Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes
Abstract
Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exclusively episomal state or integrated into the host chromosome and virions are continuously released without killing the host. To date, a relatively small number of inovirus isolates have been extensively studied, either for biotechnological applications, such as phage display, or because of their effect on the toxicity of known bacterial pathogens including Vibrio cholerae and Neisseria meningitidis. Here, we show that the current 56 members of the Inoviridae family represent a minute fraction of a highly diverse group of inoviruses. Using a machine learning approach leveraging a combination of marker gene and genome features, we identified 10,295 inovirus-like sequences from microbial genomes and metagenomes. Collectively, our results call for reclassification of the current Inoviridae family into a viral order including six distinct proposed families associated with nearly all bacterial phyla across virtually every ecosystem. Putative inoviruses were also detected in several archaeal genomes, suggesting that, collectively, members of this supergroup infect hosts across the domains Bacteriamore »
- Authors:
-
[1];
[2];
[1];
[5];
[1];
[1];
[1];
[1]
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Inst. Pasteur, Paris (France)
- Colorado State Univ., Fort Collins, CO (United States)
- Univ. of California, San Francisco, CA (United States)
- Univ. of California, Berkeley, CA (United States)
- Univ. of California, San Francisco, CA (United States). Quantitative Biosciences Inst.
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Sciences Foundation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1581331
- Grant/Contract Number:
- AC02-05CH11231; EAR 1331940
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Microbiology
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 11; Journal ID: ISSN 2058-5276
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Archaea; Bacteriophages; Environmental microbiology; Phage biology; Metagenomics
Citation Formats
Roux, Simon, Krupovic, Mart, Daly, Rebecca A., Borges, Adair L., Nayfach, Stephen, Schulz, Frederik, Sharrar, Allison, Matheus Carnevali, Paula B., Cheng, Jan-Fang, Ivanova, Natalia N., Bondy-Denomy, Joseph, Wrighton, Kelly C., Woyke, Tanja, Visel, Axel, Kyrpides, Nikos C., and Eloe-Fadrosh, Emiley A. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. United States: N. p., 2019.
Web. doi:10.1038/s41564-019-0510-x.
Roux, Simon, Krupovic, Mart, Daly, Rebecca A., Borges, Adair L., Nayfach, Stephen, Schulz, Frederik, Sharrar, Allison, Matheus Carnevali, Paula B., Cheng, Jan-Fang, Ivanova, Natalia N., Bondy-Denomy, Joseph, Wrighton, Kelly C., Woyke, Tanja, Visel, Axel, Kyrpides, Nikos C., & Eloe-Fadrosh, Emiley A. Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes. United States. https://doi.org/10.1038/s41564-019-0510-x
Roux, Simon, Krupovic, Mart, Daly, Rebecca A., Borges, Adair L., Nayfach, Stephen, Schulz, Frederik, Sharrar, Allison, Matheus Carnevali, Paula B., Cheng, Jan-Fang, Ivanova, Natalia N., Bondy-Denomy, Joseph, Wrighton, Kelly C., Woyke, Tanja, Visel, Axel, Kyrpides, Nikos C., and Eloe-Fadrosh, Emiley A. Mon .
"Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes". United States. https://doi.org/10.1038/s41564-019-0510-x. https://www.osti.gov/servlets/purl/1581331.
