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Title: Viral dark matter and virus–host interactions resolved from publicly available microbial genomes

Abstract

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.

Authors:
 [1];  [2];  [3];  [1]
  1. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, United States
  2. Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada, Graduate Program in Bioinformatics, University of British Columbia, Vancouver, Canada
  3. U.S Department of Energy Joint Genome Institute, Walnut Creek, United States
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1209986
Alternate Identifier(s):
OSTI ID: 1209987; OSTI ID: 1628837
Grant/Contract Number:  
Joint Genome Institute (DE-AC02-05CH11231); AC02-05CH11231
Resource Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 4; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
Life Sciences & Biomedicine - Other Topics

Citation Formats

Roux, Simon, Hallam, Steven J., Woyke, Tanja, and Sullivan, Matthew B. Viral dark matter and virus–host interactions resolved from publicly available microbial genomes. United States: N. p., 2015. Web. doi:10.7554/eLife.08490.
Roux, Simon, Hallam, Steven J., Woyke, Tanja, & Sullivan, Matthew B. Viral dark matter and virus–host interactions resolved from publicly available microbial genomes. United States. https://doi.org/10.7554/eLife.08490
Roux, Simon, Hallam, Steven J., Woyke, Tanja, and Sullivan, Matthew B. Wed . "Viral dark matter and virus–host interactions resolved from publicly available microbial genomes". United States. https://doi.org/10.7554/eLife.08490.
@article{osti_1209986,
title = {Viral dark matter and virus–host interactions resolved from publicly available microbial genomes},
author = {Roux, Simon and Hallam, Steven J. and Woyke, Tanja and Sullivan, Matthew B.},
abstractNote = {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 = {10.7554/eLife.08490},
journal = {eLife},
number = ,
volume = 4,
place = {United States},
year = {Wed Jul 22 00:00:00 EDT 2015},
month = {Wed Jul 22 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.7554/eLife.08490

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Cited by: 272 works
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Works referenced in this record:

Rising to the challenge: accelerated pace of discovery transforms marine virology
journal, February 2015

  • Brum, Jennifer R.; Sullivan, Matthew B.
  • Nature Reviews Microbiology, Vol. 13, Issue 3
  • DOI: 10.1038/nrmicro3404

Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages
journal, November 2012

  • Flores, Cesar O.; Valverde, Sergi; Weitz, Joshua S.
  • The ISME Journal, Vol. 7, Issue 3
  • DOI: 10.1038/ismej.2012.135

Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton
journal, April 2015

  • Labonté, Jessica M.; Swan, Brandon K.; Poulos, Bonnie
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.48

Bacteriophages drive strain diversification in a marine Flavobacterium : implications for phage resistance and physiological properties
journal, August 2009


Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

Beyond biogeographic patterns: processes shaping the microbial landscape
journal, May 2012

  • Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire
  • Nature Reviews Microbiology, Vol. 10, Issue 7
  • DOI: 10.1038/nrmicro2795

Explaining microbial population genomics through phage predation
journal, November 2009

  • Rodriguez-Valera, Francisco; Martin-Cuadrado, Ana-Belen; Rodriguez-Brito, Beltran
  • Nature Reviews Microbiology, Vol. 7, Issue 11
  • DOI: 10.1038/nrmicro2235

A Molecular View of Microbial Diversity and the Biosphere
journal, May 1997


Phage–bacteria infection networks
journal, February 2013

  • Weitz, Joshua S.; Poisot, Timothée; Meyer, Justin R.
  • Trends in Microbiology, Vol. 21, Issue 2
  • DOI: 10.1016/j.tim.2012.11.003

Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes: Molecular evolution of T4 myoviruses
journal, February 2012


Reticulate Representation of Evolutionary and Functional Relationships between Phage Genomes
journal, February 2008

  • Lima-Mendez, G.; Van Helden, J.; Toussaint, A.
  • Molecular Biology and Evolution, Vol. 25, Issue 4
  • DOI: 10.1093/molbev/msn023

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus
journal, April 2014


Isolation and characterization of bacteriophages infecting Salmonella spp.
journal, May 2006


Patterns and ecological drivers of ocean viral communities
journal, May 2015


Prophages and bacterial genomics: what have we learned so far?: Prophage genomics
journal, June 2003


Diversity and Abundance of Single-Stranded DNA Viruses in Human Feces
journal, September 2011

  • Kim, Min-Soo; Park, Eun-Jin; Roh, Seong Woon
  • Applied and Environmental Microbiology, Vol. 77, Issue 22
  • DOI: 10.1128/AEM.06331-11

Probing Individual Environmental Bacteria for Viruses by Using Microfluidic Digital PCR
journal, June 2011


Marine viruses — major players in the global ecosystem
journal, October 2007


Recombination and Recombination-Dependent dna Replication in Bacteriophage t4
journal, December 1998


A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses
journal, January 2012


Viral tagging reveals discrete populations in Synechococcus viral genome sequence space
journal, July 2014

  • Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C.
  • Nature, Vol. 513, Issue 7517
  • DOI: 10.1038/nature13459

Single-stranded genomic architecture constrains optimal codon usage
journal, July 2011


Easyfig: a genome comparison visualizer
journal, January 2011


VirSorter: mining viral signal from microbial genomic data
journal, January 2015

  • Roux, Simon; Enault, Francois; Hurwitz, Bonnie L.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.985

Rapid diversification of coevolving marine Synechococcus and a virus
journal, March 2012

