Skip to main content
SpringerLink
Log in

CRISPR/Cas and CRISPR/Cmr Immune Systems of Archaea

  • Chapter
Regulatory RNAs in Prokaryotes

Abstract

The CRISPR/Cas (Clustered Regularly Interspaced Short Palindromic Repeats/ CRISPR-Associated Genes) and CRISPR/Cmr systems (Cmr: Cas module-RAMP (Repeat-Associated Mysterious Proteins)) provide the basis for adaptive and hereditable immune responses directed against the DNA and RNA, respectively, of invading elements. The former consists of CRISPR loci physically linked to a cassette of cas genes which together appear to constitute integral genetic modules. cmr genes, clustered in Cmr modules, are sometimes physically linked to CRISPR/Cas modules. The CRISPR/Cas immune system occurs in almost all archaea and about 40 % of bacteria. Cmr modules are less common, occurring in only about one third of genomes carrying CRISPR/Cas modules. An outline of how the CRISPR/Cas and CRISPR/Cmr systems function is indicated in Figure 1 where the former targets DNA and the latter RNA (mRNA and/or viral RNA) of the genetic elements.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761–764

    Article  PubMed  CAS  Google Scholar 

  • Arnold HP, She Q, Phan H, Stedman K, Prangishvili D, Holz I et al. (1999) The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol Microbiol 34: 217–226

    Article  PubMed  CAS  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709–1712

    Article  PubMed  CAS  Google Scholar 

  • Basta T, Smyth J, Forterre P, Prangishvili D, Peng X (2009) Novel archaeal plasmid pAH1 and its interactions with the lipothrixvirus AFV1. Mol Microbiol 71: 23–34

    Article  PubMed  CAS  Google Scholar 

  • Bettstetter M, Peng X, Garrett RA, Prangishvili D (2003) AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 315: 68–79

    Article  PubMed  CAS  Google Scholar 

  • Bize A, Karlsson EA, Ekefjard K, Quax TE, Pina M, Prevost MC et al. (2009) A unique virus release mechanism in the Archaea. Proc Natl Acad Sci U S A 106: 11306–11311

    Article  PubMed  CAS  Google Scholar 

  • Bize A, Peng X, Prokofeva M, Maclellan K, Lucas S, Forterre P et al. (2008) Viruses in acidic geothermal environments of the Kamchatka Peninsula. Res Microbiol 159: 358–366

    Article  PubMed  CAS  Google Scholar 

  • Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151: 2551–2561

    Article  PubMed  CAS  Google Scholar 

  • Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP et al. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321: 960–964

    Article  PubMed  CAS  Google Scholar 

  • Brügger K, Torarinsson E, Redder P, Chen L, Garrett RA (2004) Shuffling of Sulfolobus genomes by autonomous and non-autonomous mobile elements. Biochem Soc Trans 32: 179–183

    Article  PubMed  Google Scholar 

  • Carte J, Wang R, Li H, Terns RM, Terns MP (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22: 3489–3496

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Brugger K, Skovgaard M, Redder P, She Q, Torarinsson E et al. (2005) The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187: 4992–4999

    Article  PubMed  CAS  Google Scholar 

  • Cortez D, Forterre P, Gribaldo S (2009) A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol 10: R65

    Article  PubMed  Google Scholar 

  • Garrett RA, Prangishvili D, Shah SA, Reuter M, Stetter KO, Peng X (2010) Metagenomic analyses of novel viruses and plasmids from a cultured environmental sample of hyperthermophilic neutrophiles. Environ Microbiol 12: 2918–2930

    Article  PubMed  CAS  Google Scholar 

  • Garrett RA, Shah SA, Vestergaard G, Deng L, Gudbergsdottir S, Kenchappa CS et al. (2011) CRISPR-based immune systems of the Sulfolobales — complexity and diversity. Biochem Soc Trans 39: 51–57

    Article  PubMed  CAS  Google Scholar 

  • Godde JS and Bickerton A (2006) The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 62: 718–729

    Article  PubMed  CAS  Google Scholar 

  • Greve B, Jensen S, Brügger K, Zillig W, Garrett RA (2004) Genomic comparison of archaeal conjugative plasmids from Sulfolobus. Archaea 1: 231–239

    Article  PubMed  CAS  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2008) CRISPRcompar: a website to compare clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 36: W145–W148

