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Title: Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks

Abstract

Microbiomes from every environment contain a myriad of uncultivated archaeal and bacterial viruses, but studying these viruses is hampered by the lack of a universal, scalable taxonomic framework. We present vConTACT v.2.0, a network-based application utilizing whole genome gene-sharing profiles for virus taxonomy that integrates distance-based hierarchical clustering and confidence scores for all taxonomic predictions. We report near-identical (96%) replication of existing genus-level viral taxonomy assignments from the International Committee on Taxonomy of Viruses for National Center for Biotechnology Information virus RefSeq. Application of vConTACT v.2.0 to 1,364 previously unclassified viruses deposited in virus RefSeq as reference genomes produced automatic, high-confidence genus assignments for 820 of the 1,364. We applied vConTACT v.2.0 to analyze 15,280 Global Ocean Virome genome fragments and were able to provide taxonomic assignments for 31% of these data, which shows that our algorithm is scalable to very large metagenomic datasets. Finally, our taxonomy tool can be automated and applied to metagenomes from any environment for virus classification.

Authors:
 [1];  [1]; ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5];  [6]; ORCiD logo [7];  [8]; ORCiD logo [9]; ORCiD logo [1]
  1. Ohio State Univ., Columbus, OH (United States)
  2. National Inst. of Health, Fort Detrick, Frederick, MD (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of Liverpool (United Kingdom); Quadram Inst. Bioscience, Norwich (United Kingdom)
  5. National Inst. of Health, Bethesda, MD (United States)
  6. Univ. of Guelph, ON (Canada)
  7. Inst. Pasteur, Paris (France)
  8. Katholieke Univ. Leuven (Belgium)
  9. Univ. of the West England, Bristol (United Kingdom)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); US National Institute of Allergy and Infectious Diseases (NIAID
OSTI Identifier:
1580836
Grant/Contract Number:  
AC02-05CH11231; HHSN272200700016I
Resource Type:
Accepted Manuscript
Journal Name:
Nature Biotechnology
Additional Journal Information:
Journal Volume: 37; Journal Issue: 6; Journal ID: ISSN 1087-0156
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bin Jang, Ho, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Lavigne, Rob, Turner, Dann, and Sullivan, Matthew B. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. United States: N. p., 2019. Web. doi:10.1038/s41587-019-0100-8.
Bin Jang, Ho, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Lavigne, Rob, Turner, Dann, & Sullivan, Matthew B. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. United States. doi:10.1038/s41587-019-0100-8.
Bin Jang, Ho, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Lavigne, Rob, Turner, Dann, and Sullivan, Matthew B. Mon . "Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks". United States. doi:10.1038/s41587-019-0100-8.
@article{osti_1580836,
title = {Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks},
author = {Bin Jang, Ho and Bolduc, Benjamin and Zablocki, Olivier and Kuhn, Jens H. and Roux, Simon and Adriaenssens, Evelien M. and Brister, J. Rodney and Kropinski, Andrew M. and Krupovic, Mart and Lavigne, Rob and Turner, Dann and Sullivan, Matthew B.},
abstractNote = {Microbiomes from every environment contain a myriad of uncultivated archaeal and bacterial viruses, but studying these viruses is hampered by the lack of a universal, scalable taxonomic framework. We present vConTACT v.2.0, a network-based application utilizing whole genome gene-sharing profiles for virus taxonomy that integrates distance-based hierarchical clustering and confidence scores for all taxonomic predictions. We report near-identical (96%) replication of existing genus-level viral taxonomy assignments from the International Committee on Taxonomy of Viruses for National Center for Biotechnology Information virus RefSeq. Application of vConTACT v.2.0 to 1,364 previously unclassified viruses deposited in virus RefSeq as reference genomes produced automatic, high-confidence genus assignments for 820 of the 1,364. We applied vConTACT v.2.0 to analyze 15,280 Global Ocean Virome genome fragments and were able to provide taxonomic assignments for 31% of these data, which shows that our algorithm is scalable to very large metagenomic datasets. Finally, our taxonomy tool can be automated and applied to metagenomes from any environment for virus classification.},
doi = {10.1038/s41587-019-0100-8},
journal = {Nature Biotechnology},
number = 6,
volume = 37,
place = {United States},
year = {2019},
month = {5}
}

