Computational approaches to predict bacteriophage–host relationships

Edwards, Robert A.; McNair, Katelyn; Faust, Karoline; Raes, Jeroen; Dutilh, Bas E.

doi:10.1093/femsre/fuv048

Computational approaches to predict bacteriophage–host relationships

Journal Article · Wed Dec 09 00:00:00 EST 2015 · FEMS Microbiology Reviews

DOI:https://doi.org/10.1093/femsre/fuv048· OSTI ID:1625320

Edwards, Robert A. ^[1]; McNair, Katelyn ^[2]; Faust, Karoline ^[3]; Raes, Jeroen ^[4]; Dutilh, Bas E. ^[5]

San Diego State Univ., CA (United States). Dept. of Computer Science; Federal Univ. of Rio de Janeiro (Brazil). Dept. of Marine Biology, Institute of Biology; Argonne National Lab. (ANL), Argonne, IL (United States). Division of Mathematics and Computer Science; DOE/OSTI
San Diego State Univ., CA (United States). Dept. of Computer Science
Rega Institute KU Leuven, Leuven (Belgium). Dept. of Microbiology and Immunology; VIB Center for the Biology of Disease, Leuven (Belgium); rije Universiteit Brussel, Pleinlaan, Brussels (Belgium). Laboratory of Microbiology
Rega Institute KU Leuven, Leuven (Belgium). Dept. of Microbiology and Immunology; VIB Center for the Biology of Disease, Leuven (Belgium); rije Universiteit Brussel, Pleinlaan, Brussels (Belgium). Laboratory of Microbiology
Federal Univ. of Rio de Janeiro (Brazil). Dept. of Marine Biology, Institute of Biology; Univ. of Utrecht (Netherlands). Theoretical Biology and Bioinformatics; Radboud Univ., Medical Center, Nijmegen (Netherlands). Centre for Molecular and Biomolecular Informatics, Radboud Institute for Molecular Life Sciences

Metagenomics has changed the face of virus discovery by enabling the accurate identification of viral genome sequences without requiring isolation of the viruses. As a result, metagenomic virus discovery leaves the first and most fundamental question about any novel virus unanswered: What host does the virus infect? The diversity of the global virosphere and the volumes of data obtained in metagenomic sequencing projects demand computational tools for virus–host prediction. We focus on bacteriophages (phages, viruses that infect bacteria), the most abundant and diverse group of viruses found in environmental metagenomes. By analyzing 820 phages with annotated hosts, we review and assess the predictive power of in silico phage–host signals. Sequence homology approaches are the most effective at identifying known phage–host pairs. Compositional and abundance-based methods contain significant signal for phage–host classification, providing opportunities for analyzing the unknowns in viral metagenomes. Together, these computational approaches further our knowledge of the interactions between phages and their hosts. Importantly, we find that all reviewed signals significantly link phages to their hosts, illustrating how current knowledge and insights about the interaction mechanisms and ecology of coevolving phages and bacteria can be exploited to predict phage–host relationships, with potential relevance for medical and industrial applications.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Science Foundation (NSF); Netherlands Organization for Scientific Research (NWO); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1625320

Journal Information:: FEMS Microbiology Reviews, Journal Name: FEMS Microbiology Reviews Journal Issue: 2 Vol. 40; ISSN 1574-6976

Publisher:: Federation of European Microbiological SocietiesCopyright Statement

Country of Publication:: United States

Language:: English

References (127)