@article{osti_1581331,
title = {Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes},
author = {Roux, Simon and Krupovic, Mart and Daly, Rebecca A. and Borges, Adair L. and Nayfach, Stephen and Schulz, Frederik and Sharrar, Allison and Matheus Carnevali, Paula B. and Cheng, Jan-Fang and Ivanova, Natalia N. and Bondy-Denomy, Joseph and Wrighton, Kelly C. and Woyke, Tanja and Visel, Axel and Kyrpides, Nikos C. and Eloe-Fadrosh, Emiley A.},
abstractNote = {Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exclusively episomal state or integrated into the host chromosome and virions are continuously released without killing the host. To date, a relatively small number of inovirus isolates have been extensively studied, either for biotechnological applications, such as phage display, or because of their effect on the toxicity of known bacterial pathogens including Vibrio cholerae and Neisseria meningitidis. Here, we show that the current 56 members of the Inoviridae family represent a minute fraction of a highly diverse group of inoviruses. Using a machine learning approach leveraging a combination of marker gene and genome features, we identified 10,295 inovirus-like sequences from microbial genomes and metagenomes. Collectively, our results call for reclassification of the current Inoviridae family into a viral order including six distinct proposed families associated with nearly all bacterial phyla across virtually every ecosystem. Putative inoviruses were also detected in several archaeal genomes, suggesting that, collectively, members of this supergroup infect hosts across the domains Bacteria and Archaea. Finally, we identified an expansive diversity of inovirus-encoded toxin–antitoxin and gene expression modulation systems, alongside evidence of both synergistic (CRISPR evasion) and antagonistic (superinfection exclusion) interactions with co-infecting viruses, which we experimentally validated in a Pseudomonas model. Capturing this previously obscured component of the global virosphere may spark new avenues for microbial manipulation approaches and innovative biotechnological applications.},
doi = {10.1038/s41564-019-0510-x},
journal = {Nature Microbiology},
number = 11,
volume = 4,
place = {United States},
year = {Mon Jul 22 00:00:00 EDT 2019},
month = {Mon Jul 22 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 109 works
Citation information provided by
Web of Science
Web of Science
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:
The diversity of single stranded DNA viruses
journal, February 2006
- Fauquet, C. M.
- Biodiversity, Vol. 7, Issue 1
Structure and assembly of filamentous bacteriophages
journal, April 2014
- Marvin, D. A.; Symmons, M. F.; Straus, S. K.
- Progress in Biophysics and Molecular Biology, Vol. 114, Issue 2
Antibodies from phage antibody libraries
journal, July 2004
- Bradbury, Andrew R. M.; Marks, James D.
- Journal of Immunological Methods, Vol. 290, Issue 1-2
Stamped microbattery electrodes based on self-assembled M13 viruses
journal, August 2008
- Nam, K. T.; Wartena, R.; Yoo, P. J.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 45
Drug delivery vectors based on filamentous bacteriophages and phage-mimetic nanoparticles
journal, January 2017
- Ju, Zhigang; Sun, Wei
- Drug Delivery, Vol. 24, Issue 1
Evolution of mutualism from parasitism in experimental virus populations: BRIEF COMMUNICATION
journal, March 2018
- Shapiro, Jason W.; Turner, Paul E.
- Evolution, Vol. 72, Issue 3
Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection
journal, March 2019
- Sweere, Johanna M.; Van Belleghem, Jonas D.; Ishak, Heather
- Science, Vol. 363, Issue 6434
Lysogenic Conversion by a Filamentous Phage Encoding Cholera Toxin
journal, June 1996
- Waldor, M. K.; Mekalanos, J. J.
- Science, Vol. 272, Issue 5270
Pathogenicity islands and phages in Vibrio cholerae evolution
journal, November 2003
- Faruque, Shah M.; Mekalanos, John J.
- Trends in Microbiology, Vol. 11, Issue 11
A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation
journal, July 2017
- Bille, Emmanuelle; Meyer, Julie; Jamet, Anne
- PLOS Pathogens, Vol. 13, Issue 7
The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage
journal, November 2008
- Rice, Scott A.; Tan, Chuan Hao; Mikkelsen, Per Jensen
- The ISME Journal, Vol. 3, Issue 3
The Role of Prophage in Plant-Pathogenic Bacteria
journal, August 2013
- Varani, Alessandro M.; Monteiro-Vitorello, Claudia Barros; Nakaya, Helder I.
- Annual Review of Phytopathology, Vol. 51, Issue 1
‘Big things in small packages: the genetics of filamentous phage and effects on fitness of their host’
journal, February 2015
- Mai-Prochnow, Anne; Hui, Janice Gee Kay; Kjelleberg, Staffan
- FEMS Microbiology Reviews, Vol. 39, Issue 4
Uncovering Earth’s virome
journal, August 2016
- Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
- Nature, Vol. 536, Issue 7617
Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data
journal, July 2017
- Paez-Espino, David; Pavlopoulos, Georgios A.; Ivanova, Natalia N.
