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Title: Investigation of recombination-intense viral groups and their genes in the Earth’s virome

Abstract

Bacteriophages (phages), or bacterial viruses, are the most abundant and diverse biological entities that impact the global ecosystem. Recent advances in metagenomics have revealed their rampant abundance in the biosphere. A fundamental aspect of bacteriophages that remains unexplored in metagenomic data is the process of recombination as a driving force in evolution that occurs among different viruses within the same bacterial host. Here, we systematically examined signatures of recombination in every gene from 211 species-level viral groups in a recently obtained dataset of the Earth’s virome that contain corresponding information on the host bacterial species. Our study revealed that signatures of recombination are widespread (84%) among the diverse viral groups. We identified 25 recombination-intense viral groups, widely distributed across the viral taxonomy, and present in bacterial species living in the human oral cavity. We also revealed a significant inverse association between the recombination-intense viral groups and Type II restriction endonucleases, that could be effective in reducing recombination among phages in a cell. Furthermore, we identified recombination-intense genes that are significantly enriched for encoding phage morphogenesis proteins. Changes in the viral genomic sequence by recombination may be important to escape cleavage by the host bacterial immune systems.

Authors:
 [1];  [2];  [3]; ORCiD logo [4]; ORCiD logo [5]
  1. Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig (Germany)
  2. Azabu Univ., Kanagawa (Japan)
  3. Tokyo Medical and Dental Univ., Tokyo (Japan)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. National Inst. of Infectious Diseases, Tokyo (Japan)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1543781
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology; Other Topics

Citation Formats

Meier-Kolthoff, Jan P., Uchiyama, Jumpei, Yahara, Hiroko, Paez-Espino, David, and Yahara, Koji. Investigation of recombination-intense viral groups and their genes in the Earth’s virome. United States: N. p., 2018. Web. doi:10.1038/s41598-018-29272-2.
Meier-Kolthoff, Jan P., Uchiyama, Jumpei, Yahara, Hiroko, Paez-Espino, David, & Yahara, Koji. Investigation of recombination-intense viral groups and their genes in the Earth’s virome. United States. https://doi.org/10.1038/s41598-018-29272-2
Meier-Kolthoff, Jan P., Uchiyama, Jumpei, Yahara, Hiroko, Paez-Espino, David, and Yahara, Koji. Tue . "Investigation of recombination-intense viral groups and their genes in the Earth’s virome". United States. https://doi.org/10.1038/s41598-018-29272-2. https://www.osti.gov/servlets/purl/1543781.
@article{osti_1543781,
title = {Investigation of recombination-intense viral groups and their genes in the Earth’s virome},
author = {Meier-Kolthoff, Jan P. and Uchiyama, Jumpei and Yahara, Hiroko and Paez-Espino, David and Yahara, Koji},
abstractNote = {Bacteriophages (phages), or bacterial viruses, are the most abundant and diverse biological entities that impact the global ecosystem. Recent advances in metagenomics have revealed their rampant abundance in the biosphere. A fundamental aspect of bacteriophages that remains unexplored in metagenomic data is the process of recombination as a driving force in evolution that occurs among different viruses within the same bacterial host. Here, we systematically examined signatures of recombination in every gene from 211 species-level viral groups in a recently obtained dataset of the Earth’s virome that contain corresponding information on the host bacterial species. Our study revealed that signatures of recombination are widespread (84%) among the diverse viral groups. We identified 25 recombination-intense viral groups, widely distributed across the viral taxonomy, and present in bacterial species living in the human oral cavity. We also revealed a significant inverse association between the recombination-intense viral groups and Type II restriction endonucleases, that could be effective in reducing recombination among phages in a cell. Furthermore, we identified recombination-intense genes that are significantly enriched for encoding phage morphogenesis proteins. Changes in the viral genomic sequence by recombination may be important to escape cleavage by the host bacterial immune systems.},
doi = {10.1038/s41598-018-29272-2},
journal = {Scientific Reports},
number = 1,
volume = 8,
place = {United States},
year = {Tue Jul 31 00:00:00 EDT 2018},
month = {Tue Jul 31 00:00:00 EDT 2018}
}

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Works referenced in this record:

