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Title: New CRISPR–Cas systems from uncultivated microbes

Abstract

We present that CRISPR-Cas systems provide microbes with adaptive immunity by employing short DNA sequences, termed spacers, that guide Cas proteins to cleave foreign DNA. Class 2 CRISPR-Cas systems are streamlined versions, in which a single RNA-bound Cas protein recognizes and cleaves target sequences. The programmable nature of these minimal systems has enabled researchers to repurpose them into a versatile technology that is broadly revolutionizing biological and clinical research. However, current CRISPR-Cas technologies are based solely on systems from isolated bacteria, leaving the vast majority of enzymes from organisms that have not been cultured untapped. Metagenomics, the sequencing of DNA extracted directly from natural microbial communities, provides access to the genetic material of a huge array of uncultivated organisms. Here, using genome-resolved metagenomics, we identify a number of CRISPR-Cas systems, including the first reported Cas9 in the archaeal domain of life, to our knowledge. This divergent Cas9 protein was found in little-studied nanoarchaea as part of an active CRISPR-Cas system. In bacteria, we discovered two previously unknown systems, CRISPR-CasX and CRISPR-CasY, which are among the most compact systems yet discovered. Notably, all required functional components were identified by metagenomics, enabling validation of robust in vivo RNA-guided DNA interference activity inmore » Escherichia coli. Lastly, interrogation of environmental microbial communities combined with in vivo experiments allows us to access an unprecedented diversity of genomes, the content of which will expand the repertoire of microbe-based biotechnologies.« less

Authors:
 [1];  [2];  [2];  [1];  [1];  [1];  [3];  [4]
+ Show Author Affiliations
  1. Univ. of California, Berkeley, CA (United States). Department of Earth and Planetary Sciences
  2. Univ. of California, Berkeley, CA (United States). Department of Molecular and Cell Biology
  3. Univ. of California, Berkeley, CA (United States). Department of Molecular and Cell Biology, Howard Hughes Medical Institute, Innovative Genomics Initiative, and MBIB Division
  4. Univ. of California, Berkeley, CA (United States). Department of Earth and Planetary Sciences and Department of Environmental Science, Policy, and Management
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1379729
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 542; Journal Issue: 7640; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Protein function predictions; RNA; Microbiology; Microbial ecology; Biotechnology

Citation Formats

Burstein, David, Harrington, Lucas B., Strutt, Steven C., Probst, Alexander J., Anantharaman, Karthik, Thomas, Brian C., Doudna, Jennifer A., and Banfield, Jillian F. New CRISPR–Cas systems from uncultivated microbes. United States: N. p., 2016. Web. doi:10.1038/nature21059.
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Burstein, David, Harrington, Lucas B., Strutt, Steven C., Probst, Alexander J., Anantharaman, Karthik, Thomas, Brian C., Doudna, Jennifer A., & Banfield, Jillian F. New CRISPR–Cas systems from uncultivated microbes. United States. https://doi.org/10.1038/nature21059
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Burstein, David, Harrington, Lucas B., Strutt, Steven C., Probst, Alexander J., Anantharaman, Karthik, Thomas, Brian C., Doudna, Jennifer A., and Banfield, Jillian F. Thu . "New CRISPR–Cas systems from uncultivated microbes". United States. https://doi.org/10.1038/nature21059. https://www.osti.gov/servlets/purl/1379729.
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@article{osti_1379729,
title = {New CRISPR–Cas systems from uncultivated microbes},
author = {Burstein, David and Harrington, Lucas B. and Strutt, Steven C. and Probst, Alexander J. and Anantharaman, Karthik and Thomas, Brian C. and Doudna, Jennifer A. and Banfield, Jillian F.},
abstractNote = {We present that CRISPR-Cas systems provide microbes with adaptive immunity by employing short DNA sequences, termed spacers, that guide Cas proteins to cleave foreign DNA. Class 2 CRISPR-Cas systems are streamlined versions, in which a single RNA-bound Cas protein recognizes and cleaves target sequences. The programmable nature of these minimal systems has enabled researchers to repurpose them into a versatile technology that is broadly revolutionizing biological and clinical research. However, current CRISPR-Cas technologies are based solely on systems from isolated bacteria, leaving the vast majority of enzymes from organisms that have not been cultured untapped. Metagenomics, the sequencing of DNA extracted directly from natural microbial communities, provides access to the genetic material of a huge array of uncultivated organisms. Here, using genome-resolved metagenomics, we identify a number of CRISPR-Cas systems, including the first reported Cas9 in the archaeal domain of life, to our knowledge. This divergent Cas9 protein was found in little-studied nanoarchaea as part of an active CRISPR-Cas system. In bacteria, we discovered two previously unknown systems, CRISPR-CasX and CRISPR-CasY, which are among the most compact systems yet discovered. Notably, all required functional components were identified by metagenomics, enabling validation of robust in vivo RNA-guided DNA interference activity in Escherichia coli. Lastly, interrogation of environmental microbial communities combined with in vivo experiments allows us to access an unprecedented diversity of genomes, the content of which will expand the repertoire of microbe-based biotechnologies.},
doi = {10.1038/nature21059},
journal = {Nature (London)},
number = 7640,
volume = 542,
place = {United States},
year = {2016},
month = {12}
}
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    Schizosaccharomyces pombe Can Reduce Acetic Acid Produced by Baijiu Spontaneous Fermentation Microbiota
    journal, November 2019