- Nature Protocols, Vol. 12, Issue 8
VirSorter: mining viral signal from microbial genomic data
journal, January 2015
- Roux, Simon; Enault, Francois; Hurwitz, Bonnie L.
- PeerJ, Vol. 3
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
Laboratory procedures to generate viral metagenomes
journal, March 2009
- Thurber, Rebecca V.; Haynes, Matthew; Breitbart, Mya
- Nature Protocols, Vol. 4, Issue 4
IMG/M: integrated genome and metagenome comparative data analysis system
journal, October 2016
- Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken
- Nucleic Acids Research, Vol. 45, Issue D1
The enigmatic archaeal virosphere
journal, November 2017
- Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick
- Nature Reviews Microbiology, Vol. 15, Issue 12
Viruses of archaea: Structural, functional, environmental and evolutionary genomics
journal, January 2018
- Krupovic, Mart; Cvirkaite-Krupovic, Virginija; Iranzo, Jaime
- Virus Research, Vol. 244
Horizontal gene transfer and genome evolution in Methanosarcina
journal, June 2015
- Garushyants, Sofya K.; Kazanov, Marat D.; Gelfand, Mikhail S.
- BMC Evolutionary Biology, Vol. 15, Issue 1
Bacteriophage evolution differs by host, lifestyle and genome
journal, July 2017
- Mavrich, Travis N.; Hatfull, Graham F.
- Nature Microbiology, Vol. 2, Issue 9
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
Multilevel Compression of Random Walks on Networks Reveals Hierarchical Organization in Large Integrated Systems
journal, April 2011
- Rosvall, Martin; Bergstrom, Carl T.
- PLoS ONE, Vol. 6, Issue 4
Origins and Evolution of the Global RNA Virome
journal, November 2018
- Wolf, Yuri I.; Kazlauskas, Darius; Iranzo, Jaime
- mBio, Vol. 9, Issue 6
Origins and evolution of viruses of eukaryotes: The ultimate modularity
journal, May 2015
- Koonin, Eugene V.; Dolja, Valerian V.; Krupovic, Mart
- Virology, Vol. 479-480
Post-segregational Killing and Phage Inhibition Are Not Mediated by Cell Death Through Toxin/Antitoxin Systems
journal, April 2018
- Song, Sooyeon; Wood, Thomas K.
- Frontiers in Microbiology, Vol. 9
CRISPR-Cas immunity in prokaryotes
journal, October 2015
- Marraffini, Luciano A.
- Nature, Vol. 526, Issue 7571
The Discovery, Mechanisms, and Evolutionary Impact of Anti-CRISPRs
journal, September 2017
- Borges, Adair L.; Davidson, Alan R.; Bondy-Denomy, Joseph
- Annual Review of Virology, Vol. 4, Issue 1
Sociovirology: Conflict, Cooperation, and Communication among Viruses
journal, October 2017
- Díaz-Muñoz, Samuel L.; Sanjuán, Rafael; West, Stuart
- Cell Host & Microbe, Vol. 22, Issue 4
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
NCBI Viral Genomes Resource
journal, November 2014
- Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming
- Nucleic Acids Research, Vol. 43, Issue D1
Identifying bacterial genes and endosymbiont DNA with Glimmer
journal, January 2007
- Delcher, Arthur L.; Bratke, Kirsten A.; Powers, Edwin C.
- Bioinformatics, Vol. 23, Issue 6
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment
journal, December 2011
- Remmert, Michael; Biegert, Andreas; Hauser, Andreas
- Nature Methods, Vol. 9, Issue 2
CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012
- Fu, Limin; Niu, Beifang; Zhu, Zhengwei
- Bioinformatics, Vol. 28, Issue 23
Accelerated Profile HMM Searches
journal, October 2011
- Eddy, Sean R.
