Diversity and evolution of class 2 CRISPR–Cas systems

Class 2 CRISPR–Cas systems are characterized by effector modules that consist of a single multidomain protein, such as Cas9 or Cpf1. We designed a computational pipeline for the discovery of novel class 2 variants and used it to identify six new CRISPR–Cas subtypes. The diverse properties of these new systems provide potential for the development of versatile tools for genome editing and regulation. In this Analysis article, we present a comprehensive census of class 2 types and class 2 subtypes in complete and draft bacterial and archaeal genomes, outline evolutionary scenarios for the independent origin of different class 2 CRISPR–Cas systems from mobile genetic elements, and propose an amended classification and nomenclature of CRISPR–Cas.

[1]  James J. Collins,et al.  Comparative Analysis of Cas9 Activators Across Multiple Species , 2016, Nature Methods.

[2]  N. Baliga,et al.  Sense overlapping transcripts in IS1341-type transposase genes are functional non-coding RNAs in archaea , 2015, RNA biology.

[3]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[4]  Feng Zhang,et al.  Crystal Structure of Cas9 in Complex with Guide RNA and Target DNA , 2014, Cell.

[5]  Eugene V Koonin,et al.  Annotation and Classification of CRISPR-Cas Systems. , 2015, Methods in molecular biology.

[6]  Philippe Horvath,et al.  The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli , 2011, Nucleic acids research.

[7]  K. Heuner,et al.  First indication for a functional CRISPR/Cas system in Francisella tularensis. , 2013, International journal of medical microbiology : IJMM.

[8]  E. Koonin,et al.  Origins and evolution of viruses of eukaryotes: The ultimate modularity , 2015, Virology.

[9]  R. Barrangou,et al.  Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria , 2012, Proceedings of the National Academy of Sciences.

[10]  Hiroshi Nishimasu.  Crystal Structure of Cas9 , 2015 .

[11]  E. Koonin,et al.  ISC, a Novel Group of Bacterial and Archaeal DNA Transposons That Encode Cas9 Homologs , 2015, Journal of bacteriology.

[12]  K. Datsenko,et al.  CRISPR RNA binding and DNA target recognition by purified Cascade complexes from Escherichia coli , 2014, Nucleic acids research.

[13]  J. Vogel,et al.  CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III , 2011, Nature.

[14]  R. Tjian,et al.  Dynamics of CRISPR-Cas9 genome interrogation in living cells , 2015, Science.

[15]  Eric S. Lander,et al.  C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector , 2016, Science.

[16]  Kira S. Makarova,et al.  Classification and evolution of type II CRISPR-Cas systems , 2014, Nucleic acids research.

[17]  Jennifer A. Doudna,et al.  Programmable RNA Tracking in Live Cells with CRISPR/Cas9 , 2016, Cell.

[18]  Yanli Wang,et al.  Two Distant Catalytic Sites Are Responsible for C2c2 RNase Activities , 2017, Cell.

[19]  E. Lander,et al.  Development and Applications of CRISPR-Cas9 for Genome Engineering , 2014, Cell.

[20]  Albert J R Heck,et al.  Structural basis for CRISPR RNA-guided DNA recognition by Cascade , 2011, Nature Structural &Molecular Biology.

[21]  C. Fraser,et al.  The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity , 2009, Science.

[22]  Alan R. Davidson,et al.  Multiple mechanisms for CRISPR–Cas inhibition by anti-CRISPR proteins , 2015, Nature.

[23]  Thomas P. Curtis,et al.  Estimating prokaryotic diversity and its limits , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Martin J Aryee,et al.  Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells , 2016, Nature Biotechnology.

[25]  Jennifer A. Doudna,et al.  New CRISPR-Cas systems from uncultivated microbes , 2016, Nature.

[26]  D. Patel,et al.  PAM-Dependent Target DNA Recognition and Cleavage by C2c1 CRISPR-Cas Endonuclease , 2016, Cell.

[27]  Benjamin L. Oakes,et al.  Programmable RNA recognition and cleavage by CRISPR/Cas9 , 2014, Nature.

[28]  Luciano A. Marraffini,et al.  CRISPR-Cas immunity in prokaryotes , 2015, Nature.

[29]  Kira S. Makarova,et al.  Comparative genomics of defense systems in archaea and bacteria , 2013, Nucleic acids research.

[30]  P. Siguier,et al.  ISDra2 transposition in Deinococcus radiodurans is downregulated by TnpB , 2013, Molecular microbiology.

[31]  Emmanuelle Charpentier,et al.  The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems , 2013, RNA biology.

[32]  Kira S. Makarova,et al.  Crystal Structure of Cpf1 in Complex with Guide RNA and Target DNA , 2016, Cell.

[33]  J. Oost,et al.  Unravelling the structural and mechanistic basis of CRISPR–Cas systems , 2014, Nature Reviews Microbiology.

[34]  Kira S. Makarova,et al.  Nature and Intensity of Selection Pressure on CRISPR-Associated Genes , 2011, Journal of bacteriology.

[35]  Jin-Soo Kim,et al.  Targeted mutagenesis in mice by electroporation of Cpf1 ribonucleoproteins , 2016, Nature Biotechnology.

[36]  E. Koonin,et al.  Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing , 2013, Biology Direct.

[37]  Albert J R Heck,et al.  RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. , 2014, Molecular cell.

[38]  Isaac B. Hilton,et al.  Editing the epigenome: technologies for programmable transcription and epigenetic modulation , 2016, Nature Methods.