From cultured to uncultured genome sequences: metagenomics and modeling microbial ecosystems Garza, Daniel R.; Dutilh, Bas E. Cellular and Molecular Life Sciences, Vol. 72, Issue 22 https://doi.org/10.1007/s00018-015-2004-1	journal	August 2015
Influenza Virus Evolution, Host Adaptation, and Pandemic Formation Taubenberger, Jeffery K.; Kash, John C. Cell Host & Microbe, Vol. 7, Issue 6 https://doi.org/10.1016/j.chom.2010.05.009	journal	June 2010
Metagenomics and future perspectives in virus discovery Mokili, John L.; Rohwer, Forest; Dutilh, Bas E. Current Opinion in Virology, Vol. 2, Issue 1 https://doi.org/10.1016/j.coviro.2011.12.004	journal	February 2012
Bacteriophage–host interaction: from splendid isolation into a messy reality Brüssow, Harald Current Opinion in Microbiology, Vol. 16, Issue 4 https://doi.org/10.1016/j.mib.2013.04.007	journal	August 2013
Phage–bacteria infection networks Weitz, Joshua S.; Poisot, Timothée; Meyer, Justin R. Trends in Microbiology, Vol. 21, Issue 2 https://doi.org/10.1016/j.tim.2012.11.003	journal	February 2013
Virus discovery: are we scientists or genome collectors? Canuti, Marta; van der Hoek, Lia Trends in Microbiology, Vol. 22, Issue 5 https://doi.org/10.1016/j.tim.2014.02.004	journal	May 2014
Safety analysis of a Russian phage cocktail: From MetaGenomic analysis to oral application in healthy human subjects McCallin, Shawna; Alam Sarker, Shafiqul; Barretto, Caroline Virology, Vol. 443, Issue 2 https://doi.org/10.1016/j.virol.2013.05.022	journal	September 2013
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
Comparative genomics of closely related salmonellae Edwards, Robert A.; Olsen, Gary J.; Maloy, Stanley R. Trends in Microbiology, Vol. 10, Issue 2 https://doi.org/10.1016/s0966-842x(01)02293-4	journal	February 2002
The human microbiome: there is much left to do Ley, Ruth Nature, Vol. 606, Issue 7914 https://doi.org/10.1038/d41586-022-01610-5	journal	June 2022
Viral and microbial community dynamics in four aquatic environments Rodriguez-Brito, Beltran; Li, LinLin; Wegley, Linda The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2010.1	journal	February 2010
Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists Chow, Cheryl-Emiliane T.; Kim, Diane Y.; Sachdeva, Rohan The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.199	journal	November 2013
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes Hingamp, Pascal; Grimsley, Nigel; Acinas, Silvia G. The ISME Journal, Vol. 7, Issue 9 https://doi.org/10.1038/ismej.2013.59	journal	April 2013
Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton Labonté, Jessica M.; Swan, Brandon K.; Poulos, Bonnie The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.48	journal	April 2015
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08656	journal	December 2009
Viral tagging reveals discrete populations in Synechococcus viral genome sequence space Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C. Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13459	journal	July 2014
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes Dutilh, Bas E.; Cassman, Noriko; McNair, Katelyn Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5498	journal	July 2014
Recent advances in genomic DNA sequencing of microbial species from single cells Lasken, Roger S.; McLean, Jeffrey S. Nature Reviews Genetics, Vol. 15, Issue 9 https://doi.org/10.1038/nrg3785	journal	August 2014
Bacteriophage resistance mechanisms Labrie, Simon J.; Samson, Julie E.; Moineau, Sylvain Nature Reviews Microbiology, Vol. 8, Issue 5 https://doi.org/10.1038/nrmicro2315	journal	March 2010
Site-specific recombination by φC31 integrase and other large serine recombinases Smith, Margaret C. M.; Brown, William R. A.; McEwan, Andrew R. Biochemical Society Transactions, Vol. 38, Issue 2 https://doi.org/10.1042/bst0380388	journal	March 2010
Rapid evolution of the human gut virome Minot, S.; Bryson, A.; Chehoud, C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 30 https://doi.org/10.1073/pnas.1300833110	journal	July 2013
Bacteria-Phage Interactions across Time and Space: Merging Local Adaptation and Time-Shift Experiments to Understand Phage Evolution Koskella, Britt The American Naturalist, Vol. 184, Issue S1 https://doi.org/10.1086/676888	journal	August 2014
Prophinder: a computational tool for prophage prediction in prokaryotic genomes Lima-Mendez, Gipsi; Van Helden, Jacques; Toussaint, Ariane Bioinformatics, Vol. 24, Issue 6 https://doi.org/10.1093/bioinformatics/btn043	journal	January 2008
CRISPI: a CRISPR interactive database Rousseau, C.; Gonnet, M.; Le Romancer, M. Bioinformatics, Vol. 25, Issue 24 https://doi.org/10.1093/bioinformatics/btp586	journal	October 2009
Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies Williams, K. P. Nucleic Acids Research, Vol. 30, Issue 4 https://doi.org/10.1093/nar/30.4.866	journal	February 2002
NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy Pruitt, K. D.; Tatusova, T.; Brown, G. R. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1079	journal	November 2011
PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies Akhter, Sajia; Aziz, Ramy K.; Edwards, Robert A. Nucleic Acids Research, Vol. 40, Issue 16 https://doi.org/10.1093/nar/gks406	journal	May 2012
Molecular evolution of bacteriophages: evidence of selection against the recognition sites of host restriction enzymes. Sharp, P. M. Molecular Biology and Evolution https://doi.org/10.1093/oxfordjournals.molbev.a040377	journal	January 1986
Coevolutionary diversification creates nested-modular structure in phage–bacteria interaction networks Beckett, Stephen J.; Williams, Hywel T. P. Interface Focus, Vol. 3, Issue 6 https://doi.org/10.1098/rsfs.2013.0033	journal	December 2013
Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time Pride, D. T.; Sun, C. L.; Salzman, J. Genome Research, Vol. 21, Issue 1 https://doi.org/10.1101/gr.111732.110	journal	December 2010
The human gut virome: Inter-individual variation and dynamic response to diet Minot, S.; Sinha, R.; Chen, J. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.122705.111	journal	August 2011
Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses: phageFISH - visualizing intracellular and free viruses Allers, Elke; Moraru, Cristina; Duhaime, Melissa B. Environmental Microbiology, Vol. 15, Issue 8 https://doi.org/10.1111/1462-2920.12100	journal	March 2013