- PLoS Computational Biology, Vol. 7, Issue 10
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, Issue 1
Conditional variable importance for random forests
journal, July 2008
- Strobl, Carolin; Boulesteix, Anne-Laure; Kneib, Thomas
- BMC Bioinformatics, Vol. 9, Issue 1
Regularization Paths for Cox's Proportional Hazards Model via Coordinate Descent
journal, January 2011
- Simon, Noah; Friedman, Jerome; Hastie, Trevor
- Journal of Statistical Software, Vol. 39, Issue 5
Taxonomy of prokaryotic viruses: 2016 update from the ICTV bacterial and archaeal viruses subcommittee
journal, December 2016
- Adriaenssens, Evelien M.; Krupovic, Mart; Knezevic, Petar
- Archives of Virology, Vol. 162, Issue 4
Versatile and open software for comparing large genomes
journal, January 2004
- Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
- Genome Biology, Vol. 5, Issue 2, R12
The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis
journal, April 2016
- Alva, Vikram; Nam, Seung-Zin; Söding, Johannes
- Nucleic Acids Research, Vol. 44, Issue W1
Cytoscape: the network visualization tool for GenomeSpace workflows
journal, January 2014
- Demchak, Barry; Hull, Tim; Reich, Michael
- F1000Research, Vol. 3
SDT: A Virus Classification Tool Based on Pairwise Sequence Alignment and Identity Calculation
journal, September 2014
- Muhire, Brejnev Muhizi; Varsani, Arvind; Martin, Darren Patrick
- PLoS ONE, Vol. 9, Issue 9
Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs
journal, January 2016
- Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica
- Nature Communications, Vol. 7, Issue 1
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017
- Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria
- Nature Microbiology, Vol. 2, Issue 11
The COG database: a tool for genome-scale analysis of protein functions and evolution
journal, January 2000
- Tatusov, R. L.
- Nucleic Acids Research, Vol. 28, Issue 1
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments
journal, January 2010
- Criscuolo, Alexis; Gribaldo, Simonetta
- BMC Evolutionary Biology, Vol. 10, Issue 1
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Genomes OnLine Database (GOLD) v.6: data updates and feature enhancements
journal, October 2016
- Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
- Nucleic Acids Research, Vol. 45, Issue D1
Matplotlib: A 2D Graphics Environment
journal, January 2007
- Hunter, John D.
- Computing in Science & Engineering, Vol. 9, Issue 3
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 44, Issue W1
Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses
journal, October 2013
- Krupovic, Mart
- Current Opinion in Virology, Vol. 3, Issue 5
Structures of replication initiation proteins from staphylococcal antibiotic resistance plasmids reveal protein asymmetry and flexibility are necessary for replication
journal, January 2016
- Carr, Stephen B.; Phillips, Simon E. V.; Thomas, Christopher D.
- Nucleic Acids Research, Vol. 44, Issue 5
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015
- Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
- Nature Protocols, Vol. 10, Issue 6
SMART 4.0: towards genomic data integration
journal, January 2004
- Letunic, I.
- Nucleic Acids Research, Vol. 32, Issue 90001
An updated evolutionary classification of CRISPR–Cas systems
journal, September 2015
- Makarova, Kira S.; Wolf, Yuri I.; Alkhnbashi, Omer S.
- Nature Reviews Microbiology, Vol. 13, Issue 11, p. 722-736
Methanolobus profundi sp. nov., a methylotrophic methanogen isolated from deep subsurface sediments in a natural gas field
journal, April 2009
- Mochimaru, H.; Tamaki, H.; Hanada, S.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 4
Poly peak parser: Method and software for identification of unknown indels using sanger sequencing of polymerase chain reaction products: POLY PEAK PARSER
journal, September 2014
- Hill, Jonathon T.; Demarest, Bradley L.; Bisgrove, Brent W.
- Developmental Dynamics, Vol. 243, Issue 12
Jalview Version 2--a multiple sequence alignment editor and analysis workbench
journal, January 2009
- Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A.
- Bioinformatics, Vol. 25, Issue 9
Streamlining the Design-to-Build Transition with Build-Optimization Software Tools
journal, November 2016
- Oberortner, Ernst; Cheng, Jan-Fang; Hillson, Nathan J.
