DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems

Abstract

Here, current understanding of microorganism–virus interactions, which shape the evolution and functioning of Earth’s ecosystems, is based primarily on cultivated organisms. Here we investigate thousands of viral and microbial genomes recovered using a cultivation independent approach to study the frequency, variety and taxonomic distribution of viral defence mechanisms. CRISPR-Cas systems that confer microorganisms with immunity to viruses are present in only 10% of 1,724 sampled microorganisms, compared with previous reports of 40% occurrence in bacteria and 81% in archaea. We attribute this large difference to the lack of CRISPR-Cas systems across major bacterial lineages that have no cultivated representatives. We correlate absence of CRISPR-Cas with lack of nucleotide biosynthesis capacity and a symbiotic lifestyle. Restriction systems are well represented in these lineages and might provide both non-specific viral defence and access to nucleotides.

Authors:
 [1];  [2]; ORCiD logo [3];  [1];  [1];  [1];  [1];  [4]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  2. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Stanford Univ., CA (United States). Dept. of Microbiology and Immunology
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  4. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science and Dept. of Environmental Science, Policy and Management
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1469126
Alternate Identifier(s):
OSTI ID: 1253373
Grant/Contract Number:  
AC02-05CH11231; SC0004918
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biological sciences; genetics; microbiology; virology

Citation Formats

Burstein, David, Sun, Christine L., Brown, Christopher T., Sharon, Itai, Anantharaman, Karthik, Probst, Alexander J., Thomas, Brian C., and Banfield, Jillian F. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. United States: N. p., 2016. Web. doi:10.1038/ncomms10613.
Burstein, David, Sun, Christine L., Brown, Christopher T., Sharon, Itai, Anantharaman, Karthik, Probst, Alexander J., Thomas, Brian C., & Banfield, Jillian F. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. United States. https://doi.org/10.1038/ncomms10613
Burstein, David, Sun, Christine L., Brown, Christopher T., Sharon, Itai, Anantharaman, Karthik, Probst, Alexander J., Thomas, Brian C., and Banfield, Jillian F. Wed . "Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems". United States. https://doi.org/10.1038/ncomms10613. https://www.osti.gov/servlets/purl/1469126.
@article{osti_1469126,
title = {Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems},
author = {Burstein, David and Sun, Christine L. and Brown, Christopher T. and Sharon, Itai and Anantharaman, Karthik and Probst, Alexander J. and Thomas, Brian C. and Banfield, Jillian F.},
abstractNote = {Here, current understanding of microorganism–virus interactions, which shape the evolution and functioning of Earth’s ecosystems, is based primarily on cultivated organisms. Here we investigate thousands of viral and microbial genomes recovered using a cultivation independent approach to study the frequency, variety and taxonomic distribution of viral defence mechanisms. CRISPR-Cas systems that confer microorganisms with immunity to viruses are present in only 10% of 1,724 sampled microorganisms, compared with previous reports of 40% occurrence in bacteria and 81% in archaea. We attribute this large difference to the lack of CRISPR-Cas systems across major bacterial lineages that have no cultivated representatives. We correlate absence of CRISPR-Cas with lack of nucleotide biosynthesis capacity and a symbiotic lifestyle. Restriction systems are well represented in these lineages and might provide both non-specific viral defence and access to nucleotides.},
doi = {10.1038/ncomms10613},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {Wed Feb 03 00:00:00 EST 2016},
month = {Wed Feb 03 00:00:00 EST 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 131 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, November 2014

  • Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
  • Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299
  • DOI: 10.1093/nar/gku1046

Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization
journal, August 2012

  • Sharon, I.; Morowitz, M. J.; Thomas, B. C.
  • Genome Research, Vol. 23, Issue 1
  • DOI: 10.1101/gr.142315.112

CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007

  • Grissa, I.; Vergnaud, G.; Pourcel, C.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm360

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Community-wide analysis of microbial genome sequence signatures
journal, January 2009

  • Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
  • Genome Biology, Vol. 10, Issue 8
  • DOI: 10.1186/gb-2009-10-8-r85

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


Classification and evolution of type II CRISPR-Cas systems
journal, April 2014

  • Chylinski, Krzysztof; Makarova, Kira S.; Charpentier, Emmanuelle
  • Nucleic Acids Research, Vol. 42, Issue 10
  • DOI: 10.1093/nar/gku241

CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes
journal, March 2007


CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea
journal, March 2008

  • Sorek, Rotem; Kunin, Victor; Hugenholtz, Philip
  • Nature Reviews Microbiology, Vol. 6, Issue 3
  • DOI: 10.1038/nrmicro1793