    Casposase structure and the mechanistic link between DNA transposition and spacer acquisition by CRISPR-Cas
    journal, January 2020

    Characterization of Cas proteins for CRISPR‐Cas editing in streptomycetes
    journal, May 2019

    • Yeo, Wan Lin; Heng, Elena; Tan, Lee Ling
    • Biotechnology and Bioengineering, Vol. 116, Issue 9
    • DOI: 10.1002/bit.27021

    CRISPR/Cas9: Nature's gift to prokaryotes and an auspicious tool in genome editing
    journal, November 2019

    • Khanzadi, Manzoor N.; Khan, Abid A.
    • Journal of Basic Microbiology, Vol. 60, Issue 2
    • DOI: 10.1002/jobm.201900420

    Developmental progress of CRISPR/Cas9 and its therapeutic applications for HIV-1 infection
    journal, July 2018

    • Deng, Qiudi; Chen, Zisheng; Shi, Lei
    • Reviews in Medical Virology, Vol. 28, Issue 5
    • DOI: 10.1002/rmv.1998

    A load driver device for engineering modularity in biological networks
    journal, November 2014

    • Mishra, Deepak; Rivera, Phillip M.; Lin, Allen
    • Nature Biotechnology, Vol. 32, Issue 12
    • DOI: 10.1038/nbt.3044

    Diversity and evolution of class 2 CRISPR–Cas systems
    journal, January 2017

    • Shmakov, Sergey; Smargon, Aaron; Scott, David
    • Nature Reviews Microbiology, Vol. 15, Issue 3
    • DOI: 10.1038/nrmicro.2016.184

    The emerging and uncultivated potential of CRISPR technology in plant science
    journal, July 2019

    Immune-orthogonal orthologues of AAV capsids and of Cas9 circumvent the immune response to the administration of gene therapy
    journal, July 2019

    • Moreno, Ana M.; Palmer, Nathan; Alemán, Fernando
    • Nature Biomedical Engineering, Vol. 3, Issue 10
    • DOI: 10.1038/s41551-019-0431-2

    The next generation of CRISPR–Cas technologies and applications
    journal, May 2019

    • Pickar-Oliver, Adrian; Gersbach, Charles A.
    • Nature Reviews Molecular Cell Biology, Vol. 20, Issue 8
    • DOI: 10.1038/s41580-019-0131-5