- ACS Synthetic Biology, Vol. 6, Issue 3
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021
- Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E.
- The ISME Journal, Vol. 15, Issue 8
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander
journal, April 2020
- Song, Xiaoming; Nie, Fulei; Chen, Wei
- Horticulture Research, Vol. 7, Issue 1
A sand fly salivary protein acts as a neutrophil chemoattractant
journal, May 2021
- Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid
- Nature Communications, Vol. 12, Issue 1
Why does the Aβ peptide of Alzheimer share structural similarity with antimicrobial peptides?
journal, March 2020
- Pastore, Annalisa; Raimondi, Francesco; Rajendran, Lawrence
- Communications Biology, Vol. 3, Issue 1
Diversity of Sea Star-Associated Densoviruses and Transcribed Endogenous Viral Elements of Densovirus Origin
journal, December 2020
- Jackson, Elliot W.; Wilhelm, Roland C.; Johnson, Mitchell R.
- Journal of Virology, Vol. 95, Issue 1
Draft Genome Sequence of Medusavirus Stheno, Isolated from the Tatakai River of Uji, Japan
journal, January 2021
- Yoshida, Koki; Zhang, Ruixuan; Garcia, Kimberly G.
- Microbiology Resource Announcements, Vol. 10, Issue 1
Cytoscape: the network visualization tool for GenomeSpace workflows
journal, July 2014
- Demchak, Barry; Hull, Tim; Reich, Michael
- F1000Research
Conditional Variable Importance for Random Forests
text, January 2008
- Strobl, Carolin; Boulesteix, Anne-Laure; Kneib, Thomas
- Universitätsbibliothek der Ludwig-Maximilians-Universität München
Multilevel compression of random walks on networks reveals hierarchical organization in large integrated systems
text, January 2010
- Rosvall, M.; Bergstrom, C. T.
- arXiv
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Taxonomy of prokaryotic viruses: 2016 update from the ICTV bacterial and archaeal viruses subcommittee
journal, December 2016
- Adriaenssens, Evelien M.; Krupovic, Mart; Knezevic, Petar
- Archives of Virology, Vol. 162, Issue 4
Complete genome analysis of a novel iflavirus from a leaf beetle, Aulacophora lewisii
journal, October 2020
- Ye, Zhuang-Xin; Li, Yue-Hong; Chen, Jian-Ping
- Archives of Virology, Vol. 166, Issue 1
Sociovirology: Conflict, Cooperation, and Communication among Viruses
journal, October 2017
- Díaz-Muñoz, Samuel L.; Sanjuán, Rafael; West, Stuart
- Cell Host & Microbe, Vol. 22, Issue 4
Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses
journal, October 2013
- Krupovic, Mart
- Current Opinion in Virology, Vol. 3, Issue 5
Antibodies from phage antibody libraries
journal, July 2004
- Bradbury, Andrew R. M.; Marks, James D.
- Journal of Immunological Methods, Vol. 290, Issue 1-2
Structure and assembly of filamentous bacteriophages
journal, April 2014
- Marvin, D. A.; Symmons, M. F.; Straus, S. K.
- Progress in Biophysics and Molecular Biology, Vol. 114, Issue 2
Pathogenicity islands and phages in Vibrio cholerae evolution
journal, November 2003
- Faruque, Shah M.; Mekalanos, John J.
- Trends in Microbiology, Vol. 11, Issue 11
Origins and evolution of viruses of eukaryotes: The ultimate modularity
journal, May 2015
- Koonin, Eugene V.; Dolja, Valerian V.; Krupovic, Mart
- Virology, Vol. 479-480
Viruses of archaea: Structural, functional, environmental and evolutionary genomics
journal, January 2018
- Krupovic, Mart; Cvirkaite-Krupovic, Virginija; Iranzo, Jaime
- Virus Research, Vol. 244
Streamlining the Design-to-Build Transition with Build-Optimization Software Tools
journal, November 2016
- Oberortner, Ernst; Cheng, Jan-Fang; Hillson, Nathan J.