    Article  PubMed  CAS  Google Scholar 

  • Gudbergsdottir S, Deng L, Chen Z, Jensen JVK, Jensen LR, She Q et al. (2011) Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vectorborne viral and plasmid genes and protospacers. Mol Microbiol 79: 35–49

    Article  PubMed  CAS  Google Scholar 

  • Guo L, Brügger K, Chao Liu C, Shah SA, Zheng H, Zhu Y et al. (2011) Genome analyses of Icelandic strains of Sulfolobus islandicus, model organisms for genetic and virus-host interaction studies. J Bacteriol in press

    Google Scholar 

  • Haft DH, Selengut J, Mongodin EF, Nelson KE (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1: e60

    Article  PubMed  Google Scholar 

  • Hale C, Kleppe K, Terns RM, Terns MP (2008) Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14: 2572–2579

    Article  PubMed  CAS  Google Scholar 

  • Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L et al. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139: 945–956

    Article  PubMed  CAS  Google Scholar 

  • Hannon GJ (2002) RNA interference. Nature 418: 244–251

    Article  PubMed  CAS  Google Scholar 

  • Held NL and Whitaker RJ (2009) Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ Microbiol 11: 457–466

    Article  PubMed  CAS  Google Scholar 

  • Horvath P and Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167–170

    Article  PubMed  CAS  Google Scholar 

  • Jansen R, Embden JD, Gaastra W, Schouls LM (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43: 1565–1575

    Article  PubMed  CAS  Google Scholar 

  • Jinek M and Doudna JA (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457: 405–412

    Article  PubMed  CAS  Google Scholar 

  • Karginov FV and Hannon GJ (2010) The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol Cell 37: 7–19

    Article  PubMed  CAS  Google Scholar 

  • Klattenhoff C and Theurkauf W (2008) Biogenesis and germline functions of piRNAs. Development 135: 3–9

    Article  PubMed  CAS  Google Scholar 

  • Krupovic M, Forterre P, Bamford DH (2010) Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J Mol Biol 397: 144–160

    Article  PubMed  CAS  Google Scholar 

  • Kunin V, Sorek R, Hugenholtz P (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 8: R61

    Article  PubMed  Google Scholar 

  • Lawrence CM, Menon S, Eilers BJ, Bothner B, Khayat R, Douglas T et al. (2009) Structural and functional studies of archaeal viruses. J Biol Chem 284: 12599–12603

    Article  PubMed  CAS  Google Scholar 

  • Lillestøl RK, Redder P, Garrett RA, Brugger K (2006) A putative viral defence mechanism in archaeal cells. Archaea 2: 59–72

    Article  PubMed  Google Scholar 

  • Lillestøl RK, Shah SA, Brugger K, Redder P, Phan H, Christiansen J et al. (2009) CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties. Mol Microbiol 72: 259–272

    Article  PubMed  Google Scholar 

  • Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) 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. Biol Direct 1: 7

    Article  PubMed  Google Scholar 

  • Marraffini LA and Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843–1845

    Article  PubMed  CAS  Google Scholar 

  • Marraffini LA and Sontheimer EJ (2010) Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463: 568–571

    Article  PubMed  CAS  Google Scholar 

  • Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Almendros C (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155: 733–740

    Article  PubMed  CAS  Google Scholar 

  • Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60: 174–182

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Blum H, She Q, Mallok S, Brügger K, Garrett RA et al. (2001) Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291: 226–234

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Brügger K, Shen B, Chen L, She Q, Garrett RA (2003) Genus-specific protein binding to the large clusters of DNA repeats (short regularly spaced repeats) present in Sulfolobus genomes. J Bacteriol 185: 2410–2417

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Kessler A, Phan H, Garrett RA, Prangishvili D (2004) Multiple variants of the archaeal DNA rudivirus SIRV1 in a single host and a novel mechanism of genomic variation. Mol Microbiol 54: 366–375

    Article  PubMed  CAS  Google Scholar 

  • Porter K, Russ BE, Dyall-Smith ML (2007) Virus-host interactions in salt lakes. Curr Opin Microbiol 10: 418–424

    Article  PubMed  CAS  Google Scholar 

  • Portillo MC and Gonzalez JM (2009) CRISPR elements in the Thermococcales: evidence for associated horizontal gene transfer in Pyrococcus furiosus. J Appl Genet 50: 421–430