[39]  M. F. White,et al.  CARF and WYL domains: ligand-binding regulators of prokaryotic defense systems , 2014, Front. Genet..

[40]  Chase L. Beisel,et al.  Guide RNA functional modules direct Cas9 activity and orthogonality. , 2014, Molecular cell.

[41]  Eugene V Koonin,et al.  Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems , 2011, Biology Direct.

[42]  Eugene V Koonin,et al.  Discovery and Functional Characterization of Diverse Class 2 CRISPR-Cas Systems. , 2015, Molecular cell.

[43]  R. Terns,et al.  The CRISPR-associated Csx1 protein of Pyrococcus furiosus is an adenosine-specific endoribonuclease , 2016, RNA.

[44]  Christopher Quince,et al.  The rational exploration of microbial diversity , 2008, The ISME Journal.

[45]  G. Church,et al.  Cas9 as a versatile tool for engineering biology , 2013, Nature Methods.

[46]  Ibtissem Grissa,et al.  CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats , 2007, Nucleic Acids Res..

[47]  Homologues of bacterial TnpB_IS605 are widespread in diverse eukaryotic transposable elements , 2013, Mobile DNA.

[48]  M. Jinek,et al.  Structural basis for the endoribonuclease activity of the type III-A CRISPR-associated protein Csm6 , 2016, RNA.

[49]  Ningning Li,et al.  The crystal structure of Cpf1 in complex with CRISPR RNA , 2016, Nature.

[50]  Sergey A. Shmakov,et al.  Cas13b is a Type VI-B CRISPR-associated RNA-Guided RNase differentially regulated by accessory proteins Csx27 and Csx28 , 2016, bioRxiv.

[51]  Le Cong,et al.  Multiplex Genome Engineering Using CRISPR/Cas Systems , 2013, Science.

[52]  Jin-Soo Kim,et al.  Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells , 2016, Nature Biotechnology.

[53]  J. Doudna,et al.  A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity , 2012, Science.

[54]  Stan J. J. Brouns,et al.  Evolution and classification of the CRISPR–Cas systems , 2011, Nature Reviews Microbiology.

[55]  J. García-Martínez,et al.  Anti-cas spacers in orphan CRISPR4 arrays prevent uptake of active CRISPR–Cas I-F systems , 2016, Nature Microbiology.

[56]  Yanli Wang,et al.  C2c1-sgRNA Complex Structure Reveals RNA-Guided DNA Cleavage Mechanism. , 2017, Molecular cell.

[57]  N. Grishin,et al.  A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action , 2006, Biology Direct.

[58]  Yongsub Kim,et al.  Generation of knockout mice by Cpf1-mediated gene targeting , 2016, Nature Biotechnology.

[59]  Rodolphe Barrangou,et al.  CRISPR‐Cas systems and RNA‐guided interference , 2013, Wiley interdisciplinary reviews. RNA.

[60]  Peter C. Fineran,et al.  CRISPR–Cas systems: beyond adaptive immunity , 2014, Nature Reviews Microbiology.

[61]  Jennifer A. Doudna,et al.  Conformational control of DNA target cleavage by CRISPR–Cas9 , 2015, Nature.

[62]  Alan R Davidson,et al.  To acquire or resist: the complex biological effects of CRISPR-Cas systems. , 2014, Trends in microbiology.

[63]  W. Sloan,et al.  What is the extent of prokaryotic diversity? , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  Stan J. J. Brouns,et al.  Crystal structure of the CRISPR RNA–guided surveillance complex from Escherichia coli , 2014, Science.

[65]  Chikara Sato,et al.  Crystal structure of the CRISPR-Cas RNA silencing Cmr complex bound to a target analog. , 2015, Molecular cell.

[66]  Shirley Graham,et al.  Structure of the CRISPR Interference Complex CSM Reveals Key Similarities with Cascade , 2013, Molecular cell.

[67]  E. Koonin,et al.  Immunity, suicide or both? Ecological determinants for the combined evolution of anti-pathogen defense systems , 2015, BMC Evolutionary Biology.

[68]  Jennifer A. Doudna,et al.  Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection , 2016, Nature.

[69]  Sita J. Saunders,et al.  An updated evolutionary classification of CRISPR–Cas systems , 2015, Nature Reviews Microbiology.

[70]  Robert C. Edgar,et al.  PILER-CR: Fast and accurate identification of CRISPR repeats , 2007, BMC Bioinformatics.

[71]  Shiyuan Li,et al.  C-Brick: A New Standard for Assembly of Biological Parts Using Cpf1. , 2016, ACS synthetic biology.

[72]  E. Koonin,et al.  Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes , 2012, Biology Direct.

[73]  A. Regev,et al.  Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System , 2015, Cell.

[74]  Stan J. J. Brouns,et al.  Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes , 2008, Science.

[75]  Jennifer A. Doudna,et al.  Structures of the CRISPR-Cmr complex reveal mode of RNA target positioning , 2015, Science.

[76]  A. Buckling,et al.  The diversity-generating benefits of a prokaryotic adaptive immune system , 2016, Nature.

[77]  Ines Fonfara,et al.  The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA , 2016, Nature.

[78]  Kira S. Makarova,et al.  Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems , 2016, Science.

[79]  Eugene V Koonin,et al.  The basic building blocks and evolution of CRISPR-CAS systems. , 2013, Biochemical Society transactions.