- ACS Synthetic Biology, Vol. 6, Issue 3
The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage
journal, November 2008
- Rice, Scott A.; Tan, Chuan Hao; Mikkelsen, Per Jensen
- The ISME Journal, Vol. 3, Issue 3
CRISPR-Cas immunity in prokaryotes
journal, October 2015
- Marraffini, Luciano A.
- Nature, Vol. 526, Issue 7571
Uncovering Earth’s virome
journal, August 2016
- Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
- Nature, Vol. 536, Issue 7617
Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs
journal, January 2016
- Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica
- Nature Communications, Vol. 7, Issue 1
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment
journal, December 2011
- Remmert, Michael; Biegert, Andreas; Hauser, Andreas
- Nature Methods, Vol. 9, Issue 2
Bacteriophage evolution differs by host, lifestyle and genome
journal, July 2017
- Mavrich, Travis N.; Hatfull, Graham F.
- Nature Microbiology, Vol. 2, Issue 9
Laboratory procedures to generate viral metagenomes
journal, March 2009
- Thurber, Rebecca V.; Haynes, Matthew; Breitbart, Mya
- Nature Protocols, Vol. 4, Issue 4
The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015
- Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
- Nature Protocols, Vol. 10, Issue 6
Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data
journal, July 2017
- Paez-Espino, David; Pavlopoulos, Georgios A.; Ivanova, Natalia N.
- Nature Protocols, Vol. 12, Issue 8
The enigmatic archaeal virosphere
journal, November 2017
- Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick
- Nature Reviews Microbiology, Vol. 15, Issue 12
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
Rhizosphere bacteriome structure and functions
journal, February 2022
- Ling, Ning; Wang, Tingting; Kuzyakov, Yakov
- Nature Communications, Vol. 13, Issue 1
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017
- Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria
- Nature Microbiology, Vol. 2, Issue 11
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha
journal, February 2022
- Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan
- Scientific Reports, Vol. 12, Issue 1
Combination of antiviral drugs inhibits SARS-CoV-2 polymerase and exonuclease and demonstrates COVID-19 therapeutic potential in viral cell culture
journal, February 2022
- Wang, Xuanting; Sacramento, Carolina Q.; Jockusch, Steffen
- Communications Biology, Vol. 5, Issue 1
Stamped microbattery electrodes based on self-assembled M13 viruses
journal, August 2008
- Nam, K. T.; Wartena, R.; Yoo, P. J.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 45
The diversity of single stranded DNA viruses
journal, February 2006
- Fauquet, C. M.
- Biodiversity, Vol. 7, Issue 1
Identifying bacterial genes and endosymbiont DNA with Glimmer
journal, January 2007
- Delcher, Arthur L.; Bratke, Kirsten A.; Powers, Edwin C.
- Bioinformatics, Vol. 23, Issue 6
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012
- Fu, Limin; Niu, Beifang; Zhu, Zhengwei
- Bioinformatics, Vol. 28, Issue 23
‘Big things in small packages: the genetics of filamentous phage and effects on fitness of their host’
journal, February 2015
- Mai-Prochnow, Anne; Hui, Janice Gee Kay; Kjelleberg, Staffan
- FEMS Microbiology Reviews, Vol. 39, Issue 4
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
SMART 4.0: towards genomic data integration
journal, January 2004
- Letunic, I.
- Nucleic Acids Research, Vol. 32, Issue 90001
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
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
Structures of replication initiation proteins from staphylococcal antibiotic resistance plasmids reveal protein asymmetry and flexibility are necessary for replication
journal, January 2016
- Carr, Stephen B.; Phillips, Simon E. V.; Thomas, Christopher D.