The portal protein plays essential roles at different steps of the SPP1 DNA packaging process
journal, May 2004


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


Ecology of the Oral Microbiome: Beyond Bacteria
journal, May 2017

  • Baker, Jonathon L.; Bor, Batbileg; Agnello, Melissa
  • Trends in Microbiology, Vol. 25, Issue 5
  • DOI: 10.1016/j.tim.2016.12.012

Roary: rapid large-scale prokaryote pan genome analysis
journal, July 2015


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
  • DOI: 10.1093/nar/gkw992

Phages in nature
journal, January 2011

  • Clokie, Martha R. J.; Millard, Andrew D.; Letarov, Andrey V.
  • Bacteriophage, Vol. 1, Issue 1
  • DOI: 10.4161/bact.1.1.14942

PGEToolbox: A Matlab Toolbox for Population Genetics and Evolution
journal, February 2008


Global transcription of CRISPR loci in the human oral cavity
journal, May 2015


Bacteriophage lysis: mechanism and regulation
journal, September 1992


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
  • DOI: 10.1038/nprot.2017.063

MBGD. Microbial Genome Database for Comparative Analysis.
journal, January 2002


Efficient Inference of Recombination Hot Regions in Bacterial Genomes
journal, February 2014

  • Yahara, Koji; Didelot, Xavier; Ansari, M. Azim
  • Molecular Biology and Evolution, Vol. 31, Issue 6
  • DOI: 10.1093/molbev/msu082

Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory
journal, September 2017


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


Bacteriophage lysis: mechanism and regulation.
journal, January 1992


Human Case of Atopobium rimae Bacteremia
journal, February 2009

  • Angelakis, Emmanouil; Roux, Véronique; Raoult, Didier
  • Emerging Infectious Diseases, Vol. 15, Issue 2
  • DOI: 10.3201/eid1502.071399

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

The Janus-Face of Bacteriophages across Human Body Habitats
journal, June 2016


Genome sequence-based species delimitation with confidence intervals and improved distance functions
journal, January 2013

  • Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter
  • BMC Bioinformatics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2105-14-60

Type II restriction endonucleases—a historical perspective and more
journal, May 2014

  • Pingoud, Alfred; Wilson, Geoffrey G.; Wende, Wolfgang
  • Nucleic Acids Research, Vol. 42, Issue 12
  • DOI: 10.1093/nar/gku447

Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms
journal, December 2021


DnaSAM: Software to perform neutrality testing for large datasets with complex null models
journal, May 2010


MBGD: microbial genome database for comparative analysis
journal, January 2003


Genome-Wide Survey of Mutual Homologous Recombination in a Highly Sexual Bacterial Species
journal, January 2012

  • Yahara, Koji; Kawai, Mikihiko; Furuta, Yoshikazu
  • Genome Biology and Evolution, Vol. 4, Issue 5
  • DOI: 10.1093/gbe/evs043

Functional identification of the DNA packaging terminase from Pseudomonas aeruginosa phage PaP3
journal, July 2012


Streptococcus mitis Strains Causing Severe Clinical Disease in Cancer Patients
journal, May 2014

  • Shelburne, Samuel A.; Sahasrabhojane, Pranoti; Saldana, Miguel
  • Emerging Infectious Diseases, Vol. 20, Issue 5
  • DOI: 10.3201/eid2005.130953

Complete Genome Sequence of Cellulomonas sp. JZ18, a Root Endophytic Bacterium Isolated from the Perennial Desert Tussock-Grass Panicum turgidum
journal, March 2021


Optimized cultivation of Campylobacter concisus from gut mucosal biopsies in inflammatory bowel disease
journal, June 2016

  • Kirk, Karina Frahm; Nielsen, Hans Linde; Thorlacius-Ussing, Ole
  • Gut Pathogens, Vol. 8, Issue 1
  • DOI: 10.1186/s13099-016-0111-7

Uncovering Earth’s virome
journal, August 2016

  • Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
  • Nature, Vol. 536, Issue 7617
  • DOI: 10.1038/nature19094

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


IMG/VR: a database of cultured and uncultured DNA Viruses and retroviruses
journal, October 2016

  • Paez-Espino, David; Chen, I. -Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1030