The cost of phage resistance in a plant pathogenic bacterium is context‐dependent Meaden, Sean; Paszkiewicz, Konrad; Koskella, Britt Evolution, Vol. 69, Issue 5 https://doi.org/10.1111/evo.12652	journal	April 2015
Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses Tyson, Gene W.; Banfield, Jillian F. Environmental Microbiology, Vol. 0, Issue 0 https://doi.org/10.1111/j.1462-2920.2007.01444.x	journal	September 2007
Virus Population Dynamics and Acquired Virus Resistance in Natural Microbial Communities Andersson, A. F.; Banfield, J. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1157358	journal	May 2008
CRISPR/Cas, the Immune System of Bacteria and Archaea Horvath, Philippe; Barrangou, Rodolphe Science, Vol. 327, Issue 5962 https://doi.org/10.1126/science.1179555	journal	January 2010
Patterns and ecological drivers of ocean viral communities Brum, J. R.; Ignacio-Espinoza, J. C.; Roux, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261498	journal	May 2015
Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria Pernthaler, A.; Pernthaler, J.; Amann, R. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/aem.68.6.3094-3101.2002	journal	June 2002
Characterization of the Integrase Gene and Attachment Site for the Myxococcus xanthus Bacteriophage Mx9 Julien, Bryan Journal of Bacteriology, Vol. 185, Issue 21 https://doi.org/10.1128/jb.185.21.6325-6330.2003	journal	November 2003
Host Controlled Variation in Bacterial Viruses1 Bertani, G.; Weigle, J. J. Journal of Bacteriology, Vol. 65, Issue 2 https://doi.org/10.1128/jb.65.2.113-121.1953	journal	January 1953
Contrasting Life Strategies of Viruses That Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging Deng, Li; Gregory, Ann; Yilmaz, Suzan mBio, Vol. 4, Issue 1 https://doi.org/10.1128/mbio.00516-12	journal	March 2013
The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats Grissa, Ibtissem; Vergnaud, Gilles; Pourcel, Christine BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-172	journal	January 2007
CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats Bland, Charles; Ramsey, Teresa L.; Sabree, Fareedah BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-209	journal	June 2007
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Phageâ€“host interplay: examples from tailed phages and Gram-negative bacterial pathogens Chaturongakul, Soraya; Ounjai, Puey Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00442	journal	August 2014
Development of a high throughput assay for indirectly measuring phage growth using the OmniLog ^TM system Henry, Matthew; Biswas, Biswajit; Vincent, Leah Bacteriophage, Vol. 2, Issue 3 https://doi.org/10.4161/bact.21440	journal	July 2012
CRISPRTarget: Bioinformatic prediction and analysis of crRNA targets Biswas, Ambarish; Gagnon, Joshua N.; Brouns, Stan J. J. RNA Biology, Vol. 10, Issue 5 https://doi.org/10.4161/rna.24046	journal	February 2013
Strain- and plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products Beitel, Christopher W.; Froenicke, Lutz; Lang, Jenna M. https://doi.org/10.7287/peerj.preprints.260v1	preprint	February 2014
Gene swapping in the dead zone Petersen, Jillian; Dubilier, Nicole eLife, Vol. 3 https://doi.org/10.7554/elife.04600	journal	October 2014
FOCUS: an alignment-free model to identify organisms in metagenomes using non-negative least squares Silva, Genivaldo Gueiros Z.; Cuevas, Daniel A.; Dutilh, Bas E. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.425	journal	January 2014
VirSorter: mining viral signal from microbial genomic data Roux, Simon; Enault, Francois; Hurwitz, Bonnie L. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.985	journal	January 2015
Basic Local Alignment Search Tool Altschul, S. Journal of Molecular Biology, Vol. 215, Issue 3 https://doi.org/10.1006/jmbi.1990.9999	journal	October 1990
Distribution and Mechanism of the Type I CRISPR-Cas Systems Staals, Raymond H. J.; Brouns, Stan J. J. CRISPR-Cas Systems https://doi.org/10.1007/978-3-662-45794-8_6	book	December 2012
Amelioration of Bacterial Genomes: Rates of Change and Exchange Lawrence, Jeffrey G.; Ochman, Howard Journal of Molecular Evolution, Vol. 44, Issue 4 https://doi.org/10.1007/PL00006158	journal	April 1997
Effects of Plants on Metacommunities and Correlation Networks of Soil Microbial Groups in an Ecologically Restored Wetland Jeong, So-Yeon; Kim, Tae Gwan Microbial Ecology, Vol. 81, Issue 3 https://doi.org/10.1007/s00248-020-01625-3	journal	October 2020
Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium Ebel-Tsipis, Judith; Botstein, David Virology, Vol. 45, Issue 3 https://doi.org/10.1016/0042-6822(71)90177-2	journal	September 1971
Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium Susskind, Miriam M.; Wright, Andrew; Botstein, David Virology, Vol. 45, Issue 3 https://doi.org/10.1016/0042-6822(71)90178-4	journal	September 1971
Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium Susskind, Miriam M.; Botstein, David; Wright, Andrew Virology, Vol. 62, Issue 2 https://doi.org/10.1016/0042-6822(74)90398-5	journal	December 1974
Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium Susskind, Miriam M.; Wright, Andrew; Botstein, David Virology, Vol. 62, Issue 2 https://doi.org/10.1016/0042-6822(74)90399-7	journal	December 1974
Comparative genomics of closely related salmonellae Edwards, Robert A.; Olsen, Gary J.; Maloy, Stanley R. Trends in Microbiology, Vol. 10, Issue 2 https://doi.org/10.1016/S0966-842X(01)02293-4	journal	February 2002
Mechanisms of multi-strain coexistence in host–phage systems with nested infection networks Jover, Luis F.; Cortez, Michael H.; Weitz, Joshua S. Journal of Theoretical Biology, Vol. 332 https://doi.org/10.1016/j.jtbi.2013.04.011	journal	September 2013
Invertible DNA determines host specificity of bacteriophage Mu van de Putte, Pieter; Cramer, Steve; Giphart-Gassler, Micheline Nature, Vol. 286, Issue 5770 https://doi.org/10.1038/286218a0	journal	July 1980
Comparative metagenomics of microbial traits within oceanic viral communities Sharon, Itai; Battchikova, Natalia; Aro, Eva-Mari The ISME Journal, Vol. 5, Issue 7 https://doi.org/10.1038/ismej.2011.2	journal	February 2011
Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages Flores, Cesar O.; Valverde, Sergi; Weitz, Joshua S. The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.135	journal	November 2012
