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

Burstein, David; Sun, Christine L.; Brown, Christopher T.; Sharon, Itai; Anantharaman, Karthik; Probst, Alexander J.; Thomas, Brian C.; Banfield, Jillian F.

doi:10.1038/ncomms10613

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

Journal Article · Wed Feb 03 00:00:00 EST 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms10613· OSTI ID:1469126

Burstein, David ^[1]; Sun, Christine L. ^[2];

^[3]; Sharon, Itai ^[1]; Anantharaman, Karthik ^[1]; Probst, Alexander J. ^[1]; Thomas, Brian C. ^[1]; Banfield, Jillian F. ^[4]

Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Stanford Univ., CA (United States). Dept. of Microbiology and Immunology
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science and Dept. of Environmental Science, Policy and Management

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0004918

OSTI ID:: 1469126

Alternate ID(s):: OSTI ID: 1253373

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 131 works

Citation information provided by
Web of Science

References (61)

REBASE—a database for DNA restriction and modification: enzymes, genes and genomes Roberts, Richard J.; Vincze, Tamas; Posfai, Janos Nucleic Acids Research, Vol. 43, Issue D1, p. D298-D299 https://doi.org/10.1093/nar/gku1046	journal	November 2014
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Sharon, I.; Morowitz, M. J.; Thomas, B. C. Genome Research, Vol. 23, Issue 1 https://doi.org/10.1101/gr.142315.112	journal	August 2012
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
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
UniRef: comprehensive and non-redundant UniProt reference clusters Suzek, B. E.; Huang, H.; McGarvey, P. Bioinformatics, Vol. 23, Issue 10 https://doi.org/10.1093/bioinformatics/btm098	journal	March 2007
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Community-wide analysis of microbial genome sequence signatures Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J. Genome Biology, Vol. 10, Issue 8 https://doi.org/10.1186/gb-2009-10-8-r85	journal	January 2009
CRISPR Immunity Drives Rapid Phage Genome Evolution in Streptococcus thermophilus Paez-Espino, David; Sharon, Itai; Morovic, Wesley mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mBio.00262-15	journal	April 2015
Classification and evolution of type II CRISPR-Cas systems Chylinski, Krzysztof; Makarova, Kira S.; Charpentier, Emmanuelle Nucleic Acids Research, Vol. 42, Issue 10 https://doi.org/10.1093/nar/gku241	journal	April 2014
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
CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea Sorek, Rotem; Kunin, Victor; Hugenholtz, Philip Nature Reviews Microbiology, Vol. 6, Issue 3 https://doi.org/10.1038/nrmicro1793	journal	March 2008
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
CRISPR adaptation biases explain preference for acquisition of foreign DNA Levy, Asaf; Goren, Moran G.; Yosef, Ido Nature, Vol. 520, Issue 7548 https://doi.org/10.1038/nature14302	journal	April 2015
IMG 4 version of the integrated microbial genomes comparative analysis system Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt963	journal	October 2013
Self-targeting by CRISPR: gene regulation or autoimmunity? Stern, Adi; Keren, Leeat; Wurtzel, Omri Trends in Genetics, Vol. 26, Issue 8 https://doi.org/10.1016/j.tig.2010.05.008	journal	August 2010
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA Garneau, Josiane E.; Dupuis, Marie-Ève; Villion, Manuela Nature, Vol. 468, Issue 7320 https://doi.org/10.1038/nature09523	journal	November 2010
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C. Current Biology, Vol. 25, Issue 6 https://doi.org/10.1016/j.cub.2015.01.014	journal	March 2015
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla Kantor, Rose S.; Wrighton, Kelly C.; Handley, Kim M. mBio, Vol. 4, Issue 5 https://doi.org/10.1128/mBio.00708-13	journal	October 2013
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
TADB: a web-based resource for Type 2 toxin–antitoxin loci in bacteria and archaea Shao, Yucheng; Harrison, Ewan M.; Bi, Dexi Nucleic Acids Research, Vol. 39, Issue suppl_1 https://doi.org/10.1093/nar/gkq908	journal	October 2010
Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus Vale, Pedro F.; Lafforgue, Guillaume; Gatchitch, Francois Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1812 https://doi.org/10.1098/rspb.2015.1270	journal	August 2015
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Evolution and classification of the CRISPR–Cas systems Makarova, Kira S.; Haft, Daniel H.; Barrangou, Rodolphe Nature Reviews Microbiology, Vol. 9, Issue 6, p. 467-477 https://doi.org/10.1038/nrmicro2577	journal	May 2011
BREX is a novel phage resistance system widespread in microbial genomes Goldfarb, Tamara; Sberro, Hila; Weinstock, Eyal The EMBO Journal, Vol. 34, Issue 2 https://doi.org/10.15252/embj.201489455	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 Emerson, Joanne B.; Thomas, Brian C.; Alvarez, Walter Environmental Microbiology, Vol. 18, Issue 6 https://doi.org/10.1111/1462-2920.12817	journal	April 2015