Prokka: rapid prokaryotic genome annotation
journal, March 2014


Why do RNA viruses recombine?
journal, July 2011

  • Simon-Loriere, Etienne; Holmes, Edward C.
  • Nature Reviews Microbiology, Vol. 9, Issue 8
  • DOI: 10.1038/nrmicro2614

A Common Evolutionary Origin for Tailed-Bacteriophage Functional Modules and Bacterial Machineries
journal, September 2011

  • Veesler, D.; Cambillau, C.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 3
  • DOI: 10.1128/MMBR.00014-11

CRISPR–Cas adaptation: insights into the mechanism of action
journal, January 2016


Mating pair stabilization mediates bacterial conjugation species specificity
journal, June 2022


Global Phage Diversity
journal, April 2003


Recombination Promoted by DNA Viruses: Phage λ to Herpes Simplex Virus
journal, September 2014


Genome-Wide Survey of Mutual Homologous Recombination in a Highly Sexual Bacterial Species
journal, January 2012

  • Yahara, Koji; Kawai, Mikihiko; Furuta, Yoshikazu
  • Genome Biology and Evolution, Vol. 4, Issue 5
  • DOI: 10.1093/gbe/evs043

CRISPRDetect: A flexible algorithm to define CRISPR arrays
journal, May 2016


Evolutionary Ecology of Prokaryotic Immune Mechanisms
journal, July 2016

  • van Houte, Stineke; Buckling, Angus; Westra, Edze R.
  • Microbiology and Molecular Biology Reviews, Vol. 80, Issue 3
  • DOI: 10.1128/mmbr.00011-16

Bacteriophages and their genomes
journal, October 2011


Recombination Promoted by DNA Viruses: Phage λ to Herpes Simplex Virus
journal, September 2014


Coinfection rates in Φ6 bacteriophage are enhanced by virus-induced changes in host cells.
text, January 2009

  • Lin, Chao,; L., Burch, Christina; B., Joseph, Sarah
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/vyp1-bq09

CRISPR–Cas adaptation: insights into the mechanism of action
journal, January 2016


Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy
journal, January 2014

  • Meier-Kolthoff, Jan P.; Hahnke, Richard L.; Petersen, Jörn
  • Standards in Genomic Sciences, Vol. 9, Issue 1
  • DOI: 10.1186/1944-3277-9-2

Efficient Inference of Recombination Hot Regions in Bacterial Genomes
journal, February 2014

  • Yahara, Koji; Didelot, Xavier; Ansari, M. Azim
  • Molecular Biology and Evolution, Vol. 31, Issue 6
  • DOI: 10.1093/molbev/msu082

ORIGINAL ARTICLE: Coinfection rates in φ6 bacteriophage are enhanced by virus-induced changes in host cells: Coinfection enhancement in φ6
journal, December 2008


Endocarditis Due to Actinomyces viscosus
journal, January 2001


Functional identification of the DNA packaging terminase from Pseudomonas aeruginosa phage PaP3
journal, July 2012


TNT, a free program for phylogenetic analysis
journal, October 2008


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Endocarditis due to Gemella haemolysans in a newly diagnosed multiple myeloma patient
journal, January 2016

  • Liu, Dongyan; Bateman, Thomas; Carr, Elisabeth
  • Journal of Community Hospital Internal Medicine Perspectives, Vol. 6, Issue 4
  • DOI: 10.3402/jchimp.v6.32357

Phages in nature
journal, January 2011

  • Clokie, Martha R. J.; Millard, Andrew D.; Letarov, Andrey V.
  • Bacteriophage, Vol. 1, Issue 1
  • DOI: 10.4161/bact.1.1.14942

Viral capsids: Mechanical characteristics, genome packaging and delivery mechanisms
journal, March 2007

  • Roos, W. H.; Ivanovska, I. L.; Evilevitch, A.
  • Cellular and Molecular Life Sciences, Vol. 64, Issue 12
  • DOI: 10.1007/s00018-007-6451-1

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
  • DOI: 10.1093/nar/gkw929

Propionibacterium acnes : infection beyond the skin
journal, December 2011

  • Perry, Alexandra; Lambert, Peter
  • Expert Review of Anti-infective Therapy, Vol. 9, Issue 12
  • DOI: 10.1586/eri.11.137