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


CRISPR adaptation biases explain preference for acquisition of foreign DNA
journal, April 2015

  • Levy, Asaf; Goren, Moran G.; Yosef, Ido
  • Nature, Vol. 520, Issue 7548
  • DOI: 10.1038/nature14302

IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

Self-targeting by CRISPR: gene regulation or autoimmunity?
journal, August 2010


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
  • DOI: 10.1093/molbev/mst010

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA
journal, November 2010

  • Garneau, Josiane E.; Dupuis, Marie-Ève; Villion, Manuela
  • Nature, Vol. 468, Issue 7320
  • DOI: 10.1038/nature09523

Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling
journal, March 2015

  • Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C.
  • Current Biology, Vol. 25, Issue 6
  • DOI: 10.1016/j.cub.2015.01.014

Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla
journal, October 2013


InterProScan 5: genome-scale protein function classification
journal, January 2014


TADB: a web-based resource for Type 2 toxin–antitoxin loci in bacteria and archaea
journal, October 2010

  • Shao, Yucheng; Harrison, Ewan M.; Bi, Dexi
  • Nucleic Acids Research, Vol. 39, Issue suppl_1
  • DOI: 10.1093/nar/gkq908

Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus
journal, August 2015

  • Vale, Pedro F.; Lafforgue, Guillaume; Gatchitch, Francois
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1812
  • DOI: 10.1098/rspb.2015.1270

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


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Evolution and classification of the CRISPR–Cas systems
journal, May 2011

  • Makarova, Kira S.; Haft, Daniel H.; Barrangou, Rodolphe
  • Nature Reviews Microbiology, Vol. 9, Issue 6, p. 467-477
  • DOI: 10.1038/nrmicro2577

BREX is a novel phage resistance system widespread in microbial genomes
journal, December 2014


Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla: High CO
journal, April 2015

  • Emerson, Joanne B.; Thomas, Brian C.; Alvarez, Walter
  • Environmental Microbiology, Vol. 18, Issue 6
  • DOI: 10.1111/1462-2920.12817

A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity
journal, June 2012


Accelerated Profile HMM Searches
journal, October 2011


Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015

  • Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
  • Nature, Vol. 523, Issue 7559
  • DOI: 10.1038/nature14486

Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle
journal, December 2014

  • He, Xuesong; McLean, Jeffrey S.; Edlund, Anna
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419038112

The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes
journal, April 2006


Intracellular survival by Chlamydia . Microreview
journal, August 2000


Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae
journal, March 2015


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

Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense
journal, April 2015

  • Westra, Edze R.; van Houte, Stineke; Oyesiku-Blakemore, Sam
  • Current Biology, Vol. 25, Issue 8
  • DOI: 10.1016/j.cub.2015.01.065

Identification of genes that are associated with DNA repeats in prokaryotes
journal, March 2002


Diverse uncultivated ultra-small bacterial cells in groundwater
journal, February 2015

  • Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7372

Phage abortive infection in lactococci: variations on a theme
journal, August 2005

  • Chopin, Marie-Christine; Chopin, Alain; Bidnenko, Elena
  • Current Opinion in Microbiology, Vol. 8, Issue 4
  • DOI: 10.1016/j.mib.2005.06.006

The Pfam protein families database
journal, November 2011

  • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1065

RNA-Guided Human Genome Engineering via Cas9
journal, January 2013


Comparative analysis of CRISPR loci in lactic acid bacteria genomes
journal, April 2009

  • Horvath, Philippe; Coûté-Monvoisin, Anne-Claire; Romero, Dennis A.
  • International Journal of Food Microbiology, Vol. 131, Issue 1
  • DOI: 10.1016/j.ijfoodmicro.2008.05.030

Multiplex Genome Engineering Using CRISPR/Cas Systems
journal, January 2013


Restriction and Modification Systems
journal, December 1991


HMMER web server: interactive sequence similarity searching
journal, May 2011

  • Finn, R. D.; Clements, J.; Eddy, S. R.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr367

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

EMBOSS: The European Molecular Biology Open Software Suite
journal, June 2000


PHAST: A Fast Phage Search Tool
journal, June 2011

  • Zhou, Y.; Liang, Y.; Lynch, K. H.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr485

The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle
journal, July 2015


Illuminating the Evolutionary History of Chlamydiae
journal, April 2004


REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, October 2009

  • Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp874

Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021


CRISPR elements in the Thermococcales: evidence for associated horizontal gene transfer inPyrococcus furiosus
journal, December 2009