A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity Jinek, M.; Chylinski, K.; Fonfara, I. Science, Vol. 337, Issue 6096, p. 816-821 https://doi.org/10.1126/science.1225829	journal	June 2012
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
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
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes Godde, James S.; Bickerton, Amanda Journal of Molecular Evolution, Vol. 62, Issue 6 https://doi.org/10.1007/s00239-005-0223-z	journal	April 2006
Intracellular survival by Chlamydia . Microreview Wyrick, Priscilla B. Cellular Microbiology, Vol. 2, Issue 4 https://doi.org/10.1046/j.1462-5822.2000.00059.x	journal	August 2000
Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae Pagnier, Isabelle; Yutin, Natalya; Croce, Olivier Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0043-z	journal	March 2015
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense Westra, Edze R.; van Houte, Stineke; Oyesiku-Blakemore, Sam Current Biology, Vol. 25, Issue 8 https://doi.org/10.1016/j.cub.2015.01.065	journal	April 2015
Identification of genes that are associated with DNA repeats in prokaryotes Jansen, Ruud.; Embden, Jan. D. A. van; Gaastra, Wim. Molecular Microbiology, Vol. 43, Issue 6 https://doi.org/10.1046/j.1365-2958.2002.02839.x	journal	March 2002
Diverse uncultivated ultra-small bacterial cells in groundwater Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7372	journal	February 2015
Phage abortive infection in lactococci: variations on a theme Chopin, Marie-Christine; Chopin, Alain; Bidnenko, Elena Current Opinion in Microbiology, Vol. 8, Issue 4 https://doi.org/10.1016/j.mib.2005.06.006	journal	August 2005
The Pfam protein families database Punta, M.; Coggill, P. C.; Eberhardt, R. Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1065	journal	November 2011
RNA-Guided Human Genome Engineering via Cas9 Mali, P.; Yang, L.; Esvelt, K. M. Science, Vol. 339, Issue 6121, p. 823-826 https://doi.org/10.1126/science.1232033	journal	January 2013
Comparative analysis of CRISPR loci in lactic acid bacteria genomes Horvath, Philippe; Coûté-Monvoisin, Anne-Claire; Romero, Dennis A. International Journal of Food Microbiology, Vol. 131, Issue 1 https://doi.org/10.1016/j.ijfoodmicro.2008.05.030	journal	April 2009
Multiplex Genome Engineering Using CRISPR/Cas Systems Cong, L.; Ran, F. A.; Cox, D. Science, Vol. 339, Issue 6121, p. 819-823 https://doi.org/10.1126/science.1231143	journal	January 2013
Restriction and Modification Systems Wilson, Geoffrey G.; Murray, Noreen E. Annual Review of Genetics, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.ge.25.120191.003101	journal	December 1991
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
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
EMBOSS: The European Molecular Biology Open Software Suite Rice, Peter; Longden, Ian; Bleasby, Alan Trends in Genetics, Vol. 16, Issue 6 https://doi.org/10.1016/S0168-9525(00)02024-2	journal	June 2000
PHAST: A Fast Phage Search Tool Zhou, Y.; Liang, Y.; Lynch, K. H. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr485	journal	June 2011
The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle Nelson, William C.; Stegen, James C. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00713	journal	July 2015
Illuminating the Evolutionary History of Chlamydiae Horn, M. Science, Vol. 304, Issue 5671 https://doi.org/10.1126/science.1096330	journal	April 2004
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes Roberts, Richard J.; Vincze, Tamas; Posfai, Janos Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp874	journal	October 2009
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
CRISPR elements in the Thermococcales: evidence for associated horizontal gene transfer inPyrococcus furiosus Portillo, M. C.; Gonzalez, J. M. Journal of Applied Genetics, Vol. 50, Issue 4 https://doi.org/10.1007/bf03195703	journal	December 2009
Evolution: Parasite Pressure Favors Fortress-like Defence Graham, Andrea L. Current Biology, Vol. 25, Issue 8 https://doi.org/10.1016/j.cub.2015.02.043	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
Evolutionary Dynamics of the Prokaryotic Adaptive Immunity System CRISPR-Cas in an Explicit Ecological Context Iranzo, J.; Lobkovsky, A. E.; Wolf, Y. I. Journal of Bacteriology, Vol. 195, Issue 17 https://doi.org/10.1128/jb.00412-13	journal	June 2013
Genome Sequence of the Fish Pathogen Renibacterium salmoninarum Suggests Reductive Evolution away from an Environmental Arthrobacter Ancestor Wiens, G. D.; Rockey, D. D.; Wu, Z. Journal of Bacteriology, Vol. 190, Issue 21 https://doi.org/10.1128/jb.00721-08	journal	August 2008
Defense Islands in Bacterial and Archaeal Genomes and Prediction of Novel Defense Systems Makarova, K. S.; Wolf, Y. I.; Snir, S. Journal of Bacteriology, Vol. 193, Issue 21 https://doi.org/10.1128/jb.05535-11	journal	September 2011
Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere Krupovic, M.; Prangishvili, D.; Hendrix, R. W. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4 https://doi.org/10.1128/mmbr.00011-11	journal	November 2011