    Article  PubMed  CAS  Google Scholar 

  • Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151: 653–663

    Article  PubMed  CAS  Google Scholar 

  • Prangishvili D, Forterre P, Garrett RA (2006a) Viruses of the Archaea: a unifying view. Nat Rev Microbiol 4: 837–848

    Article  PubMed  CAS  Google Scholar 

  • Prangishvili D, Garrett RA, Koonin EV (2006b) Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 117: 52–67

    Article  PubMed  CAS  Google Scholar 

  • Rachel R, Bettstetter M, Hedlund BP, Haring M, Kessler A, Stetter KO et al. (2002) Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch Virol 147: 2419–2429

    Article  PubMed  CAS  Google Scholar 

  • Redder P and Garrett RA (2006) Mutations and rearrangements in the genome of Sulfolobus solfataricus P2. J Bacteriol 188: 4198–4206

    Article  PubMed  CAS  Google Scholar 

  • Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ (2009) Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci U S A 106: 8605–8610

    Article  PubMed  CAS  Google Scholar 

  • Santangelo TJ, Cubonova L, Skinner KM, Reeve JN (2009) Archaeal intrinsic transcription termination in vivo. J Bacteriol 191: 7102–7108

    Article  PubMed  CAS  Google Scholar 

  • Shah SA and Garrett RA (2011) CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res Microbiol 162: 27–38

    Article  PubMed  CAS  Google Scholar 

  • Shah SA, Hansen NR, Garrett RA (2009) Distribution of CRISPR spacer matches in viruses and plasmids of crenarchaeal acidothermophiles and implications for their inhibitory mechanism. Biochem Soc Trans 37: 23–28

    Article  PubMed  CAS  Google Scholar 

  • She Q, Peng X, Zillig W, Garrett RA (2001) Gene capture in archaeal chromosomes. Nature 409: 478

    Article  PubMed  CAS  Google Scholar 

  • She Q, Phan H, Garrett RA, Albers SV, Stedman KM, Zillig W (1998) Genetic profile of pNOB8 from Sulfolobus: the first conjugative plasmid from an archaeon. Extremophiles 2: 417–425

    Article  PubMed  CAS  Google Scholar 

  • Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, Drungowski M et al. (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci U S A 99: 7536–7541

    Article  PubMed  CAS  Google Scholar 

  • Tang TH, Polacek N, Zywicki M, Huber H, Brügger K, Garrett R et al. (2005) Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol Microbiol 55: 469–481

    Article  PubMed  CAS  Google Scholar 

  • Torarinsson E, Klenk HP, Garrett RA (2005) Divergent transcriptional and translational signals in Archaea. Environ Microbiol 7: 47–54

    Article  PubMed  CAS  Google Scholar 

  • Tyson GW and Banfield JF (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200–207

    PubMed  CAS  Google Scholar 

  • Veith A, Klingl A, Zolghadr B, Lauber K, Mentele R, Lottspeich F et al. (2009) Acidianus, Sulfolobus and Metallosphaera surface layers: structure, composition and gene expression. Mol Microbiol 73: 58–72

    Article  PubMed  CAS  Google Scholar 

  • Vestergaard G, Shah SA, Bize A, Reitberger W, Reuter M, Phan H et al. (2008) Stygiolobus rodshaped virus and the interplay of crenarchaeal rudiviruses with the CRISPR antiviral system. J Bacteriol 190: 6837–6845

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Duan Z, Zhu H, Guo X, Wang Z, Zhou J et al. (2007) A novel Sulfolobus non-conjugative extrachromosomal genetic element capable of integration into the host genome and spreading in the presence of a fusellovirus. Virology 363: 124–133

    Article  PubMed  CAS  Google Scholar 

  • Zillig W, Arnold HP, Holz I, Prangishvili D, Schweier A, Stedman K et al. (1998) Genetic elements in the extremely thermophilic archaeon Sulfolobus. Extremophiles 2: 131–140

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Archaea Centre, Department of Biology, Copenhagen University, Copenhagen, Denmark

    Roger A. Garrett

Authors
  1. Shiraz A. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gisle Vestergaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roger A. Garrett
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag/Wien

About this chapter

Cite this chapter

Shah, S.A., Vestergaard, G., Garrett, R.A. (2012). CRISPR/Cas and CRISPR/Cmr Immune Systems of Archaea. In: Regulatory RNAs in Prokaryotes. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0218-3_9

Download citation

Publish with us

Policies and ethics

Search

Navigation