How Many Bootstrap Replicates Are Necessary?
journal, March 2010

  • Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P.
  • Journal of Computational Biology, Vol. 17, Issue 3
  • DOI: 10.1089/cmb.2009.0179

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


Bacteriophage genomics
journal, October 2008


MBGD. Microbial Genome Database for Comparative Analysis.
journal, January 2002


Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases
journal, March 2014


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
  • DOI: 10.1093/nar/gkw992

Streptococcus mitis Strains Causing Severe Clinical Disease in Cancer Patients
journal, May 2014

  • Shelburne, Samuel A.; Sahasrabhojane, Pranoti; Saldana, Miguel
  • Emerging Infectious Diseases, Vol. 20, Issue 5
  • DOI: 10.3201/eid2005.130953

Optimized cultivation of Campylobacter concisus from gut mucosal biopsies in inflammatory bowel disease
journal, June 2016

  • Kirk, Karina Frahm; Nielsen, Hans Linde; Thorlacius-Ussing, Ole
  • Gut Pathogens, Vol. 8, Issue 1
  • DOI: 10.1186/s13099-016-0111-7

Origins of Highly Mosaic Mycobacteriophage Genomes
journal, April 2003


Roary: rapid large-scale prokaryote pan genome analysis
journal, July 2015


Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea
journal, February 2021

  • Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier
  • Microbiology Resource Announcements, Vol. 10, Issue 5
  • DOI: 10.1128/mra.00297-20

Estimating Phylogenetic Trees from Distance Matrices
journal, September 1972

  • Farris, James S.
  • The American Naturalist, Vol. 106, Issue 951
  • DOI: 10.1086/282802

Virus taxonomy in the age of metagenomics
journal, January 2017

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

An essential role for the baseplate protein Gp45 in phage adsorption to Staphylococcus aureus
journal, May 2016

  • Li, Xuehua; Koç, Cengiz; Kühner, Petra
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep26455

New Bacterial Species Associated with Chronic Periodontitis
journal, May 2003


Propionibacterium acnes : infection beyond the skin
journal, December 2011

  • Perry, Alexandra; Lambert, Peter
  • Expert Review of Anti-infective Therapy, Vol. 9, Issue 12
  • DOI: 10.1586/eri.11.137

DnaSAM: Software to perform neutrality testing for large datasets with complex null models
journal, May 2010


CRISPR Immunity Drives Rapid Phage Genome Evolution in Streptococcus thermophilus
journal, April 2015


Human Case of Atopobium rimae Bacteremia
journal, February 2009

  • Angelakis, Emmanouil; Roux, Véronique; Raoult, Didier
  • Emerging Infectious Diseases, Vol. 15, Issue 2
  • DOI: 10.3201/eid1502.071399

Resolving the paradox of sex and recombination
journal, April 2002

  • Otto, Sarah P.; Lenormand, Thomas
  • Nature Reviews Genetics, Vol. 3, Issue 4
  • DOI: 10.1038/nrg761

TNT, a free program for phylogenetic analysis
journal, October 2008


Endocarditis due to Gemella haemolysans in a newly diagnosed multiple myeloma patient
journal, January 2016

  • Liu, Dongyan; Bateman, Thomas; Carr, Elisabeth
  • Journal of Community Hospital Internal Medicine Perspectives, Vol. 6, Issue 4
  • DOI: 10.3402/jchimp.v6.32357

Endocarditis Due to Actinomyces viscosus
journal, January 2001


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
  • DOI: 10.1038/nprot.2017.063

Endocarditis Due to Actinomyces viscosus
journal, January 2001


The Janus-Face of Bacteriophages across Human Body Habitats
text, January 2016


ORIGINAL ARTICLE: Coinfection rates in φ6 bacteriophage are enhanced by virus-induced changes in host cells: Coinfection enhancement in φ6
journal, December 2008


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
  • DOI: 10.1093/nar/gkw290

IMG/VR: a database of cultured and uncultured DNA Viruses and retroviruses
journal, October 2016

  • Paez-Espino, David; Chen, I. -Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1030

Uncovering Earth’s virome
journal, August 2016

  • Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A.
  • Nature, Vol. 536, Issue 7617
  • DOI: 10.1038/nature19094