- Nucleic Acids Research, Vol. 44, Issue 5
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 44, Issue W1
The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis
journal, April 2016
- Alva, Vikram; Nam, Seung-Zin; Söding, Johannes
- Nucleic Acids Research, Vol. 44, Issue W1
Genomes OnLine Database (GOLD) v.6: data updates and feature enhancements
journal, October 2016
- Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
- Nucleic Acids Research, Vol. 45, Issue D1
Methanolobus profundi sp. nov., a methylotrophic methanogen isolated from deep subsurface sediments in a natural gas field
journal, April 2009
- Mochimaru, H.; Tamaki, H.; Hanada, S.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 4
Evolution of mutualism from parasitism in experimental virus populations: BRIEF COMMUNICATION
journal, March 2018
- Shapiro, Jason W.; Turner, Paul E.
- Evolution, Vol. 72, Issue 3
Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection
journal, March 2019
- Sweere, Johanna M.; Van Belleghem, Jonas D.; Ishak, Heather
- Science, Vol. 363, Issue 6434
PBAD-Based Shuttle Vectors for Functional Analysis of Toxic and Highly Regulated Genes in Pseudomonas and Burkholderia spp. and Other Bacteria
journal, October 2008
- Qiu, D.; Damron, F. H.; Mima, T.
- Applied and Environmental Microbiology, Vol. 74, Issue 23
Isolation and characterization of a filamentous viruslike particle from Clostridium acetobutylicum NCIB 6444.
journal, January 1991
- Kim, A. Y.; Blaschek, H. P.
- Journal of Bacteriology, Vol. 173, Issue 2
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
Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere
journal, November 2011
- Krupovic, M.; Prangishvili, D.; Hendrix, R. W.
- Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4
The Role of Prophage in Plant-Pathogenic Bacteria
journal, August 2013
- Varani, Alessandro M.; Monteiro-Vitorello, Claudia Barros; Nakaya, Helder I.
- Annual Review of Phytopathology, Vol. 51, Issue 1
The Discovery, Mechanisms, and Evolutionary Impact of Anti-CRISPRs
journal, September 2017
- Borges, Adair L.; Davidson, Alan R.; Bondy-Denomy, Joseph
- Annual Review of Virology, Vol. 4, Issue 1
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Conditional variable importance for random forests
journal, July 2008
- Strobl, Carolin; Boulesteix, Anne-Laure; Kneib, Thomas
- BMC Bioinformatics, Vol. 9, Issue 1
Horizontal gene transfer and genome evolution in Methanosarcina
journal, June 2015
- Garushyants, Sofya K.; Kazanov, Marat D.; Gelfand, Mikhail S.
- BMC Evolutionary Biology, Vol. 15, Issue 1
Cytoscape: the network visualization tool for GenomeSpace workflows
journal, January 2014
- Demchak, Barry; Hull, Tim; Reich, Michael
- F1000Research, Vol. 3
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation
journal, July 2017
- Bille, Emmanuelle; Meyer, Julie; Jamet, Anne
- PLOS Pathogens, Vol. 13, Issue 7
Regularization Paths for Cox's Proportional Hazards Model via Coordinate Descent
journal, January 2011
- Simon, Noah; Friedman, Jerome; Hastie, Trevor
- Journal of Statistical Software, Vol. 39, Issue 5
Filamentous bacteriophages and their role in the virulence and evolution of pathogenic bacteria
journal, January 2015
- Ilyina, T. S.
- Molecular Genetics, Microbiology and Virology, Vol. 30, Issue 1
Beyond phage display: non-traditional applications of the filamentous bacteriophage as a vaccine carrier, therapeutic biologic, and bioconjugation scaffold
journal, August 2015
- Henry, Kevin A.; Arbabi-Ghahroudi, Mehdi; Scott, Jamie K.
- Frontiers in Microbiology, Vol. 6
Post-segregational Killing and Phage Inhibition Are Not Mediated by Cell Death Through Toxin/Antitoxin Systems
journal, April 2018
- Song, Sooyeon; Wood, Thomas K.
- Frontiers in Microbiology, Vol. 9
Multilevel compression of random walks on networks reveals hierarchical organization in large integrated systems
text, January 2010
- Rosvall, M.; Bergstrom, C. T.
- arXiv
DNest4: Diffusive Nested Sampling in C++ and Python
preprint, January 2016
- Brewer, Brendon J.; Foreman-Mackey, Daniel
- arXiv
VirSorter: mining viral signal from microbial genomic data
journal, January 2015
- Roux, Simon; Enault, Francois; Hurwitz, Bonnie L.