Cited By (47)

Anti-CRISPR: discovery, mechanism and function Pawluk, April; Davidson, Alan R.; Maxwell, Karen L. Nature Reviews Microbiology, Vol. 16, Issue 1 https://doi.org/10.1038/nrmicro.2017.120	journal	October 2017
Unlinked rRNA genes are widespread among bacteria and archaea Brewer, Tess E.; Albertsen, Mads; Edwards, Arwyn The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0552-3	journal	November 2019
Long-term genomic coevolution of host-parasite interaction in the natural environment Laanto, Elina; Hoikkala, Ville; Ravantti, Janne Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00158-7	journal	July 2017
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
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
Comparative genomics and genome biology of Campylobacter showae Hsu, Tiffany; Gemmell, Matthew R.; Franzosa, Eric A. Emerging Microbes & Infections, Vol. 8, Issue 1 https://doi.org/10.1080/22221751.2019.1622455	journal	January 2019
A matter of background: DNA repair pathways as a possible cause for the sparse distribution of CRISPR-Cas systems in bacteria Bernheim, Aude; Bikard, David; Touchon, Marie Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772 https://doi.org/10.1098/rstb.2018.0088	journal	March 2019
Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome Goltsman, Daniela S. Aliaga; Sun, Christine L.; Proctor, Diana M. https://doi.org/10.1101/266700	posted_content	August 2018
Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome Goltsman, Daniela S. Aliaga; Sun, Christine L.; Proctor, Diana M. Genome Research, Vol. 28, Issue 10 https://doi.org/10.1101/gr.236000.118	journal	September 2018
Anti‐CRISPR proteins targeting the CRISPR‐Cas system enrich the toolkit for genetic engineering Liu, Qiong; Zhang, Hongxia; Huang, Xiaotian The FEBS Journal, Vol. 287, Issue 4 https://doi.org/10.1111/febs.15139	journal	November 2019
Adapting Drug Approval Pathways for Bacteriophage-Based Therapeutics Cooper, Callum J.; Khan Mirzaei, Mohammadali; Nilsson, Anders S. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01209	journal	August 2016
CRISPR-Cas Systems Features and the Gene-Reservoir Role of Coagulase-Negative Staphylococci Rossi, Ciro C.; Souza-Silva, Thaysa; Araújo-Alves, Amanda V. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01545	journal	August 2017
Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales Daly, Rebecca A.; Borton, Mikayla A.; Wilkins, Michael J. Nature Microbiology, Vol. 1, Issue 10 https://doi.org/10.1038/nmicrobiol.2016.146	journal	September 2016
Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants Makarova, Kira S.; Wolf, Yuri I.; Iranzo, Jaime Nature Reviews Microbiology, Vol. 18, Issue 2 https://doi.org/10.1038/s41579-019-0299-x	journal	December 2019
Atypical organizations and epistatic interactions of CRISPRs and cas clusters in genomes and their mobile genetic elements Bernheim, Aude; Bikard, David; Touchon, Marie Nucleic Acids Research https://doi.org/10.1093/nar/gkz1091	journal	November 2019
The effect of bacterial mutation rate on the evolution of CRISPR-Cas adaptive immunity Chevallereau, Anne; Meaden, Sean; van Houte, Stineke Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772 https://doi.org/10.1098/rstb.2018.0094	journal	March 2019
The ecology and evolution of microbial CRISPR-Cas adaptive immune systems Westra, Edze R.; van Houte, Stineke; Gandon, Sylvain Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772 https://doi.org/10.1098/rstb.2019.0101	journal	March 2019
Co-occurrence of multiple CRISPRs and cas clusters suggests epistatic interactions Bernheim, Aude; Bikard, David; Touchon, Marie bioRxiv https://doi.org/10.1101/592600	posted_content	March 2019