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    Works referencing / citing this record:

    Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses
    journal, September 2016

    • Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E.
    • Nature, Vol. 537, Issue 7622
    • DOI: 10.1038/nature19366

    A structured annotation frame for the transposable phages: A new proposed family “Saltoviridae” within the Caudovirales
    journal, March 2015


    The global ocean microbiome
    journal, December 2015


    Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
    journal, April 2014


    Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation
    journal, November 2015

    • O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney
    • Nucleic Acids Research, Vol. 44, Issue D1
    • DOI: 10.1093/nar/gkv1189

    Classification of Myoviridae bacteriophages using protein sequence similarity
    journal, January 2009


    Analysis of Spounaviruses as a Case Study for the Overdue Reclassification of Tailed Phages
    journal, May 2019


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    journal, December 2018

    • Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E.
    • Nature Biotechnology, Vol. 37, Issue 1
    • DOI: 10.1038/nbt.4306

    IntScore: a web tool for confidence scoring of biological interactions
    journal, May 2012

    • Kamburov, Atanas; Stelzl, Ulrich; Herwig, Ralf
    • Nucleic Acids Research, Vol. 40, Issue W1
    • DOI: 10.1093/nar/gks492

    Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer
    journal, November 2016

    • Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar
    • BMC Genomics, Vol. 17, Issue 1
    • DOI: 10.1186/s12864-016-3286-x

    Genome-based phylogeny of dsDNA viruses by a novel alignment-free method
    journal, January 2012


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    journal, November 2006


    Biological species in the viral world
    journal, May 2018

    • Bobay, Louis-Marie; Ochman, Howard
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 23
    • DOI: 10.1073/pnas.1717593115

    Taxonomy of prokaryotic viruses: 2017 update from the ICTV Bacterial and Archaeal Viruses Subcommittee
    journal, January 2018

    • Adriaenssens, Evelien M.; Wittmann, Johannes; Kuhn, Jens H.
    • Archives of Virology, Vol. 163, Issue 4
    • DOI: 10.1007/s00705-018-3723-z

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


    The ‘Neglected’ Soil Virome – Potential Role and Impact
    journal, August 2018


    Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools
    journal, June 2008


    Detecting overlapping protein complexes in protein-protein interaction networks
    journal, March 2012

    • Nepusz, Tamás; Yu, Haiyuan; Paccanaro, Alberto
    • Nature Methods, Vol. 9, Issue 5
    • DOI: 10.1038/nmeth.1938

    Evaluation of the genomic diversity of viruses infecting bacteria, archaea and eukaryotes using a common bioinformatic platform: steps towards a unified taxonomy
    journal, September 2018

    • Aiewsakun, Pakorn; Adriaenssens, Evelien M.; Lavigne, Rob
    • Journal of General Virology, Vol. 99, Issue 9
    • DOI: 10.1099/jgv.0.001110

    NCBI Viral Genomes Resource
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    • Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming
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    • DOI: 10.1093/nar/gku1207

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    journal, April 2017

    • Adams, Michael J.; Lefkowitz, Elliot J.; King, Andrew M. Q.
    • Archives of Virology, Vol. 162, Issue 8
    • DOI: 10.1007/s00705-017-3358-5

    Phage or foe: an insight into the impact of viral predation on microbial communities
    journal, January 2018


    Bacteriophage evolution differs by host, lifestyle and genome
    journal, July 2017


    Putative archaeal viruses from the mesopelagic ocean
    journal, January 2017


    Viral metabolic reprogramming in marine ecosystems
    journal, June 2016


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


    Comparing the performance of biomedical clustering methods
    journal, September 2015

    • Wiwie, Christian; Baumbach, Jan; Röttger, Richard
    • Nature Methods, Vol. 12, Issue 11
    • DOI: 10.1038/nmeth.3583