    Clades of huge phages from across Earth’s ecosystems
    journal, February 2020

    Broad-spectrum enzymatic inhibition of CRISPR-Cas12a
    journal, April 2019

    • Knott, Gavin J.; Thornton, Brittney W.; Lobba, Marco J.
    • Nature Structural & Molecular Biology, Vol. 26, Issue 4
    • DOI: 10.1038/s41594-019-0208-z

    Comparative genomics and evolution of trans-activating RNAs in Class 2 CRISPR-Cas systems
    journal, June 2018

    PAM identification by CRISPR-Cas effector complexes: diversified mechanisms and structures
    journal, September 2018

    A new statistic for efficient detection of repetitive sequences
    journal, April 2019

    Multiplex genome editing of microorganisms using CRISPR-Cas
    journal, April 2019

    • Adiego-Pérez, Belén; Randazzo, Paola; Daran, Jean Marc
    • FEMS Microbiology Letters, Vol. 366, Issue 8
    • DOI: 10.1093/femsle/fnz086

    Microbial Dark Matter Investigations: How Microbial Studies Transform Biological Knowledge and Empirically Sketch a Logic of Scientific Discovery
    journal, February 2018

    • Bernard, Guillaume; Pathmanathan, Jananan S.; Lannes, Romain
    • Genome Biology and Evolution, Vol. 10, Issue 3
    • DOI: 10.1093/gbe/evy031

    Structural insights into the modulatory role of the accessory protein WYL1 in the Type VI-D CRISPR-Cas system
    journal, April 2019

    • Zhang, Heng; Dong, Cheng; Li, Li
    • Nucleic Acids Research, Vol. 47, Issue 10
    • DOI: 10.1093/nar/gkz269

    Cellular Reprogramming, Genome Editing, and Alternative CRISPR Cas9 Technologies for Precise Gene Therapy of Duchenne Muscular Dystrophy
    journal, January 2017

    • Gee, Peter; Xu, Huaigeng; Hotta, Akitsu
    • Stem Cells International, Vol. 2017
    • DOI: 10.1155/2017/8765154

    On the global CRISPR array behavior in class I systems
    journal, August 2017

    Building a genome engineering toolbox in nonmodel prokaryotic microbes
    journal, May 2018

    • Freed, Emily; Fenster, Jacob; Smolinski, Sharon L.
    • Biotechnology and Bioengineering, Vol. 115, Issue 9
    • DOI: 10.1002/bit.26727

    Expanding targeting scope, editing window, and base transition capability of base editing in Corynebacterium glutamicum
    journal, July 2019

    • Wang, Yu; Liu, Ye; Li, Junwei
    • Biotechnology and Bioengineering, Vol. 116, Issue 11
    • DOI: 10.1002/bit.27121

    A highly specific SpCas9 variant is identified by in vivo screening in yeast
    journal, January 2018

    • Casini, Antonio; Olivieri, Michele; Petris, Gianluca
    • Nature Biotechnology, Vol. 36, Issue 3
    • DOI: 10.1038/nbt.4066

    A decade of discovery: CRISPR functions and applications
    journal, June 2017

    Nucleic acid cleavage with a hyperthermophilic Cas9 from an uncultured Ignavibacterium
    journal, October 2019

    • Schmidt, Stephanie Tzouanas; Yu, Feiqiao Brian; Blainey, Paul C.
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 46
    • DOI: 10.1073/pnas.1904273116

    Functionally diverse type V CRISPR-Cas systems
    journal, December 2018

    • Yan, Winston X.; Hunnewell, Pratyusha; Alfonse, Lauren E.
    • Science, Vol. 363, Issue 6422
    • DOI: 10.1126/science.aav7271

    Cas9 versus Cas12a/Cpf1: Structure-function comparisons and implications for genome editing
    text, January 2018

    Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms
    text, January 2017

    Gene editing in dermatology: Harnessing CRISPR for the treatment of cutaneous disease
    journal, January 2020

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