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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:
Journal Article: 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. 2016. "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},
url = {https://www.osti.gov/biblio/1469126}, journal = {Nature Communications},
issn = {2041-1723},
number = ,
volume = 7,
place = {United States},
year = {Wed Feb 03 00:00:00 EST 2016},
month = {Wed Feb 03 00:00:00 EST 2016}
}

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Cited by: 131 works
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Works referenced in this record:

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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


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


The Pfam protein families database
journal, November 2011


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


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


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


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


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


PHAST: A Fast Phage Search Tool
journal, June 2011


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


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


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


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


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


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


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


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


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013


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


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


The Pfam protein families database
journal, November 2011


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


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


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


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


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


Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere
journal, November 2011


Restriction and Modification Systems
journal, December 1991


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


Accelerated Profile HMM Searches
journal, October 2011


Works referencing / citing this record:

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


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


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


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


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


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


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


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


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


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


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


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


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


Phylogenomics of Cas4 family nucleases
journal, November 2017


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


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


The enigmatic archaeal virosphere
journal, November 2017


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


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


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


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


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


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


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


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


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


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


Phylogenomics of Cas4 family nucleases
journal, November 2017


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


Bacteriophages and Bacterial Plant Diseases
journal, January 2017


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


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


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