Short-term observations of marine bacterial and viral communities: patterns, connections and resilience Needham, David M.; Chow, Cheryl-Emiliane T.; Cram, Jacob A. The ISME Journal, Vol. 7, Issue 7 https://doi.org/10.1038/ismej.2013.19	journal	February 2013
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus Sullivan, Matthew B.; Waterbury, John B.; Chisholm, Sallie W. Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01929	journal	August 2003
Structure, function and diversity of the healthy human microbiome No authors listed Nature, Vol. 486, Issue 7402, p. 207-214 https://doi.org/10.1038/nature11234	journal	June 2012
Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome Modi, Sheetal R.; Lee, Henry H.; Spina, Catherine S. Nature, Vol. 499, Issue 7457 https://doi.org/10.1038/nature12212	journal	June 2013
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes Nielsen, H. Bjørn; Almeida, Mathieu; Juncker, Agnieszka Sierakowska Nature Biotechnology, Vol. 32, Issue 8 https://doi.org/10.1038/nbt.2939	journal	July 2014
Genome signature-based dissection of human gut metagenomes to extract subliminal viral sequences Ogilvie, Lesley A.; Bowler, Lucas D.; Caplin, Jonathan Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3420	journal	September 2013
Explaining microbial population genomics through phage predation Rodriguez-Valera, Francisco; Martín-Cuadrado, Ana-Belén; Rodriguez-Brito, Beltrán Nature Precedings https://doi.org/10.1038/npre.2009.3489.1	journal	July 2009
Viral metagenomics Edwards, Robert A.; Rohwer, Forest Nature Reviews Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/nrmicro1163	journal	May 2005
Explaining microbial population genomics through phage predation Rodriguez-Valera, Francisco; Martin-Cuadrado, Ana-Belen; Rodriguez-Brito, Beltran Nature Reviews Microbiology, Vol. 7, Issue 11 https://doi.org/10.1038/nrmicro2235	journal	November 2009
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander Song, Xiaoming; Nie, Fulei; Chen, Wei Horticulture Research, Vol. 7, Issue 1 https://doi.org/10.1038/s41438-020-0261-0	journal	April 2020
Site-specific recombination by φC31 integrase and other large serine recombinases Smith, Margaret C. M.; Brown, William R. A.; McEwan, Andrew R. Biochemical Society Transactions, Vol. 38, Issue 2 https://doi.org/10.1042/BST0380388	journal	March 2010
Diversity in the serine recombinases: Diversity in the serine recombinases Smith, Margaret C. M.; Thorpe, Helena M. Molecular Microbiology, Vol. 44, Issue 2 https://doi.org/10.1046/j.1365-2958.2002.02891.x	journal	April 2002
Statistical structure of host-phage interactions Flores, C. O.; Meyer, J. R.; Valverde, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 28 https://doi.org/10.1073/pnas.1101595108	journal	June 2011
Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut Reyes, A.; Wu, M.; McNulty, N. P. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1319470110	journal	November 2013
Degenerate target sites mediate rapid primed CRISPR adaptation Fineran, P. C.; Gerritzen, M. J. H.; Suarez-Diez, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1400071111	journal	April 2014
Structure of the lambda att sites generated by int-dependent deletions. Hoess, R. H.; Landy, A. Proceedings of the National Academy of Sciences, Vol. 75, Issue 11 https://doi.org/10.1073/pnas.75.11.5437	journal	November 1978
A Greedy Algorithm for Aligning DNA Sequences Zhang, Zheng; Schwartz, Scott; Wagner, Lukas Journal of Computational Biology, Vol. 7, Issue 1-2 https://doi.org/10.1089/10665270050081478	journal	February 2000
PILER: identification and classification of genomic repeats Edgar, R. C.; Myers, E. W. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1003	journal	June 2005
A fast, lock-free approach for efficient parallel counting of occurrences of k-mers Marçais, Guillaume; Kingsford, Carl Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr011	journal	January 2011
Reference-independent comparative metagenomics using cross-assembly: crAss Dutilh, Bas E.; Schmieder, Robert; Nulton, Jim Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts613	journal	October 2012
Linking environmental prokaryotic viruses and their host through CRISPRs Sanguino, Laura; Franqueville, Laure; Vogel, Timothy M. FEMS Microbiology Ecology, Vol. 91, Issue 5 https://doi.org/10.1093/femsec/fiv046	journal	May 2015
Genetic Studies of Lysogenicity in Escherichia coli Lederberg, Esther M.; Lederberg, Joshua Genetics, Vol. 38, Issue 1 https://doi.org/10.1093/genetics/38.1.51	journal	January 1953
Codon usage in bacteria: correlation with gene expressivity Gouy, M.; Gautier, C. Nucleic Acids Research, Vol. 10, Issue 22 https://doi.org/10.1093/nar/10.22.7055	journal	January 1982
Phage_Finder: Automated identification and classification of prophage regions in complete bacterial genome sequences Fouts, Derrick E. Nucleic Acids Research, Vol. 34, Issue 20 https://doi.org/10.1093/nar/gkl732	journal	October 2006
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats Grissa, I.; Vergnaud, G.; Pourcel, C. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm360	journal	May 2007
CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome Stern, A.; Mick, E.; Tirosh, I. Genome Research, Vol. 22, Issue 10 https://doi.org/10.1101/gr.138297.112	journal	June 2012
Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome: Rumen viral metagenome Berg Miller, Margret E.; Yeoman, Carl J.; Chia, Nicholas Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02593.x	journal	October 2011
Oxygen minimum zones harbour novel viral communities with low diversity: Viral community characteristics of an oxygen minimum zone Cassman, Noriko; Prieto-Davó, Alejandra; Walsh, Kevin Environmental Microbiology, Vol. 14, Issue 11 https://doi.org/10.1111/j.1462-2920.2012.02891.x	journal	October 2012
Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage: CRISPR spacers reveal hosts of marine vent viral assemblage Anderson, Rika E.; Brazelton, William J.; Baross, John A. FEMS Microbiology Ecology, Vol. 77, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01090.x	journal	April 2011
Reverse Transcriptase-Mediated Tropism Switching in Bordetella Bacteriophage Liu, M. Science, Vol. 295, Issue 5562 https://doi.org/10.1126/science.1067467	journal	March 2002
CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes Barrangou, R.; Fremaux, C.; Deveau, H. Science, Vol. 315, Issue 5819 https://doi.org/10.1126/science.1138140	journal	March 2007
