Gene sharing networks to automate genome-based prokaryotic viral taxonomy
Abstract
Viruses of bacteria and archaea impact natural, engineered and human ecosystems, but their study is hampered by the lack of a universal or scalable taxonomic framework. Furthermore we introduce vConTACT v2.0, a network-based application to establish prokaryotic virus taxonomy that scales to thousands of uncultivated virus genomes, and integrates distance-based hierarchical clustering and confidence scores for all taxonomic predictions. Performance tests demonstrated significant improvements over the original tool and near-identical (96%) correspondence to current International Committee on Taxonomy of Viruses (ICTV) viral taxonomy where genus-level assignments are available. Beyond these “known viruses”, vConTACT v2.0 suggested automatic genus assignments for 1,364 previously unclassified reference viruses, with perfectly scoring assignments submitted as new taxonomic proposals to ICTV. Scaling experiments with 15,280 global ocean large viral genome fragments demonstrated that the reference network was rapidly scalable and robust to adding large-scale viral metagenomic datasets. Together these efforts provide a critically-needed, systematically classified reference network and an accurate, scalable, and automatable taxonomic analysis tool.
- Authors:
-
[1];
[3];
[4];
[7];
[8];
[1]
- The Ohio State Univ., Columbus, OH (United States)
- National Institutes of Health, Fort Detrick, Frederick, MD (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Univ. of Liverpool, Liverpool (United Kingdom)
- National Inst. of Health (NIH), Bethesda, MD (United States)
- Univ. of Guelph, Guelph, ON (Canada)
- Inst. Pasteur, Paris (France)
- Univ. of the West of England, Bristol (United Kingdom)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1569046
- Grant/Contract Number:
- AC52-07NA27344
- 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; 54 ENVIRONMENTAL SCIENCES
Citation Formats
Jang, Ho Bin, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Turner, Dann, and Sullivan, Matthew B. Gene sharing networks to automate genome-based prokaryotic viral taxonomy. United States: N. p., 2019.
Web. doi:10.1101/533240.
Jang, Ho Bin, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Turner, Dann, & Sullivan, Matthew B. Gene sharing networks to automate genome-based prokaryotic viral taxonomy. United States. https://doi.org/10.1101/533240
Jang, Ho Bin, Bolduc, Benjamin, Zablocki, Olivier, Kuhn, Jens H., Roux, Simon, Adriaenssens, Evelien M., Brister, J. Rodney, Kropinski, Andrew M., Krupovic, Mart, Turner, Dann, and Sullivan, Matthew B. Tue .
"Gene sharing networks to automate genome-based prokaryotic viral taxonomy". United States. https://doi.org/10.1101/533240. https://www.osti.gov/servlets/purl/1569046.
@article{osti_1569046,
title = {Gene sharing networks to automate genome-based prokaryotic viral taxonomy},
author = {Jang, Ho Bin 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 Turner, Dann and Sullivan, Matthew B.},
abstractNote = {Viruses of bacteria and archaea impact natural, engineered and human ecosystems, but their study is hampered by the lack of a universal or scalable taxonomic framework. Furthermore we introduce vConTACT v2.0, a network-based application to establish prokaryotic virus taxonomy that scales to thousands of uncultivated virus genomes, and integrates distance-based hierarchical clustering and confidence scores for all taxonomic predictions. Performance tests demonstrated significant improvements over the original tool and near-identical (96%) correspondence to current International Committee on Taxonomy of Viruses (ICTV) viral taxonomy where genus-level assignments are available. Beyond these “known viruses”, vConTACT v2.0 suggested automatic genus assignments for 1,364 previously unclassified reference viruses, with perfectly scoring assignments submitted as new taxonomic proposals to ICTV. Scaling experiments with 15,280 global ocean large viral genome fragments demonstrated that the reference network was rapidly scalable and robust to adding large-scale viral metagenomic datasets. Together these efforts provide a critically-needed, systematically classified reference network and an accurate, scalable, and automatable taxonomic analysis tool.},
doi = {10.1101/533240},
journal = {Nature Biotechnology},
number = 6,
volume = 37,
place = {United States},
year = {2019},
month = {1}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Genome-based phylogeny of dsDNA viruses by a novel alignment-free method
journal, January 2012
- Gao, Yang; Luo, Liaofu
- Gene, Vol. 492, Issue 1
VICTOR: genome-based phylogeny and classification of prokaryotic viruses
journal, July 2017
- Meier-Kolthoff, Jan P.; Göker, Markus
- Bioinformatics, Vol. 33, Issue 21
Imbroglios of Viral Taxonomy: Genetic Exchange and Failings of Phenetic Approaches
journal, September 2002
- Lawrence, J. G.; Hatfull, G. F.; Hendrix, R. W.
- Journal of Bacteriology, Vol. 184, Issue 17
Visual Analysis of Dynamic Networks Using Change Centrality
conference, August 2012
- Federico, P.; Pfeffer, J.; Aigner, W.