  • Marston, M. F.; Pierciey, F. J.; Shepard, A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 12
  • DOI: 10.1073/pnas.1120310109

Previously unknown and highly divergent ssDNA viruses populate the oceans
journal, July 2013


Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses
journal, November 2013

  • Roux, Simon; Enault, François; Bronner, Gisèle
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3700

The Impact of the Gut Microbiota on Human Health: An Integrative View
journal, March 2012


Metabolic reprogramming by viruses in the sunlit and dark ocean
journal, January 2013


Virus Population Dynamics and Acquired Virus Resistance in Natural Microbial Communities
journal, May 2008


Codon Bias is a Major Factor Explaining Phage Evolution in Translationally Biased Hosts
journal, February 2008


Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges
journal, July 2013

  • Kamke, Janine; Sczyrba, Alexander; Ivanova, Natalia
  • The ISME Journal, Vol. 7, Issue 12
  • DOI: 10.1038/ismej.2013.111

The major role of viruses in cellular evolution: facts and hypotheses
journal, October 2013


Microbial ecology of expanding oxygen minimum zones
journal, May 2012

  • Wright, Jody J.; Konwar, Kishori M.; Hallam, Steven J.
  • Nature Reviews Microbiology, Vol. 10, Issue 6
  • DOI: 10.1038/nrmicro2778

ACLAME: A CLAssification of Mobile genetic Elements, update 2010
journal, November 2009

  • Leplae, Raphaël; Lima-Mendez, Gipsi; Toussaint, Ariane
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp938

Hypervariable loci in the human gut virome
journal, February 2012

  • Minot, S.; Grunberg, S.; Wu, G. D.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 10
  • DOI: 10.1073/pnas.1119061109

IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Phage_Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences
journal, October 2006


Going viral: next-generation sequencing applied to phage populations in the human gut
journal, August 2012

  • Reyes, Alejandro; Semenkovich, Nicholas P.; Whiteson, Katrine
  • Nature Reviews Microbiology, Vol. 10, Issue 9
  • DOI: 10.1038/nrmicro2853

Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla: High CO
journal, April 2015

  • Emerson, Joanne B.; Thomas, Brian C.; Alvarez, Walter
  • Environmental Microbiology, Vol. 18, Issue 6
  • DOI: 10.1111/1462-2920.12817

PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies
journal, May 2012

  • Akhter, Sajia; Aziz, Ramy K.; Edwards, Robert A.
  • Nucleic Acids Research, Vol. 40, Issue 16
  • DOI: 10.1093/nar/gks406

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Multiple Layers of Chimerism in a Single-Stranded DNA Virus Discovered by Deep Sequencing
journal, April 2015

  • Krupovic, M.; Zhi, N.; Li, J.
  • Genome Biology and Evolution, Vol. 7, Issue 4
  • DOI: 10.1093/gbe/evv034

Behind the chlamydial cloak: The replication cycle of chlamydiaphage Chp2, revealed
journal, August 2008


NeSSM: A Next-Generation Sequencing Simulator for Metagenomics
journal, October 2013


Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists
journal, May 2011


Alignment-free genome comparison with feature frequency profiles (FFP) and optimal resolutions
journal, February 2009

  • Sims, Gregory E.; Jun, Se-Ran; Wu, Guohong A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 8
  • DOI: 10.1073/pnas.0813249106

Statistical structure of host-phage interactions
journal, June 2011

  • Flores, C. O.; Meyer, J. R.; Valverde, S.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 28
  • DOI: 10.1073/pnas.1101595108

Prophinder: a computational tool for prophage prediction in prokaryotic genomes
journal, January 2008


The coexistence of Escherichia coli serotype O157:H7 and its specific bacteriophage in continuous culture
journal, December 2004


A fast, lock-free approach for efficient parallel counting of occurrences of k-mers
journal, January 2011


Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean
journal, November 2012

  • Allers, Elke; Wright, Jody J.; Konwar, Kishori M.
  • The ISME Journal, Vol. 7, Issue 2
  • DOI: 10.1038/ismej.2012.108

NCBI Reference Sequences: current status, policy and new initiatives
journal, January 2009

  • Pruitt, K. D.; Tatusova, T.; Klimke, W.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn721

An efficient algorithm for large-scale detection of protein families
journal, April 2002


Related haloarchaeal pleomorphic viruses contain different genome types
journal, March 2012

  • Senčilo, Ana; Paulin, Lars; Kellner, Stefanie
  • Nucleic Acids Research, Vol. 40, Issue 12
  • DOI: 10.1093/nar/gks215

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics
journal, August 2014


Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts
journal, October 2011

  • Enav, Hagay; Béjà, Oded; Mandel-Gutfreund, Yael
  • The ISME Journal, Vol. 6, Issue 3
  • DOI: 10.1038/ismej.2011.146

PHAST: A Fast Phage Search Tool
journal, June 2011

  • Zhou, Y.; Liang, Y.; Lynch, K. H.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr485

Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment
journal, August 2013

  • Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3120

Biochemical activities of the ParA partition protein of the P1 plasmid
journal, May 1992


Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage
journal, March 1999

  • Hendrix, R. W.; Smith, M. C. M.; Burns, R. N.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 5
  • DOI: 10.1073/pnas.96.5.2192

Expanding the Marine Virosphere Using Metagenomics
journal, December 2013


The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008


The impact of prophages on bacterial chromosomes: Prophage-chromosome interaction
journal, June 2004


The Uncultured Microbial Majority
journal, October 2003


The microbial ocean from genomes to biomes
journal, May 2009