Probing Individual Environmental Bacteria for Viruses by Using Microfluidic Digital PCR Tadmor, A. D.; Ottesen, E. A.; Leadbetter, J. R. Science, Vol. 333, Issue 6038 https://doi.org/10.1126/science.1200758	journal	June 2011
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
Reconstruction of Novel Cyanobacterial Siphovirus Genomes from Mediterranean Metagenomic Fosmids Mizuno, Carolina Megumi; Rodriguez-Valera, Francisco; Garcia-Heredia, Inmaculada Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/AEM.02742-12	journal	November 2012
Characterization of the ELPhiS Prophage from Salmonella enterica Serovar Enteritidis Strain LK5 Hanna, L. Farris; Matthews, T. David; Dinsdale, Elizabeth A. Applied and Environmental Microbiology, Vol. 78, Issue 6 https://doi.org/10.1128/AEM.07241-11	journal	January 2012
Prevalence of Broad-Host-Range Lytic Bacteriophages of Sphaerotilus natans, Escherichia coli, andPseudomonas aeruginosa Jensen, Ellen C.; Schrader, Holly S.; Rieland, Brenda Applied and Environmental Microbiology, Vol. 64, Issue 2 https://doi.org/10.1128/AEM.64.2.575-580.1998	journal	February 1998
Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria Pernthaler, A.; Pernthaler, J.; Amann, R. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/AEM.68.6.3094-3101.2002	journal	June 2002
A Broad-Host-Range, Generalized Transducing Phage (SN-T) Acquires 16S rRNA Genes from Different Genera of Bacteria Beumer, Amy; Robinson, Jayne B. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8301-8304.2005	journal	December 2005
Characterization of the Integrase Gene and Attachment Site for the Myxococcus xanthus Bacteriophage Mx9 Julien, Bryan Journal of Bacteriology, Vol. 185, Issue 21 https://doi.org/10.1128/JB.185.21.6325-6330.2003	journal	November 2003
Host Controlled Variation in Bacterial Viruses1 Bertani, G.; Weigle, J. J. Journal of Bacteriology, Vol. 65, Issue 2 https://doi.org/10.1128/JB.65.2.113-121.1953	journal	January 1953
Characteristics of PRD1, a Plasmid-Dependent Broad Host Range DNA Bacteriophage Olsen, Ronald H.; Siak, June-Sang; Gray, Robert H. Journal of Virology, Vol. 14, Issue 3 https://doi.org/10.1128/JVI.14.3.689-699.1974	journal	January 1974
Complete Genome Sequence of Bacillus thuringiensis subsp. kurstaki Strain HD73 Liu, G.; Song, L.; Shu, C. Genome Announcements, Vol. 1, Issue 2 https://doi.org/10.1128/genomeA.00080-13	journal	February 2013
Contrasting Life Strategies of Viruses that Infect Photo- and Heterotrophic Bacteria, as Revealed by Viral Tagging Deng, Li; Gregory, Ann; Yilmaz, Suzan mBio, Vol. 3, Issue 6 https://doi.org/10.1128/mBio.00373-12	journal	October 2012
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
PhiSiGns: an online tool to identify signature genes in phages and design PCR primers for examining phage diversity Dwivedi, Bhakti; Schmieder, Robert; Goldsmith, Dawn B. BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-37	journal	March 2012
Use of Fluorescently Labeled Phage in the Detection and Identification of Bacterial Species Mosier-Boss, P. A.; Lieberman, S. H.; Andrews, J. M. Applied Spectroscopy, Vol. 57, Issue 9 https://doi.org/10.1366/00037020360696008	journal	September 2003
Expanding the Marine Virosphere Using Metagenomics Mizuno, Carolina Megumi; Rodriguez-Valera, Francisco; Kimes, Nikole E. PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1003987	journal	December 2013
The Sorcerer II Global Ocean Sampling Expedition: Metagenomic Characterization of Viruses within Aquatic Microbial Samples Williamson, Shannon J.; Rusch, Douglas B.; Yooseph, Shibu PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001456	journal	January 2008
The Molecular and Genetic Basis of Repeatable Coevolution between Escherichia coli and Bacteriophage T3 in a Laboratory Microcosm Perry, Elizabeth B.; Barrick, Jeffrey E.; Bohannan, Brendan J. M. PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0130639	journal	June 2015
Species-Level Deconvolution of Metagenome Assemblies with Hi-C–Based Contact Probability Maps Burton, Joshua N.; Liachko, Ivan; Dunham, Maitreya J. G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 7 https://doi.org/10.1534/g3.114.011825	journal	May 2014
Increasing DNA Transfer Efficiency by Temporary Inactivation of Host Restriction Edwards, Robert A.; Helm, R. Allen; Maloy, Stanley R. BioTechniques, Vol. 26, Issue 5 https://doi.org/10.2144/99265st02	journal	May 1999
Beyond research: a primer for considerations on using viral metagenomics in the field and clinic Hall, Richard J.; Draper, Jenny L.; Nielsen, Fiona G. G. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00224	journal	March 2015
Structural Aspects of the Interaction of Dairy Phages with Their Host Bacteria Mahony, Jennifer; van Sinderen, Douwe Viruses, Vol. 4, Issue 9 https://doi.org/10.3390/v4091410	journal	August 2012
Understanding Bacteriophage Specificity in Natural Microbial Communities Koskella, Britt; Meaden, Sean Viruses, Vol. 5, Issue 3 https://doi.org/10.3390/v5030806	journal	March 2013
Metagenomic ventures into outer sequence space Dutilh, Bas E. Bacteriophage, Vol. 4, Issue 4 https://doi.org/10.4161/21597081.2014.979664	journal	December 2014
Exploring the Vast Diversity of Marine Viruses Breitbart, Mya; Thompson, Luke; Suttle, Curtis Oceanography, Vol. 20, Issue 2 https://doi.org/10.5670/oceanog.2007.58	journal	June 2007
Strain- and plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products Beitel, Christopher W.; Froenicke, Lutz; Lang, Jenna M. https://doi.org/10.7287/peerj.preprints.260	preprint	February 2014
Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics Roux, Simon; Hawley, Alyse K.; Torres Beltran, Monica eLife, Vol. 3 https://doi.org/10.7554/eLife.03125	journal	August 2014
Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms Marbouty, Martial; Cournac, Axel; Flot, Jean-François eLife, Vol. 3 https://doi.org/10.7554/eLife.03318	journal	December 2014
Viral dark matter and virus–host interactions resolved from publicly available microbial genomes Roux, Simon; Hallam, Steven J.; Woyke, Tanja eLife, Vol. 4 https://doi.org/10.7554/eLife.08490	journal	July 2015
Strain- and plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products Beitel, Christopher W.; Froenicke, Lutz; Lang, Jenna M. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.415	journal	January 2014