    Deciphering the Human Virome with Single-Virus Genomics and Metagenomics
    journal, March 2018

    • de la Cruz Peña, Maria; Martinez-Hernandez, Francisco; Garcia-Heredia, Inmaculada
    • Viruses, Vol. 10, Issue 3
    • DOI: 10.3390/v10030113

    Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
    journal, October 2017


    Challenges in RNA virus bioinformatics
    journal, March 2014


    Assessing experimentally derived interactions in a small world
    journal, April 2003

    • Goldberg, D. S.; Roth, F. P.
    • Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
    • DOI: 10.1073/pnas.0735871100

    Structure and function of the global ocean microbiome
    journal, May 2015


    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

    Whole-genome prokaryotic phylogeny
    journal, May 2004


    A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
    journal, August 2018

    • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
    • Nature Biotechnology, Vol. 36, Issue 10
    • DOI: 10.1038/nbt.4229

    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

    Fast and sensitive protein alignment using DIAMOND
    journal, November 2014

    • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
    • Nature Methods, Vol. 12, Issue 1
    • DOI: 10.1038/nmeth.3176

    Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee
    journal, January 2016

    • Krupovic, Mart; Dutilh, Bas E.; Adriaenssens, Evelien M.
    • Archives of Virology, Vol. 161, Issue 4
    • DOI: 10.1007/s00705-015-2728-0

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


    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

    VICTOR: genome-based phylogeny and classification of prokaryotic viruses
    journal, July 2017


    Molecular Bases and Role of Viruses in the Human Microbiome
    journal, November 2014


    IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes
    journal, November 2018

    • Paez-Espino, David; Roux, Simon; Chen, I-Min A.
    • Nucleic Acids Research, Vol. 47, Issue D1
    • DOI: 10.1093/nar/gky1127

    vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria
    journal, January 2017


    pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
    journal, October 2010

    • Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
    • BMC Bioinformatics, Vol. 11, Issue 1
    • DOI: 10.1186/1471-2105-11-538

    The human microbiome: at the interface of health and disease
    journal, March 2012

    • Cho, Ilseung; Blaser, Martin J.
    • Nature Reviews Genetics, Vol. 13, Issue 4
    • DOI: 10.1038/nrg3182

    Virus taxonomy in the age of metagenomics
    journal, January 2017

    • Simmonds, Peter; Adams, Mike J.; Benkő, Mária
    • Nature Reviews Microbiology, Vol. 15, Issue 3
    • DOI: 10.1038/nrmicro.2016.177

    ViPTree: the viral proteomic tree server
    journal, March 2017


    Real Time Classification of Viruses in 12 Dimensions
    journal, May 2013


    Bacteria-Phage Antagonistic Coevolution in Soil
    journal, March 2011


    Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
    journal, September 1997

    • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
    • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
    • DOI: 10.1093/nar/25.17.3389

    Single-virus genomics reveals hidden cosmopolitan and abundant viruses
    journal, June 2017

    • Martinez-Hernandez, Francisco; Fornas, Oscar; Lluesma Gomez, Monica
    • Nature Communications, Vol. 8, Issue 1
    • DOI: 10.1038/ncomms15892

    Host-linked soil viral ecology along a permafrost thaw gradient
    journal, July 2018


    Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
    journal, August 2014

    • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
    • Nature Reviews Microbiology, Vol. 12, Issue 9
    • DOI: 10.1038/nrmicro3330

    iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure
    journal, July 2016

    • Bolduc, Benjamin; Youens-Clark, Ken; Roux, Simon
    • The ISME Journal, Vol. 11, Issue 1
    • DOI: 10.1038/ismej.2016.89

    Virus-mediated archaeal hecatomb in the deep seafloor
    journal, October 2016

    • Danovaro, Roberto; Dell’Anno, Antonio; Corinaldesi, Cinzia
    • Science Advances, Vol. 2, Issue 10
    • DOI: 10.1126/sciadv.1600492