Tissue- and population-level microbiome analysis of the wasp spider Argiope bruennichi identifies a novel dominant bacterial symbiont Sheffer, Monica M.; Uhl, Gabriele; Prost, Stefan bioRxiv https://doi.org/10.1101/822437	posted_content	November 2019
Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community Sieber, Christian M. K.; Paul, Blair G.; Castelle, Cindy J. mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mBio.02128-19	journal	November 2019
Phylogenomics of Cas4 family nucleases Hudaiberdiev, Sanjarbek; Shmakov, Sergey; Wolf, Yuri I. BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-017-1081-1	journal	November 2017
Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity Tian, Renmao; Ning, Daliang; He, Zhili Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00825-w	journal	April 2020
Genus-wide comparison of Pseudovibrio bacterial genomes reveal diverse adaptations to different marine invertebrate hosts Alex, Anoop; Antunes, Agostinho PLOS ONE, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pone.0194368	journal	May 2018
An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes Horn, Hannes; Slaby, Beate M.; Jahn, Martin T. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01751	journal	November 2016
Bacteriophages and Bacterial Plant Diseases Buttimer, Colin; McAuliffe, Olivia; Ross, R. P. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00034	journal	January 2017
Bacterial and Archaeal Viruses of Himalayan Hot Springs at Manikaran Modulate Host Genomes Sharma, Anukriti; Schmidt, Matthias; Kiesel, Bärbel Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03095	journal	December 2018
Reconstructing the functions of endosymbiotic Mollicutes in fungus-growing ants Sapountzis, Panagiotis; Zhukova, Mariya; Shik, Jonathan Z. eLife, Vol. 7 https://doi.org/10.7554/elife.39209	journal	November 2018
New CRISPR–Cas systems from uncultivated microbes Burstein, David; Harrington, Lucas B.; Strutt, Steven C. Nature, Vol. 542, Issue 7640 https://doi.org/10.1038/nature21059	journal	December 2016
The enigmatic archaeal virosphere Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick Nature Reviews Microbiology, Vol. 15, Issue 12 https://doi.org/10.1038/nrmicro.2017.125	journal	November 2017
Visualization and prediction of CRISPR incidence in microbial trait-space to identify drivers of antiviral immune strategy Weissman, Jake L.; Laljani, Rohan M. R.; Fagan, William F. The ISME Journal, Vol. 13, Issue 10 https://doi.org/10.1038/s41396-019-0411-2	journal	June 2019
Long-term genomic coevolution of host-parasite interaction in the natural environment Laanto, Elina; Hoikkala, Ville; Ravantti, Janne bioRxiv https://doi.org/10.1101/101576	posted_content	January 2017
Saccharibacteria (TM7) in the Human Oral Microbiome Bor, B.; Bedree, J. K.; Shi, W. Journal of Dental Research, Vol. 98, Issue 5 https://doi.org/10.1177/0022034519831671	journal	February 2019
Insights Obtained by Culturing Saccharibacteria With Their Bacterial Hosts Bor, B.; Collins, A. J.; Murugkar, P. P. Journal of Dental Research, Vol. 99, Issue 6 https://doi.org/10.1177/0022034520905792	journal	February 2020
A functional type II-A CRISPR-Cas system from Listeria enables efficient genome editing of large non-integrating bacteriophage Hupfeld, Mario; Trasanidou, Despoina; Ramazzini, Livia ETH Zurich https://doi.org/10.3929/ethz-b-000291147	text	January 2018
Optimizing de novo genome assembly from PCR-amplified metagenomes Roux, Simon; Trubl, Gareth; Goudeau, Danielle PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6902	journal	January 2019
Measurement of bacterial replication rates in microbial communities Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C. Nature Biotechnology, Vol. 34, Issue 12 https://doi.org/10.1038/nbt.3704	journal	November 2016