- PeerJ, Vol. 3
Works referencing / citing this record:
Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids
journal, July 2019
- Kazlauskas, Darius; Varsani, Arvind; Koonin, Eugene V.
- Nature Communications, Vol. 10, Issue 1
Phage liquid crystalline droplets form occlusive sheaths that encapsulate and protect infectious rod-shaped bacteria
journal, February 2020
- Tarafder, Abul K.; von Kügelgen, Andriko; Mellul, Adam J.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 9
Comparative genomics groups phages of Negativicutes and classical Firmicutes despite different Gram‐staining properties
journal, July 2019
- Rands, Chris M.; Brüssow, Harald; Zdobnov, Evgeny M.
- Environmental Microbiology, Vol. 21, Issue 11
Expansion of known ssRNA phage genomes: From tens to over a thousand
journal, February 2020
- Callanan, J.; Stockdale, S. R.; Shkoporov, A.
- Science Advances, Vol. 6, Issue 6
Single-Stranded DNA Viruses in Antarctic Cryoconite Holes
journal, November 2019
- Sommers, Pacifica; Fontenele, Rafaela S.; Kringen, Tayele
- Viruses, Vol. 11, Issue 11
Discovery of several thousand highly diverse circular DNA viruses
text, January 2020
- Tisza, Michael J.; Pastrana, Diana V.; Welch, Nicole L.
- Apollo - University of Cambridge Repository
New insights into intestinal phages
journal, January 2020
- Sausset, R.; Petit, M. A.; Gaboriau-Routhiau, V.
- Mucosal Immunology, Vol. 13, Issue 2
Three families of Asgard archaeal viruses identified in metagenome-assembled genomes
journal, June 2022
- Medvedeva, Sofia; Sun, Jiarui; Yutin, Natalya
- Nature Microbiology, Vol. 7, Issue 7
Phage liquid crystalline droplets form occlusive sheaths that encapsulate and protect infectious rod-shaped bacteria
journal, February 2020
- Tarafder, Abul K.; von Kügelgen, Andriko; Mellul, Adam J.
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 9
Expansion of known ssRNA phage genomes: From tens to over a thousand
journal, February 2020
- Callanan, J.; Stockdale, S. R.; Shkoporov, A.
- Science Advances, Vol. 6, Issue 6
More than Simple Parasites: the Sociobiology of Bacteriophages and Their Bacterial Hosts
journal, April 2020
- Secor, Patrick R.; Dandekar, Ajai A.
- mBio, Vol. 11, Issue 2
Advantages and Limits of Metagenomic Assembly and Binning of a Giant Virus
journal, June 2020
- Schulz, Frederik; Andreani, Julien; Francis, Rania
- mSystems, Vol. 5, Issue 3
Discovery of several thousand highly diverse circular DNA viruses.
journalarticle, January 2020
- Tisza, Michael J.; Pastrana, Diana V.; Welch, Nicole L.
- eLife Sciences Publications, Ltd
Pf Bacteriophage and Their Impact on Pseudomonas Virulence, Mammalian Immunity, and Chronic Infections
journal, February 2020
- Secor, Patrick R.; Burgener, Elizabeth B.; Kinnersley, M.
- Frontiers in Immunology, Vol. 11
Activation of the Cell Wall Stress Response in Pseudomonas aeruginosa Infected by a Pf4 Phage Variant
journal, October 2020
- Tortuel, Damien; Tahrioui, Ali; Rodrigues, Sophie
- Microorganisms, Vol. 8, Issue 11
Single-Stranded DNA Viruses in Antarctic Cryoconite Holes
journal, November 2019
- Sommers, Pacifica; Fontenele, Rafaela S.; Kringen, Tayele
- Viruses, Vol. 11, Issue 11
“French Phage Network” Annual Conference—Fifth Meeting Report
journal, April 2020
- Laumay, Floriane; Chaïb, Amel; Linares, Romain
- Viruses, Vol. 12, Issue 4