1932

Abstract

Effective clearance of an infection requires that the immune system rapidly detects and neutralizes invading parasites while strictly avoiding self-antigens that would result in autoimmunity. The cellular machinery and complex signaling pathways that coordinate an effective immune response have generally been considered properties of the eukaryotic immune system. However, a surprisingly sophisticated adaptive immune system that relies on small RNAs for sequence-specific targeting of foreign nucleic acids was recently discovered in bacteria and archaea. Molecular vaccination in prokaryotes is achieved by integrating short fragments of foreign nucleic acids into a repetitive locus in the host chromosome known as a CRISPR (clustered regularly interspaced short palindromic repeat). Here we review the mechanisms of CRISPR-mediated immunity and discuss the ecological and evolutionary implications of these adaptive defense systems.

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2013-06-02
2024-10-12
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Literature Cited

  1. Hankin EH. 1.  1896. L'action bactericide des eaux de la Jumna et du Gange sur le vibrion du cholera. Ann. Inst. Pasteur 10:511–23 [Google Scholar]
  2. Bergh O, Borsheim KY, Bratbak G, Heldal M. 2.  1989. High abundance of viruses found in aquatic environments. Nature 340:467–68 [Google Scholar]
  3. Suttle CA. 3.  2005. Viruses in the sea. Nature 437:356–61 [Google Scholar]
  4. Weinbauer MG. 4.  2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127–81 [Google Scholar]
  5. Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasić L, Thingstad TF. 5.  et al. 2009. Explaining microbial population genomics through phage predation. Nat. Rev. Microbiol. 7:828–36 [Google Scholar]
  6. Bikard D, Marraffini LA. 6.  2011. Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr. Opin. Immunol. 24:15–20 [Google Scholar]
  7. Deveau H, Garneau JE, Moineau S. 7.  2010. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 64:475–93 [Google Scholar]
  8. Stern A, Sorek R. 8.  2010. The phage-host arms race: shaping the evolution of microbes. BioEssays 33:43–51 [Google Scholar]
  9. Westra ER, Swarts D, Staals R, Jore MM, Brouns SJJ, van der Oost J. 9.  2012. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311–38 [Google Scholar]
  10. Horvath P, Barrangou R. 10.  2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–70 [Google Scholar]
  11. Marraffini LA, Sontheimer EJ. 11.  2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181–90 [Google Scholar]
  12. Pougach KS, Lopatina AV, Severinov KV. 12.  2012. CRISPR adaptive immunity systems of prokaryotes. Mol. Biol. 46:175–82 [Google Scholar]
  13. Wiedenheft B, Sternberg SH, Doudna JA. 13.  2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–38 [Google Scholar]
  14. Kunin V, Sorek R, Hugenholtz P. 14.  2007. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol. 8:R61 [Google Scholar]
  15. Godde JS, Bickerton A. 15.  2006. The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J. Mol. Evol. 62:718–29 [Google Scholar]
  16. Mojica FJ, Díez-Villaseñor C, Soria E, Juez G. 16.  2000. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol. Microbiol. 36:244–46 [Google Scholar]
  17. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. 17.  1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169:5429–33 [Google Scholar]
  18. Grissa I, Vergnaud G, Pourcel C. 18.  2007. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35:W52–57 [Google Scholar]
  19. Rousseau C, Gonnet M, Le Romancer M, Nicolas J. 19.  2009. CRISPI: a CRISPR interactive database. Bioinformatics 25:3317–18 [Google Scholar]
  20. Palmer KL, Gilmore MS. 20.  2010. Multidrug-resistant enterococci lack CRISPR-cas.. mBio 1:e00227 [Google Scholar]
  21. Jansen R, Embden JD, Gaastra W, Schouls LM. 21.  2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565–75 [Google Scholar]
  22. Pourcel C, Salvignol G, Vergnaud G. 22.  2005. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:653–63 [Google Scholar]
  23. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M. 23.  et al. 2012. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol. Cell 45:292–302 [Google Scholar]
  24. Lillestøl RK, Shah SA, Brügger K, Redder P, Phan H. 24.  et al. 2009. CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties. Mol. Microbiol. 72:259–72 [Google Scholar]
  25. Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M. 25.  et al. 2010. Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol. Microbiol. 77:1367–79 [Google Scholar]
  26. Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, Wagner R. 26.  2010. Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol. Microbiol. 75:1495–512 [Google Scholar]
  27. Yosef I, Goren MG, Qimron U. 27.  2012. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40:5569–76 [Google Scholar]
  28. Haft DH, Selengut J, Mongodin EF, Nelson KE. 28.  2005. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 1:e60 [Google Scholar]
  29. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 29.  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 [Google Scholar]
  30. Makarova KS, Wolf YI, van der Oost J, Koonin EV. 30.  2009. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4:29 [Google Scholar]