  • Portillo, M. C.; Gonzalez, J. M.
  • Journal of Applied Genetics, Vol. 50, Issue 4
  • DOI: 10.1007/bf03195703

The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes
journal, April 2006


Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling
journal, March 2015

  • Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C.
  • Current Biology, Vol. 25, Issue 6
  • DOI: 10.1016/j.cub.2015.01.014

Evolution: Parasite Pressure Favors Fortress-like Defence
journal, April 2015


Phage abortive infection in lactococci: variations on a theme
journal, August 2005

  • Chopin, Marie-Christine; Chopin, Alain; Bidnenko, Elena
  • Current Opinion in Microbiology, Vol. 8, Issue 4
  • DOI: 10.1016/j.mib.2005.06.006

Diverse uncultivated ultra-small bacterial cells in groundwater
journal, February 2015

  • Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7372

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

Identification of genes that are associated with DNA repeats in prokaryotes
journal, March 2002


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


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
  • DOI: 10.1093/molbev/mst010

CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007

  • Grissa, I.; Vergnaud, G.; Pourcel, C.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm360

TADB: a web-based resource for Type 2 toxin–antitoxin loci in bacteria and archaea
journal, October 2010

  • Shao, Yucheng; Harrison, Ewan M.; Bi, Dexi
  • Nucleic Acids Research, Vol. 39, Issue suppl_1
  • DOI: 10.1093/nar/gkq908

The Pfam protein families database
journal, November 2011

  • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1065

HMMER web server: interactive sequence similarity searching
journal, May 2011

  • Finn, R. D.; Clements, J.; Eddy, S. R.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr367

IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
journal, November 2014

  • Roberts, Richard J.; Vincze, Tamas; Posfai, Janos
  • Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299
  • DOI: 10.1093/nar/gku1046

Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization
journal, August 2012

  • Sharon, I.; Morowitz, M. J.; Thomas, B. C.
  • Genome Research, Vol. 23, Issue 1
  • DOI: 10.1101/gr.142315.112

Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses
journal, September 2007


Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity
journal, June 2012


RNA-Guided Human Genome Engineering via Cas9
journal, January 2013


Evolutionary Dynamics of the Prokaryotic Adaptive Immunity System CRISPR-Cas in an Explicit Ecological Context
journal, June 2013

  • Iranzo, J.; Lobkovsky, A. E.; Wolf, Y. I.
  • Journal of Bacteriology, Vol. 195, Issue 17
  • DOI: 10.1128/jb.00412-13

Genome Sequence of the Fish Pathogen Renibacterium salmoninarum Suggests Reductive Evolution away from an Environmental Arthrobacter Ancestor
journal, August 2008

  • Wiens, G. D.; Rockey, D. D.; Wu, Z.
  • Journal of Bacteriology, Vol. 190, Issue 21
  • DOI: 10.1128/jb.00721-08

Defense Islands in Bacterial and Archaeal Genomes and Prediction of Novel Defense Systems
journal, September 2011

  • Makarova, K. S.; Wolf, Y. I.; Snir, S.
  • Journal of Bacteriology, Vol. 193, Issue 21
  • DOI: 10.1128/jb.05535-11

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
  • DOI: 10.1128/mmbr.00011-11

Restriction and Modification Systems
journal, December 1991


Community-wide analysis of microbial genome sequence signatures
journal, January 2009

  • Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
  • Genome Biology, Vol. 10, Issue 8
  • DOI: 10.1186/gb-2009-10-8-r85

Accelerated Profile HMM Searches
journal, October 2011


Works referencing / citing this record:

Anti-CRISPR: discovery, mechanism and function
journal, October 2017

  • Pawluk, April; Davidson, Alan R.; Maxwell, Karen L.
  • Nature Reviews Microbiology, Vol. 16, Issue 1
  • DOI: 10.1038/nrmicro.2017.120

Unlinked rRNA genes are widespread among bacteria and archaea
journal, November 2019


Long-term genomic coevolution of host-parasite interaction in the natural environment
journal, July 2017


Defining the human gut host–phage network through single-cell viral tagging
journal, August 2019


Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018

  • Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik
  • Nature Reviews Microbiology, Vol. 16, Issue 10
  • DOI: 10.1038/s41579-018-0076-2

Comparative genomics and genome biology of Campylobacter showae
journal, January 2019