- 2012 International Conference on Advances in Social Networks Analysis and Mining (ASONAM 2012), 2012 IEEE/ACM International Conference on Advances in Social Networks Analysis and Mining
Host-linked soil viral ecology along a permafrost thaw gradient
journal, July 2018
- Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R.
- Nature Microbiology, Vol. 3, Issue 8
Virus-mediated archaeal hecatomb in the deep seafloor
journal, October 2016
- Danovaro, Roberto; Dell’Anno, Antonio; Corinaldesi, Cinzia
- Science Advances, Vol. 2, Issue 10
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
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
Virus taxonomy in the age of metagenomics
journal, January 2017
- Simmonds, Peter; Adams, Mike J.; Benkő, Mária
- Nature Reviews Microbiology, Vol. 15, Issue 3
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
The Phage Proteomic Tree: a Genome-Based Taxonomy for Phage
journal, August 2002
- Rohwer, F.; Edwards, R.
- Journal of Bacteriology, Vol. 184, Issue 16
NCBI Viral Genomes Resource
journal, November 2014
- Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming
- Nucleic Acids Research, Vol. 43, Issue D1
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
Patterns and ecological drivers of ocean viral communities
journal, May 2015
- Brum, J. R.; Ignacio-Espinoza, J. C.; Roux, S.
- Science, Vol. 348, Issue 6237
Real Time Classification of Viruses in 12 Dimensions
journal, May 2013
- Yu, Chenglong; Hernandez, Troy; Zheng, Hui
- PLoS ONE, Vol. 8, Issue 5
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
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
journal, April 2014
- Zhao, Mengxin; Xue, Kai; Wang, Feng
- The ISME Journal, Vol. 8, Issue 10
The ‘Neglected’ Soil Virome – Potential Role and Impact
journal, August 2018
- Pratama, Akbar Adjie; van Elsas, Jan Dirk
- Trends in Microbiology, Vol. 26, Issue 8
Marine viruses — major players in the global ecosystem
journal, October 2007
- Suttle, Curtis A.
- Nature Reviews Microbiology, Vol. 5, Issue 10
Bacteriophage evolution differs by host, lifestyle and genome
journal, July 2017
- Mavrich, Travis N.; Hatfull, Graham F.
- Nature Microbiology, Vol. 2, Issue 9
Classification of Myoviridae bacteriophages using protein sequence similarity
journal, January 2009
- Lavigne, Rob; Darius, Paul; Summer, Elizabeth J.
- BMC Microbiology, Vol. 9, Issue 1
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
Putative archaeal viruses from the mesopelagic ocean
journal, January 2017
- Vik, Dean R.; Roux, Simon; Brum, Jennifer R.
- PeerJ, Vol. 5
Phage Taxonomy: We Agree To Disagree
journal, October 2004
- Nelson, D.
- Journal of Bacteriology, Vol. 186, Issue 21
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
Challenges in RNA virus bioinformatics
journal, March 2014
- Marz, Manja; Beerenwinkel, Niko; Drosten, Christian
- Bioinformatics, Vol. 30, Issue 13
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
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
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
Whole-genome prokaryotic phylogeny
journal, May 2004
- Henz, S. R.; Huson, D. H.; Auch, A. F.
- Bioinformatics, Vol. 21, Issue 10
Viral metabolic reprogramming in marine ecosystems
journal, June 2016
- Hurwitz, Bonnie L.; U’Ren, Jana M.
- Current Opinion in Microbiology, Vol. 31
Minimum Information about an Uncultivated Virus Genome (MIUViG)
journal, December 2018
- Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E.
- Nature Biotechnology, Vol. 37, Issue 1
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
Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity
journal, April 2015
- Pope, Welkin H.; Bowman, Charles A.; Russell, Daniel A.
- eLife, Vol. 4
Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements
journal, September 2016
- Iranzo, Jaime; Koonin, Eugene V.; Prangishvili, David
- Journal of Virology, Vol. 90, Issue 24
Fast and sensitive protein alignment using DIAMOND
journal, November 2014
- Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
- Nature Methods, Vol. 12, Issue 1
The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification
journal, February 2018
- Aiewsakun, Pakorn; Simmonds, Peter
- Microbiome, Vol. 6, Issue 1
Phage or foe: an insight into the impact of viral predation on microbial communities
journal, January 2018
- Fernández, Lucía; Rodríguez, Ana; García, Pilar
- The ISME Journal, Vol. 12, Issue 5
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
Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017)
journal, April 2017
- Adams, Michael J.; Lefkowitz, Elliot J.; King, Andrew M. Q.
- Archives of Virology, Vol. 162, Issue 8
The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing
journal, August 2016
- Iranzo, Jaime; Krupovic, Mart; Koonin, Eugene V.