  31. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E. 31.  et al. 2011. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9:467–77 [Google Scholar]
  32. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ. 32.  et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–64 [Google Scholar]
  33. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER. 33.  et al. 2011. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18:529–36 [Google Scholar]
  34. Gesner EM, Schellenberg MJ, Garside EL, George MM, MacMillan AM. 34.  2011. Recognition and maturation of effector RNAs in a CRISPR interference pathway. Nat. Struct. Mol. Biol. 18:688–92 [Google Scholar]
  35. Sashital DG, Jinek M, Doudna JA. 35.  2011. An RNA induced conformational change required for CRISPR RNA cleavage by the endonuclease Cse3. Nat. Struct. Mol. Biol. 18:680–87 [Google Scholar]
  36. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJJ. 36.  et al. 2011. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477:486–89 [Google Scholar]
  37. Lintner NG, Kerou M, Brumfield SK, Graham S, Liu H. 37.  et al. 2011. Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). J. Biol. Chem. 286:21643–56 [Google Scholar]
  38. Chen Z, Yang H, Pavletich NP. 38.  2008. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453:489–84 [Google Scholar]
  39. Nam KH, Haitjema C, Liu X, Ding F, Wang H. 39.  et al. 2012. Cas5d protein processes pre-crRNA and assembles into a Cascade-like interference complex in Subtype I-C/Dvulg CRISPR-Cas system. Structure 20:1574–84 [Google Scholar]
  40. Wiedenheft B, van Duijn E, Bultema J, Waghmare S, Zhou K. 40.  et al. 2011. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. USA 108:10092–97 [Google Scholar]
  41. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y. 41.  et al. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–7 [Google Scholar]
  42. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R. 42.  et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71 [Google Scholar]
  43. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 43.  2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–21 [Google Scholar]
  44. Marraffini LA, Sontheimer EJ. 44.  2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–45 [Google Scholar]
  45. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR. 45.  et al. 2009. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:945–56 [Google Scholar]
  46. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K. 46.  et al. 2012. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell 45:303–13 [Google Scholar]
  47. Zhang J, Kasciukovic T, White MF. 47.  2012. The CRISPR associated protein Cas4 is a 5′ to 3′ DNA exonuclease with an iron-sulfur cluster. PLoS ONE 7:e47232 [Google Scholar]
  48. Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, Shinkai A. 48.  2010. Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol. 395:270–81 [Google Scholar]
  49. Young JC, Dill BD, Pan C, Hettich RL, Banfield JF. 49.  et al. 2012. Phage-induced expression of CRISPR-associated proteins is revealed by shotgun proteomics in Streptococcus thermophilus. PLoS ONE 7:e38077 [Google Scholar]
  50. Shinkai A, Kira S, Nakagawa N, Kashihara A, Kuramitsu S, Yokoyama S. 50.  2007. Transcription activation mediated by a cyclic AMP receptor protein from Thermus thermophilus HB8. J. Bacteriol. 189:3891–901 [Google Scholar]
  51. Cocozaki AI, Ramia NF, Shao Y, Hale CR, Terns RM. 51.  et al. 2012. Structure of the Cmr2 subunit of the CRISPR-Cas RNA silencing complex. Structure 20:545–53 [Google Scholar]
  52. Zhu X, Ye K. 52.  2012. Crystal structure of Cmr2 suggests a nucleotide cyclase-related enzyme in type III CRISPR-Cas systems. FEBS Lett. 586:939–45 [Google Scholar]
  53. Lintner NG, Frankel KA, Tsutakawa SE, Alsbury DL, Copie V. 53.  et al. 2011. The structure of the CRISPR-associated protein Csa3 provides insight into the regulation of the CRISPR/Cas system. J. Mol. Biol. 405:939–55 [Google Scholar]
  54. Medina-Aparicio L, Rebollar-Flores JE, Gallego-Hernández AL, Vázquez A, Olvera L. 54.  et al. 2011. The CRISPR/Cas immune system is an operon regulated by LeuO, H-NS, and leucine-responsive regulatory protein in Salmonella enterica serovar Typhi. J. Bacteriol. 193:2396–407 [Google Scholar]
  55. Westra ER, Pul U, Heidrich N, Jore MM, Lundgren M. 55.  et al. 2010. H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol. Microbiol. 77:1380–93 [Google Scholar]
  56. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H. 56.  et al. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236–38 [Google Scholar]
  57. Navarre WW, McClelland M, Libby SJ, Fang FC. 57.  2007. Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev. 21:1456–71 [Google Scholar]
  58. Bouffartigues E, Buckle M, Badaut C, Travers A, Rimsky S. 58.  2007. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol. 14:441–48 [Google Scholar]
  59. Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M. 59.  et al. 2007. High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res. 35:6330–37 [Google Scholar]
  60. Liu YJ, Chen H, Kenney LJ, Yan J. 60.  2010. A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev. 24:339–44 [Google Scholar]
  61. Hernández-Lucas I, Gallego-Hernández AL, Encarnación S, Fernández-Mora M, Martínez-Batallar AG. 61.  et al. 2008. The LysR-type transcriptional regulator LeuO controls expression of several genes in Salmonella enterica serovar Typhi. J. Bacteriol. 190:1658–70 [Google Scholar]