A matter of background: DNA repair pathways as a possible cause for the sparse distribution of CRISPR-Cas systems in bacteria
journal, March 2019

  • Bernheim, Aude; Bikard, David; Touchon, Marie
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772
  • DOI: 10.1098/rstb.2018.0088

Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome
posted_content, August 2018

  • Goltsman, Daniela S. Aliaga; Sun, Christine L.; Proctor, Diana M.
  • DOI: 10.1101/266700

Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome
journal, September 2018

  • Goltsman, Daniela S. Aliaga; Sun, Christine L.; Proctor, Diana M.
  • Genome Research, Vol. 28, Issue 10
  • DOI: 10.1101/gr.236000.118

Anti‐CRISPR proteins targeting the CRISPR‐Cas system enrich the toolkit for genetic engineering
journal, November 2019

  • Liu, Qiong; Zhang, Hongxia; Huang, Xiaotian
  • The FEBS Journal, Vol. 287, Issue 4
  • DOI: 10.1111/febs.15139

Adapting Drug Approval Pathways for Bacteriophage-Based Therapeutics
journal, August 2016

  • Cooper, Callum J.; Khan Mirzaei, Mohammadali; Nilsson, Anders S.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.01209

CRISPR-Cas Systems Features and the Gene-Reservoir Role of Coagulase-Negative Staphylococci
journal, August 2017

  • Rossi, Ciro C.; Souza-Silva, Thaysa; Araújo-Alves, Amanda V.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01545

Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales
journal, September 2016


Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants
journal, December 2019

  • Makarova, Kira S.; Wolf, Yuri I.; Iranzo, Jaime
  • Nature Reviews Microbiology, Vol. 18, Issue 2
  • DOI: 10.1038/s41579-019-0299-x

Atypical organizations and epistatic interactions of CRISPRs and cas clusters in genomes and their mobile genetic elements
journal, November 2019

  • Bernheim, Aude; Bikard, David; Touchon, Marie
  • Nucleic Acids Research
  • DOI: 10.1093/nar/gkz1091

The effect of bacterial mutation rate on the evolution of CRISPR-Cas adaptive immunity
journal, March 2019

  • Chevallereau, Anne; Meaden, Sean; van Houte, Stineke
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772
  • DOI: 10.1098/rstb.2018.0094

The ecology and evolution of microbial CRISPR-Cas adaptive immune systems
journal, March 2019

  • Westra, Edze R.; van Houte, Stineke; Gandon, Sylvain
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772
  • DOI: 10.1098/rstb.2019.0101

Co-occurrence of multiple CRISPRs and cas clusters suggests epistatic interactions
posted_content, March 2019

  • Bernheim, Aude; Bikard, David; Touchon, Marie
  • bioRxiv
  • DOI: 10.1101/592600

Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
journal, November 2019

  • Sieber, Christian M. K.; Paul, Blair G.; Castelle, Cindy J.
  • mBio, Vol. 10, Issue 6
  • DOI: 10.1128/mBio.02128-19

Phylogenomics of Cas4 family nucleases
journal, November 2017

  • Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I.
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-1081-1

Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity
journal, April 2020


An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes
journal, November 2016


Bacteriophages and Bacterial Plant Diseases
journal, January 2017


Bacterial and Archaeal Viruses of Himalayan Hot Springs at Manikaran Modulate Host Genomes
journal, December 2018


Reconstructing the functions of endosymbiotic Mollicutes in fungus-growing ants
journal, November 2018

  • Sapountzis, Panagiotis; Zhukova, Mariya; Shik, Jonathan Z.
  • eLife, Vol. 7
  • DOI: 10.7554/elife.39209

New CRISPR–Cas systems from uncultivated microbes
journal, December 2016

  • Burstein, David; Harrington, Lucas B.; Strutt, Steven C.
  • Nature, Vol. 542, Issue 7640
  • DOI: 10.1038/nature21059

The enigmatic archaeal virosphere
journal, November 2017

  • Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick
  • Nature Reviews Microbiology, Vol. 15, Issue 12
  • DOI: 10.1038/nrmicro.2017.125

Visualization and prediction of CRISPR incidence in microbial trait-space to identify drivers of antiviral immune strategy
journal, June 2019

  • Weissman, Jake L.; Laljani, Rohan M. R.; Fagan, William F.
  • The ISME Journal, Vol. 13, Issue 10
  • DOI: 10.1038/s41396-019-0411-2

Long-term genomic coevolution of host-parasite interaction in the natural environment
posted_content, January 2017