Systematic prediction of functionally linked genes in bacterial and archaeal genomes Shmakov, Sergey A.; Faure, Guilhem; Makarova, Kira S. Nature Protocols, Vol. 14, Issue 10 https://doi.org/10.1038/s41596-019-0211-1	journal	September 2019
Genome-wide correlation analysis suggests different roles of CRISPR-Cas systems in the acquisition of antibiotic resistance genes in diverse species Shehreen, Saadlee; Chyou, Te-yuan; Fineran, Peter C. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1772 https://doi.org/10.1098/rstb.2018.0384	journal	March 2019
Phages actively challenge niche communities in the Antarctic soils Bezuidt, Oliver K. I.; Lebre, Pedro Humberto; Pierneef, Rian bioRxiv https://doi.org/10.1101/2020.01.17.911081	posted_content	January 2020
Tissue- and Population-Level Microbiome Analysis of the Wasp Spider Argiope bruennichi Identified a Novel Dominant Bacterial Symbiont Sheffer, Monica M.; Uhl, Gabriele; Prost, Stefan Microorganisms, Vol. 8, Issue 1 https://doi.org/10.3390/microorganisms8010008	journal	December 2019
Exploring the ecological function of CRISPR-Cas virus defense Lundgren, Magnus Communicative & Integrative Biology, Vol. 9, Issue 5 https://doi.org/10.1080/19420889.2016.1216740	journal	August 2016
CRISPRdisco: An Automated Pipeline for the Discovery and Analysis of CRISPR-Cas Systems Crawley, Alexandra B.; Henriksen, James R.; Barrangou, Rodolphe The CRISPR Journal, Vol. 1, Issue 2 https://doi.org/10.1089/crispr.2017.0022	journal	April 2018
CRISPR-Cas Defense System and Potential Prophages in Cyanobacteria Associated with the Coral Black Band Disease Buerger, Patrick; Wood-Charlson, Elisha M.; Weynberg, Karen D. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.02077	journal	December 2016
Incomplete Selective Sweeps of Microcystis Population Detected by the Leader-End CRISPR Fragment Analysis in a Natural Pond Kimura, Shigeko; Uehara, Mika; Morimoto, Daichi Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00425	journal	March 2018
Prokaryotic Genome Expansion Is Facilitated by Phages and Plasmids but Impaired by CRISPR Gao, Na L.; Chen, Jingchao; Wang, Teng Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02254	journal	October 2019
Multiple Origins and Specific Evolution of CRISPR/Cas9 Systems in Minimal Bacteria (Mollicutes) Ipoutcha, Thomas; Tsarmpopoulos, Iason; Talenton, Vincent Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02701	journal	November 2019
Detection and variability analyses of CRISPR-like loci in the H. pylori genome Garcia-Zea, Jerson Alexander; de la Herran, Roberto; Rodriguez, Francisca Robles PeerJ Preprints https://doi.org/10.7287/peerj.preprints.27196v1	journal	September 2018

Similar Records

Bacterial CRISPR/Cas DNA endonucleases: A revolutionary technology that could dramatically impact viral research and treatment

Journal Article · Fri May 15 00:00:00 EDT 2015 · Virology · OSTI ID:1469126

Kennedy, Edward M.

Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling

Journal Article · Sun Mar 01 00:00:00 EST 2015 · Current Biology, 25(6):690-701 · OSTI ID:1469126

Castelle, Cindy; Wrighton, Kelly C.; Thomas, Brian C.; +10 more

Searching for fat tails in CRISPR-Cas systems: Data analysis and mathematical modeling

Journal Article · Fri Mar 26 00:00:00 EDT 2021 · PLoS Computational Biology (Online) · OSTI ID:1469126

Pavlova, Yekaterina S.; Paez-Espino, David; Morozov, Andrew Yu.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biological sciences
genetics
microbiology
virology

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

Citation Formats

References (61)

Cited By (47)

Similar Records

Related Subjects