 8
                : 2
                : e02129-16
                Affiliations
                [a ]Department of Oceanography, University of Hawai'i at Mānoa, Honolulu, Hawai'i, USA
                [b ]Hawai'i Institute of Marine Biology, University of Hawai'i at Mānoa, Kāne'ohe, Hawai'i, USA
                Oregon State University
                Author notes
                Address correspondence to Olivia D. Nigro, onigro@ 123456hawaii.edu , or Grieg F. Steward, grieg@ 123456hawaii.edu .
                [*]

                Present address: Sean P. Jungbluth, Department of Energy, Joint Genome Institute, Walnut Creek, California, USA; Huei-Ting Lin, Institute of Oceanography, National Taiwan University, Taipei, Taiwan; Chih-Chiang Hsieh, Research Center for Environmental Changes, Academia Sinica, Nangang District, Taipei, Taiwan; Jaclyn A. Miranda, Thermo Fisher Scientific, Carlsbad, California, USA.

                Contribution no. 354 from the Center for Dark Energy Biosphere Investigations and contribution no. 9887 from the School of Ocean and Earth Science and Technology at the University of Hawai'i at Mānoa.

                Author information
                http://orcid.org/0000-0001-5988-0522
                Article
                mBio02129-16
                10.1128/mBio.02129-16
                5340873
                28270584
                d1e36dde-90b4-4f0d-aa26-b5fab00dcf98
                Copyright © 2017 Nigro et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 22 November 2016
                : 6 February 2017
                Page count
                supplementary-material: 3, Figures: 6, Tables: 1, Equations: 0, References: 70, Pages: 15, Words: 10116
                Funding
                Funded by: National Science Foundation (NSF) https://doi.org/10.13039/100000001
                Award ID: OCE-1260723
                Award ID: MCB-0604014
                Award Recipient : Sean P. Jungbluth Award Recipient : Michael S. Rappé
                Funded by: National Science Foundation (NSF) https://doi.org/10.13039/100000001
                Award ID: EF-0424599
                Award ID: OCE-0939564
                Award Recipient : Jaclyn A. Miranda Award Recipient : Christopher R. Schvarcz Award Recipient : Grieg F. Steward
                Funded by: National Science Foundation (NSF) https://doi.org/10.13039/100000001
                Award ID: EF-0424599
                Award ID: OCE-0939564
                Award Recipient : Olivia D. Nigro Award Recipient : Sean P. Jungbluth Award Recipient : Huei-Ting Lin Award Recipient : Chih-Chiang Hsieh Award Recipient : Jaclyn A. Miranda Award Recipient : Christopher R. Schvarcz Award Recipient : Michael S. Rappé Award Recipient : Grieg F. Steward
                Categories
                Research Article
                Custom metadata
                March/April 2017

                Life sciences
                Life sciences

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