  • Laanto, Elina; Hoikkala, Ville; Ravantti, Janne
  • bioRxiv
  • DOI: 10.1101/101576

Saccharibacteria (TM7) in the Human Oral Microbiome
journal, February 2019


Insights Obtained by Culturing Saccharibacteria With Their Bacterial Hosts
journal, February 2020


Optimizing de novo genome assembly from PCR-amplified metagenomes
journal, January 2019


Measurement of bacterial replication rates in microbial communities
journal, November 2016

  • Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C.
  • Nature Biotechnology, Vol. 34, Issue 12
  • DOI: 10.1038/nbt.3704

Systematic prediction of functionally linked genes in bacterial and archaeal genomes
journal, September 2019


Genome-wide correlation analysis suggests different roles of CRISPR-Cas systems in the acquisition of antibiotic resistance genes in diverse species
journal, March 2019

  • Shehreen, Saadlee; Chyou, Te-yuan; Fineran, Peter C.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772
  • DOI: 10.1098/rstb.2018.0384

Phages actively challenge niche communities in the Antarctic soils
posted_content, January 2020


Tissue- and Population-Level Microbiome Analysis of the Wasp Spider Argiope bruennichi Identified a Novel Dominant Bacterial Symbiont
journal, December 2019


New CRISPR–Cas systems from uncultivated microbes
journal, December 2016

  • Burstein, David; Harrington, Lucas B.; Strutt, Steven C.
  • Nature, Vol. 542, Issue 7640
  • DOI: 10.1038/nature21059

Visualization and prediction of CRISPR incidence in microbial trait-space to identify drivers of antiviral immune strategy
journal, June 2019

  • Weissman, Jake L.; Laljani, Rohan M. R.; Fagan, William F.
  • The ISME Journal, Vol. 13, Issue 10
  • DOI: 10.1038/s41396-019-0411-2

Exploring the ecological function of CRISPR-Cas virus defense
journal, August 2016


CRISPRdisco: An Automated Pipeline for the Discovery and Analysis of CRISPR-Cas Systems
journal, April 2018

  • Crawley, Alexandra B.; Henriksen, James R.; Barrangou, Rodolphe
  • The CRISPR Journal, Vol. 1, Issue 2
  • DOI: 10.1089/crispr.2017.0022

A matter of background: DNA repair pathways as a possible cause for the sparse distribution of CRISPR-Cas systems in bacteria
journal, March 2019

  • Bernheim, Aude; Bikard, David; Touchon, Marie
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772
  • DOI: 10.1098/rstb.2018.0088

Long-term genomic coevolution of host-parasite interaction in the natural environment
posted_content, January 2017

  • Laanto, Elina; Hoikkala, Ville; Ravantti, Janne
  • bioRxiv
  • DOI: 10.1101/101576

Phylogenomics of Cas4 family nucleases
journal, November 2017

  • Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I.
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-1081-1

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes
journal, November 2016


CRISPR-Cas Defense System and Potential Prophages in Cyanobacteria Associated with the Coral Black Band Disease
journal, December 2016

  • Buerger, Patrick; Wood-Charlson, Elisha M.; Weynberg, Karen D.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.02077

Bacteriophages and Bacterial Plant Diseases
journal, January 2017


CRISPR-Cas Systems Features and the Gene-Reservoir Role of Coagulase-Negative Staphylococci
journal, August 2017

  • Rossi, Ciro C.; Souza-Silva, Thaysa; Araújo-Alves, Amanda V.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01545

Incomplete Selective Sweeps of Microcystis Population Detected by the Leader-End CRISPR Fragment Analysis in a Natural Pond
journal, March 2018


Bacterial and Archaeal Viruses of Himalayan Hot Springs at Manikaran Modulate Host Genomes
journal, December 2018


Prokaryotic Genome Expansion Is Facilitated by Phages and Plasmids but Impaired by CRISPR
journal, October 2019


Multiple Origins and Specific Evolution of CRISPR/Cas9 Systems in Minimal Bacteria (Mollicutes)
journal, November 2019

  • Ipoutcha, Thomas; Tsarmpopoulos, Iason; Talenton, Vincent
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.02701

Detection and variability analyses of CRISPR-like loci in the H. pylori genome
journal, September 2018


Reconstructing the functions of endosymbiotic Mollicutes in fungus-growing ants
journal, November 2018

  • Sapountzis, Panagiotis; Zhukova, Mariya; Shik, Jonathan Z.
  • eLife, Vol. 7
  • DOI: 10.7554/elife.39209