- mBio, Vol. 7, Issue 4
Structure and function of the global ocean microbiome
journal, May 2015
- Sunagawa, S.; Coelho, L. P.; Chaffron, S.
- Science, Vol. 348, Issue 6237
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
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
Comparing the performance of biomedical clustering methods
journal, September 2015
- Wiwie, Christian; Baumbach, Jan; Röttger, Richard
- Nature Methods, Vol. 12, Issue 11
Unification of the Globally Distributed Spindle-Shaped Viruses of the Archaea
journal, December 2013
- Krupovic, M.; Quemin, E. R. J.; Bamford, D. H.
- Journal of Virology, Vol. 88, Issue 4
Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics
journal, October 2017
- Roux, Simon; Chan, Leong-Keat; Egan, Rob
- Nature Communications, Vol. 8, Issue 1
Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools
journal, June 2008
- Lavigne, Rob; Seto, Donald; Mahadevan, Padmanabhan
- Research in Microbiology, Vol. 159, Issue 5
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
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
Evaluation of clustering algorithms for protein-protein interaction networks
journal, November 2006
- Brohée, Sylvain; van Helden, Jacques
- BMC Bioinformatics, Vol. 7, Issue 1
ViPTree: the viral proteomic tree server
journal, March 2017
- Nishimura, Yosuke; Yoshida, Takashi; Kuronishi, Megumi
- Bioinformatics, Vol. 33, Issue 15
Molecular Bases and Role of Viruses in the Human Microbiome
journal, November 2014
- Abeles, Shira R.; Pride, David T.
- Journal of Molecular Biology, Vol. 426, Issue 23
Detecting overlapping protein complexes in protein-protein interaction networks
journal, March 2012
- Nepusz, Tamás; Yu, Haiyuan; Paccanaro, Alberto
- Nature Methods, Vol. 9, Issue 5
Horizontal Gene Transfer and the Evolution of Microvirid Coliphage Genomes
journal, January 2006
- Rokyta, D. R.; Burch, C. L.; Caudle, S. B.
- Journal of Bacteriology, Vol. 188, Issue 3
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
vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria
journal, January 2017
- Bolduc, Benjamin; Jang, Ho Bin; Doulcier, Guilhem
- PeerJ, Vol. 5
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
Python for Scientific Computing
journal, January 2007
- Oliphant, Travis E.
- Computing in Science & Engineering, Vol. 9, Issue 3
Bacteria-Phage Antagonistic Coevolution in Soil
journal, March 2011
- Gomez, P.; Buckling, A.
- Science, Vol. 332, Issue 6025
A structured annotation frame for the transposable phages: A new proposed family “Saltoviridae” within the Caudovirales
journal, March 2015
- Hulo, Chantal; Masson, Patrick; Le Mercier, Philippe
- Virology, Vol. 477
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
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
The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008
- Falkowski, P. G.; Fenchel, T.; Delong, E. F.
- Science, Vol. 320, Issue 5879
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
Viromes, Not Gene Markers, for Studying Double-Stranded DNA Virus Communities
journal, December 2014
- Sullivan, Matthew B.
- Journal of Virology, Vol. 89, Issue 5
Uncovering Earth’s virome
journal, August 2016
- Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
- Nature, Vol. 536, Issue 7617
Bacteriophages of Gordonia spp. Display a Spectrum of Diversity and Genetic Relationships
journal, August 2017
- Pope, Welkin H.; Mavrich, Travis N.; Garlena, Rebecca A.
- mBio, Vol. 8, Issue 4
The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’
journal, November 2009
- Sullivan, Matthew B.; Krastins, Bryan; Hughes, Jennifer L.
- Environmental Microbiology, Vol. 11, Issue 11
Lysogeny in nature: mechanisms, impact and ecology of temperate phages
journal, March 2017
- Howard-Varona, Cristina; Hargreaves, Katherine R.; Abedon, Stephen T.
- The ISME Journal, Vol. 11, Issue 7
Ménage à trois in the human gut: interactions between host, bacteria and phages
journal, May 2017
- Mirzaei, Mohammadali Khan; Maurice, Corinne F.
- Nature Reviews Microbiology, Vol. 15, Issue 7
NWChem: A comprehensive and scalable open-source solution for large scale molecular simulations
journal, September 2010
- Valiev, M.; Bylaska, E. J.; Govind, N.
- Computer Physics Communications, Vol. 181, Issue 9, p. 1477-1489
Works referencing / citing this record:
VIBRANT: Automated recovery, annotation and curation of microbial viruses, and evaluation of virome function from genomic sequences
posted_content, November 2019
- Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik
Prevalence of viral photosynthesis genes along a freshwater to saltwater transect in Southeast USA
journal, July 2019
- Ruiz‐Perez, Carlos A.; Tsementzi, Despina; Hatt, Janet K.
- Environmental Microbiology Reports, Vol. 11, Issue 5