Why do RNA viruses recombine?
journal, July 2011

  • Simon-Loriere, Etienne; Holmes, Edward C.
  • Nature Reviews Microbiology, Vol. 9, Issue 8
  • DOI: 10.1038/nrmicro2614

The Janus-Face of Bacteriophages across Human Body Habitats
text, January 2016


Bacteriophage genomics
journal, October 2003


How Many Bootstrap Replicates Are Necessary?
journal, March 2010

  • Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P.
  • Journal of Computational Biology, Vol. 17, Issue 3
  • DOI: 10.1089/cmb.2009.0179

Rhizosphere bacteriome structure and functions
journal, February 2022


The role of bacteriophages in periodontal health and disease
journal, October 2016

  • Pinto, Graça; Silva, Maria Daniela; Peddey, Mark
  • Future Microbiology, Vol. 11, Issue 10
  • DOI: 10.2217/fmb-2016-0081

Bacteriophage genomics
journal, October 2008


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens
journal, March 2021


Statistical Properties of the Number of Recombination Events in the History of a Sample of dna Sequences
journal, September 1985


Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory
journal, September 2017


Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy
journal, January 2014

  • Meier-Kolthoff, Jan P.; Hahnke, Richard L.; Petersen, Jörn
  • Standards in Genomic Sciences, Vol. 9, Issue 1
  • DOI: 10.1186/1944-3277-9-2

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
  • DOI: 10.1038/ismej.2017.16

MVP: a microbe–phage interaction database
journal, November 2017

  • Gao, Na L.; Zhang, Chengwei; Zhang, Zhanbing
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx1124

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
  • DOI: 10.1038/nmeth.1818

Bacteremia Caused by Capnocytophaga Species in Patients with Neutropenia and Cancer: Results of a Multicenter Study
journal, August 2001

  • Martino, Rodrigo; Rámila, Elena; Capdevila, Josep A.
  • Clinical Infectious Diseases, Vol. 33, Issue 4
  • DOI: 10.1086/322649

New Bacterial Species Associated with Chronic Periodontitis
journal, May 2003


The Human Gut Phage Community and Its Implications for Health and Disease
journal, June 2017

  • Manrique, Pilar; Dills, Michael; Young, Mark
  • Viruses, Vol. 9, Issue 6
  • DOI: 10.3390/v9060141

Resolving the paradox of sex and recombination
journal, April 2002

  • Otto, Sarah P.; Lenormand, Thomas
  • Nature Reviews Genetics, Vol. 3, Issue 4
  • DOI: 10.1038/nrg761

Type II restriction endonucleases — a historical perspective and more
journal, June 2016

  • Pingoud, Alfred; Wilson, Geoffrey G.; Wende, Wolfgang
  • Nucleic Acids Research, Vol. 44, Issue 16
  • DOI: 10.1093/nar/gkw513

CRISPRDetect: A flexible algorithm to define CRISPR arrays
journal, May 2016


Global transcription of CRISPR loci in the human oral cavity
journal, May 2015


Genome sequence-based species delimitation with confidence intervals and improved distance functions
journal, January 2013

  • Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter
  • BMC Bioinformatics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2105-14-60

Bacteriophages and their genomes
journal, October 2011


Bacteriophage lysis: mechanism and regulation
journal, September 1992


Statistical Properties of the Number of Recombination Events in the History of a Sample of dna Sequences
journal, September 1985


Works referencing / citing this record:

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journal, August 2019

  • Yahara, Koji; Lehours, Philippe; Vale, Filipa F.
  • Microbial Genomics, Vol. 5, Issue 8
  • DOI: 10.1099/mgen.0.000282

Ecological and Evolutionary Processes Shaping Viral Genetic Diversity
text, January 2019

  • Retel, Cas; Märkle, Hanna; Becks, Lutz
  • Molecular Diversity Preservation International MDPI
  • DOI: 10.7892/boris.128447

Analysis of genetic recombination and the pan-genome of a highly recombinogenic bacteriophage species
journal, August 2019

  • Yahara, Koji; Lehours, Philippe; Vale, Filipa F.
  • Microbial Genomics, Vol. 5, Issue 8
  • DOI: 10.1099/mgen.0.000282

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

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