Cited By (84)

Minimum Information about an Uncultivated Virus Genome (MIUViG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. Nature Biotechnology, Vol. 37, Issue 1 https://doi.org/10.1038/nbt.4306	journal	December 2018
Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans Coutinho, Felipe H.; Silveira, Cynthia B.; Gregoracci, Gustavo B. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15955	journal	July 2017
CRISPR analysis suggests that small circular single-stranded DNA smacoviruses infect Archaea instead of humans Díez-Villaseñor, César; Rodriguez-Valera, Francisco Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08167-w	journal	January 2019
Reply to: Caution in inferring viral strategies from abundance correlations in marine metagenomes Coutinho, F. H.; Silveira, C. B.; Gregoracci, G. B. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08286-4	journal	January 2019
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Murine colitis reveals a disease-associated bacteriophage community Duerkop, Breck A.; Kleiner, Manuel; Paez-Espino, David Nature Microbiology, Vol. 3, Issue 9 https://doi.org/10.1038/s41564-018-0210-y	journal	July 2018
WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs Galiez, Clovis; Siebert, Matthias; Enault, François Bioinformatics, Vol. 33, Issue 19 https://doi.org/10.1093/bioinformatics/btx383	journal	July 2017
PPR-Meta: a tool for identifying phages and plasmids from metagenomic fragments using deep learning Fang, Zhencheng; Tan, Jie; Wu, Shufang GigaScience, Vol. 8, Issue 6 https://doi.org/10.1093/gigascience/giz066	journal	June 2019
Alignment-free $d_2^*$ oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences Ahlgren, Nathan A.; Ren, Jie; Lu, Yang Young Nucleic Acids Research, Vol. 45, Issue 1 https://doi.org/10.1093/nar/gkw1002	journal	November 2016
Interpretable detection of novel human viruses from genome sequencing data Bartoszewicz, Jakub M.; Seidel, Anja; Renard, Bernhard Y. NAR Genomics and Bioinformatics, Vol. 3, Issue 1 https://doi.org/10.1093/nargab/lqab004	journal	February 2021
Genomic and Seasonal Variations among Aquatic Phages Infecting the Baltic Sea Gammaproteobacterium Rheinheimera sp. Strain BAL341 Nilsson, E.; Li, K.; Fridlund, J. Applied and Environmental Microbiology, Vol. 85, Issue 18 https://doi.org/10.1128/aem.01003-19	journal	July 2019
Genomes of Abundant and Widespread Viruses from the Deep Ocean Mizuno, Carolina Megumi; Ghai, Rohit; Saghaï, Aurélien mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mbio.00805-16	journal	July 2016
Limitations of Correlation-Based Inference in Complex Virus-Microbe Communities Coenen, Ashley R.; Weitz, Joshua S. mSystems, Vol. 3, Issue 4 https://doi.org/10.1128/msystems.00084-18	journal	August 2018
A Viral Ecogenomics Framework To Uncover the Secrets of Nature’s “Microbe Whisperers” Roux, Simon mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00111-19	journal	May 2019
Computational prediction of inter-species relationships through omics data analysis and machine learning Leite, Diogo Manuel Carvalho; Brochet, Xavier; Resch, Grégory BMC Bioinformatics, Vol. 19, Issue S14 https://doi.org/10.1186/s12859-018-2388-7	journal	November 2018
Alignment-free genomic sequence comparison using FCGR and signal processing Lichtblau, Daniel BMC Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1186/s12859-019-3330-3	journal	December 2019
Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes Silveira, Cynthia B.; Coutinho, Felipe H.; Cavalcanti, Giselle S. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6523-2	journal	February 2020
Diversities and potential biogeochemical impacts of mangrove soil viruses Jin, Min; Guo, Xun; Zhang, Rui Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0675-9	journal	April 2019
Long-read metagenomic exploration of extrachromosomal mobile genetic elements in the human gut Suzuki, Yoshihiko; Nishijima, Suguru; Furuta, Yoshikazu Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0737-z	journal	August 2019
Correction to: Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00828-7	journal	March 2020
MARVEL, a Tool for Prediction of Bacteriophage Sequences in Metagenomic Bins Amgarten, Deyvid; Braga, Lucas P. P.; da Silva, Aline M. Frontiers in Genetics, Vol. 9 https://doi.org/10.3389/fgene.2018.00304	journal	August 2018
Ultrastructure and Viral Metagenome of Bacteriophages from an Anaerobic Methane Oxidizing Methylomirabilis Bioreactor Enrichment Culture Gambelli, Lavinia; Cremers, Geert; Mesman, Rob Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01740	journal	November 2016
Insights of Phage-Host Interaction in Hypersaline Ecosystem through Metagenomics Analyses Motlagh, Amir Mohaghegh; Bhattacharjee, Ananda S.; Coutinho, Felipe H. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00352	journal	March 2017
Intriguing Interaction of Bacteriophage-Host Association: An Understanding in the Era of Omics Parmar, Krupa M.; Gaikwad, Saurabh L.; Dhakephalkar, Prashant K. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00559	journal	April 2017
Evolutionary History of Bacteriophages in the Genus Paraburkholderia Pratama, Akbar Adjie; Chaib De Mares, Maryam; van Elsas, Jan Dirk Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00835	journal	May 2018
Comprehensive Insights Into Composition, Metabolic Potentials, and Interactions Among Archaeal, Bacterial, and Viral Assemblages in Meromictic Lake Shunet in Siberia Wu, Yu-Ting; Yang, Cheng-Yu; Chiang, Pei-Wen Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01763	journal	August 2018
Phages for Phage Therapy: Isolation, Characterization, and Host Range Breadth Hyman, Paul Pharmaceuticals, Vol. 12, Issue 1 https://doi.org/10.3390/ph12010035	journal	March 2019
Phages and Human Health: More Than Idle Hitchhikers No authors listed Viruses, Vol. 11, Issue 7 https://doi.org/10.3390/v11070587	journal	June 2019
A Protocol for Extraction of Infective Viromes Suitable for Metagenomics Sequencing from Low Volume Fecal Samples Deng, Ling; Silins, Ronalds; Castro-Mejía, Josué L. Viruses, Vol. 11, Issue 7 https://doi.org/10.3390/v11070667	journal	July 2019
“French Phage Network”—Second Meeting Report Torres-Barceló, Clara; Kaltz, Oliver; Froissart, Rémy Viruses, Vol. 9, Issue 4 https://doi.org/10.3390/v9040087	journal	April 2017
The Human Gut Phage Community and Its Implications for Health and Disease Manrique, Pilar; Dills, Michael; Young, Mark Viruses, Vol. 9, Issue 6 https://doi.org/10.3390/v9060141	journal	June 2017
Additional file 1 of Comparative genomic analysis of five freshwater cyanophages and reference-guided metagenomic data mining Du, Kang; Yang, Feng; Zhang, Jun-Tao figshare https://doi.org/10.6084/m9.figshare.20501957	dataset	January 2022
Additional file 1 of A compendium of ruminant gastrointestinal phage genomes revealed a higher proportion of lytic phages than in any other environments Wu, Yingjian; Gao, Na; Sun, Chuqing figshare https://doi.org/10.6084/m9.figshare.25547037	dataset	January 2024
MetaCRAST: Reference-guided extraction of CRISPR spacers from unassembled metagenomes Moller, Abraham G.; Liang, Chun https://doi.org/10.7287/peerj.preprints.2278v4	preprint	August 2017
Determining virus-host interactions and glycerol metabolism profiles in geographically diverse solar salterns with metagenomics Moller, Abraham G.; Liang, Chun PeerJ, Vol. 5 https://doi.org/10.7717/peerj.2844	journal	January 2017
Mini‐Metagenomics and Nucleotide Composition Aid the Identification and Host Association of Novel Bacteriophage Sequences Deaton, Jonathan; Yu, Feiqiao Brian; Quake, Stephen R. Advanced Biosystems, Vol. 3, Issue 11 https://doi.org/10.1002/adbi.201900108	journal	May 2019
An Integrative Approach to Virus–Host Protein–Protein Interactions Cook, Helen V.; Jensen, Lars Juhl Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-8618-7_8	book	January 2018
Approaches to optimize therapeutic bacteriophage and bacteriophage-derived products to combat bacterial infections Reuter, Monika; Kruger, Detlev H. Virus Genes, Vol. 56, Issue 2 https://doi.org/10.1007/s11262-020-01735-7	journal	February 2020
Temporal dynamics of uncultured viruses: a new dimension in viral diversity Arkhipova, Ksenia; Skvortsov, Timofey; Quinn, John P. The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.157	journal	October 2017
Lysogeny in nature: mechanisms, impact and ecology of temperate phages Howard-Varona, Cristina; Hargreaves, Katherine R.; Abedon, Stephen T. The ISME Journal, Vol. 11, Issue 7 https://doi.org/10.1038/ismej.2017.16	journal	March 2017
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection Seshadri, Rekha; Leahy, Sinead C.; Attwood, Graeme T. Nature Biotechnology, Vol. 36, Issue 4 https://doi.org/10.1038/nbt.4110	journal	March 2018
Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data Paez-Espino, David; Pavlopoulos, Georgios A.; Ivanova, Natalia N. Nature Protocols, Vol. 12, Issue 8 https://doi.org/10.1038/nprot.2017.063	journal	July 2017
Lysogeny is prevalent and widely distributed in the murine gut microbiota Kim, Min-Soo; Bae, Jin-Woo The ISME Journal, Vol. 12, Issue 4 https://doi.org/10.1038/s41396-018-0061-9	journal	February 2018
A virus or more in (nearly) every cell: ubiquitous networks of virus–host interactions in extreme environments Munson-McGee, Jacob H.; Peng, Shengyun; Dewerff, Samantha The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0071-7	journal	February 2018
Multiple mechanisms drive phage infection efficiency in nearly identical hosts Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0099-8	journal	March 2018
Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes Ahlgren, Nathan A.; Fuchsman, Clara A.; Rocap, Gabrielle The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0289-4	journal	October 2018
The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition Cornuault, Jeffrey K.; Moncaut, Elisabeth; Loux, Valentin The ISME Journal, Vol. 14, Issue 3 https://doi.org/10.1038/s41396-019-0566-x	journal	December 2019
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Global phylogeography and ancient evolution of the widespread human gut virus crAssphage Edwards, Robert A.; Vega, Alejandro A.; Norman, Holly M. Nature Microbiology, Vol. 4, Issue 10 https://doi.org/10.1038/s41564-019-0494-6	journal	July 2019
Defining the human gut host–phage network through single-cell viral tagging Džunková, Mária; Low, Soo Jen; Daly, Joshua N. Nature Microbiology, Vol. 4, Issue 12 https://doi.org/10.1038/s41564-019-0526-2	journal	August 2019
Using CAPTURE to detect spacer acquisition in native CRISPR arrays McKenzie, Rebecca E.; Almendros, Cristóbal; Vink, Jochem N. A. Nature Protocols, Vol. 14, Issue 3 https://doi.org/10.1038/s41596-018-0123-5	journal	February 2019
Host Taxon Predictor - A Tool for Predicting Taxon of the Host of a Newly Discovered Virus Gałan, Wojciech; Bąk, Maciej; Jakubowska, Małgorzata Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-39847-2	journal	March 2019
Biological species in the viral world Bobay, Louis-Marie; Ochman, Howard Proceedings of the National Academy of Sciences, Vol. 115, Issue 23 https://doi.org/10.1073/pnas.1717593115	journal	May 2018
IMG/VR: a database of cultured and uncultured DNA Viruses and retroviruses Paez-Espino, David; Chen, I. -Min A.; Palaniappan, Krishna Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1030	journal	October 2016
MVP: a microbe–phage interaction database Gao, Na L.; Zhang, Chengwei; Zhang, Zhanbing Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1124	journal	November 2017
Gene networks provide a high-resolution view of bacteriophage ecology Shapiro, Jason W.; Putonti, Catherine mBio https://doi.org/10.1101/148668	posted_content	June 2017
The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition Cornuault, Jeffrey K.; Moncaut, Elisabeth; Loux, Valentin The ISME Journal https://doi.org/10.1101/575076	journal	March 2019
Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake Okazaki, Yusuke; Nishimura, Yosuke; Yoshida, Takashi Environmental Microbiology, Vol. 21, Issue 12 https://doi.org/10.1111/1462-2920.14816	journal	September 2019
A viral reckoning: viruses emerge as essential manipulators of global ecosystems: Crystal ball Roux, Simon; Brum, Jennifer R. Environmental Microbiology Reports, Vol. 11, Issue 1 https://doi.org/10.1111/1758-2229.12700	journal	October 2018
Prevalence of viral photosynthesis genes along a freshwater to saltwater transect in Southeast USA Ruiz‐Perez, Carlos A.; Tsementzi, Despina; Hatt, Janet K. Environmental Microbiology Reports, Vol. 11, Issue 5 https://doi.org/10.1111/1758-2229.12780	journal	July 2019
Rapid identification of human‐infecting viruses Zhang, Zheng; Cai, Zena; Tan, Zhiying Transboundary and Emerging Diseases, Vol. 66, Issue 6 https://doi.org/10.1111/tbed.13314	journal	August 2019
Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay Marbouty, Martial; Baudry, Lyam; Cournac, Axel Science Advances, Vol. 3, Issue 2 https://doi.org/10.1126/sciadv.1602105	journal	February 2017
Gene Co-occurrence Networks Reflect Bacteriophage Ecology and Evolution Shapiro, Jason W.; Putonti, Catherine mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mbio.01870-17	journal	March 2018
Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism Bäckström, Disa; Yutin, Natalya; Jørgensen, Steffen L. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.02497-18	journal	March 2019
Soil Viruses Are Underexplored Players in Ecosystem Carbon Processing Trubl, Gareth; Jang, Ho Bin; Roux, Simon mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/msystems.00076-18	journal	October 2018
Trends of Microdiversity Reveal Depth-Dependent Evolutionary Strategies of Viruses in the Mediterranean Coutinho, Felipe Hernandes; Rosselli, Riccardo; Rodríguez-Valera, Francisco mSystems, Vol. 4, Issue 6 https://doi.org/10.1128/msystems.00554-19	journal	November 2019
Predicting virus-host association by Kernelized logistic matrix factorization and similarity network fusion Liu, Dan; Ma, Yingjun; Jiang, Xingpeng BMC Bioinformatics, Vol. 20, Issue S16 https://doi.org/10.1186/s12859-019-3082-0	journal	December 2019
Long-read based de novo assembly of low-complexity metagenome samples results in finished genomes and reveals insights into strain diversity and an active phage system Somerville, Vincent; Lutz, Stefanie; Schmid, Michael BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1500-0	journal	June 2019
The virome: a missing component of biological interaction networks in health and disease Handley, Scott A. Genome Medicine, Vol. 8, Issue 1 https://doi.org/10.1186/s13073-016-0287-y	journal	April 2016
VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data Ren, Jie; Ahlgren, Nathan A.; Lu, Yang Young Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0283-5	journal	July 2017
Environmental drivers of viral community composition in Antarctic soils identified by viromics Adriaenssens, Evelien M.; Kramer, Rolf; Van Goethem, Marc W. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0301-7	journal	July 2017
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0752-0	journal	October 2019
Depth-related variability in viral communities in highly stratified sulfidic mine tailings Gao, Shao-Ming; Schippers, Axel; Chen, Nan Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00848-3	journal	June 2020
Biogeography and environmental conditions shape bacteriophage-bacteria networks across the human microbiome Hannigan, Geoffrey D.; Duhaime, Melissa B.; Koutra, Danai PLOS Computational Biology, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pcbi.1006099	journal	April 2018
A Protocol for Extraction of Infective Viromes Suitable for Metagenomics Sequencing from Low Volume Fecal Samples Deng, Ling; Silins, Ronalds; Castro Mejia, Josue Leonardo https://doi.org/10.20944/preprints201906.0125.v1	preprint	June 2019
Interpretable detection of novel human viruses from genome sequencing data Bartoszewicz, Jakub M.; Seidel, Anja; Renard, Bernhard Y. Robert Koch-Institut https://doi.org/10.25646/9594	text	January 2021
Linking Virus Genomes with Host Taxonomy Mihara, Tomoko; Nishimura, Yosuke; Shimizu, Yugo Viruses, Vol. 8, Issue 3 https://doi.org/10.3390/v8030066	journal	March 2016
HostPhinder: A Phage Host Prediction Tool Villarroel, Julia; Kleinheinz, Kortine; Jurtz, Vanessa Viruses, Vol. 8, Issue 5 https://doi.org/10.3390/v8050116	journal	May 2016
Minimum information about an uncultivated virus genome (MIUVIG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. ETH Zurich https://doi.org/10.3929/ethz-b-000315358	text	January 2019
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh BioMed Central https://doi.org/10.5167/uzh-183761	text	January 2019
Determining virus-host interactions and glycerol metabolism profiles in geographically diverse solar salterns with metagenomics Moller, Abraham G.; Liang, Chun https://doi.org/10.7287/peerj.preprints.2106v2	preprint	July 2016
Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils Trubl, Gareth; Roux, Simon; Solonenko, Natalie PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7265	journal	January 2019

Figures / Tables (5)

Similar Records

Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton

Journal Article · Mon Apr 06 20:00:00 EDT 2015 · The ISME Journal · OSTI ID:1347108

A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes

Journal Article · Wed Jul 23 20:00:00 EDT 2014 · Nature Communications · OSTI ID:1623951

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CRISPR
co-occurrence
metagenomics
microbiology
oligonucleotide usage
phages
viruses of microbes

Computational approaches to predict bacteriophage–host relationships

Citation Formats

References (127)

Cited By (84)

Figures / Tables (5)

Similar Records

Related Subjects