  62. Fang M, Majumder A, Tsai KJ, Wu HY. 62.  2000. ppGpp-dependent leuO expression in bacteria under stress. Biochem. Biophys. Res. Commun. 276:64–70 [Google Scholar]
  63. Majumder A, Fang M, Tsai KJ, Ueguchi C, Mizuno T, Wu HY. 63.  2001. LeuO expression in response to starvation for branched-chain amino acids. J. Biol. Chem. 276:19046–51 [Google Scholar]
  64. Potrykus K, Cashel M. 64.  2008. (p)ppGpp: still magical?. Annu. Rev. Microbiol. 62:35–51 [Google Scholar]
  65. Tosa T, Pizer LI. 65.  1971. Biochemical bases for the antimetabolite action of L-serine hydroxamate. J. Bacteriol. 106:972–82 [Google Scholar]
  66. Williams E, Lowe TM, Savas J, DiRuggiero J. 66.  2007. Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation. Extremophiles 11:19–29 [Google Scholar]
  67. Strand KR, Sun C, Li T, Jenney FE Jr, Schut GJ, Adams MW. 67.  2010. Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species. Arch. Microbiol. 192:447–59 [Google Scholar]
  68. Plagens A, Tjaden B, Hagemann A, Randau L, Hensel R. 68.  2012. Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J. Bacteriol. 194:2491–500 [Google Scholar]
  69. Götz D, Paytubi S, Munro S, Lundgren M, Bernander R, White MF. 69.  2007. Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol. 8:R220 [Google Scholar]
  70. Perez-Rodriguez R, Haitjema C, Huang Q, Nam KH, Bernardis S. 70.  et al. 2011. Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol. Microbiol. 79:584–99 [Google Scholar]
  71. Juranek S, Eban T, Altuvia Y, Brown M, Morozov P. 71.  et al. 2012. A genome-wide view of the expression and processing patterns of Thermus thermophilus HB8 CRISPR RNAs. RNA 18:783–94 [Google Scholar]
  72. Tang TH, Polacek N, Zywicki M, Huber H, Brugger K. 72.  et al. 2005. Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol. Microbiol. 55:469–81 [Google Scholar]
  73. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H. 73.  et al. 2002. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc. Natl. Acad. Sci. USA 99:7536–41 [Google Scholar]
  74. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R. 74.  2010. A single-base resolution map of an archaeal transcriptome. Genome Res. 20:133–41 [Google Scholar]
  75. Bolotin A, Ouinquis B, Sorokin A, Ehrlich SD. 75.  2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–61 [Google Scholar]
  76. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E. 76.  2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174–82 [Google Scholar]
  77. Barrangou R, Horvath P. 77.  2012. CRISPR: new horizons in phage resistance and strain identification. Annu. Rev. Food Sci. Technol. 3:143–62 [Google Scholar]
  78. Brussow H. 78.  2001. Phages of dairy bacteria. Annu. Rev. Microbiol. 55:283–303 [Google Scholar]
  79. Moineau S, Lévesque C. 79.  2005. Control of bacteriophages in industrial fermentations. Bacteriophages: Biology and Applications E Kutter, A Sulakvelidze 282–93 Boca Raton, FL: CRC [Google Scholar]
  80. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P. 80.  et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–12 [Google Scholar]
  81. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C. 81.  et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:1390–400 [Google Scholar]
  82. Horvath P, Romero DA, Couté-Monvoisin AC, Richards M, Deveau H. 82.  et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:1401–12 [Google Scholar]
  83. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Almendros C. 83.  2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733–40 [Google Scholar]
  84. Almendros C, Guzmán NM, Díez-Villaseñor C, García-Martínez J, Mojica FJ. 84.  2012. Target motifs affecting natural immunity by a constitutive CRISPR-Cas system in Escherichia coli. PLoS ONE 7:e50797 [Google Scholar]
  85. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA. 85.  2012. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. 194:5728–38 [Google Scholar]
  86. van der Ploeg JR. 86.  2009. Analysis of CRISPR in Streptococcus mutans suggests frequent occurrence of acquired immunity against infection by M102-like bacteriophages. Microbiology 155:1966–76 [Google Scholar]
  87. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 87.  2011. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 39:9275–82 [Google Scholar]
  88. Ellinger P, Arslan Z, Wurm R, Tschapek B, Mackenzie C. 88.  et al. 2012. The crystal structure of the CRISPR-associated protein Csn2 from Streptococcus agalactiae. J. Struct. Biol. 178:350–62 [Google Scholar]
  89. Koo Y, Jung DK, Bae E. 89.  2012. Crystal structure of Streptococcus pyogenes Csn2 reveals calcium-dependent conformational changes in its tertiary and quaternary structure. PLoS ONE 7:e33401 [Google Scholar]
  90. Nam KH, Kurinov I, Ke AL. 90.  2011. Crystal structure of clustered regularly interspaced short palindromic repeats (CRISPR)-associated Csn2 protein revealed Ca2+-dependent double-stranded DNA binding activity. J. Biol. Chem. 286:30759–68 [Google Scholar]
  91. Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E. 91.  2012. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun. 3:945 [Google Scholar]
  92. Swarts DC, Mosterd C, van Passel MW, Brouns SJ. 92.  2012. CRISPR interference directs strand specific spacer acquisition. PLoS ONE 7:e35888 [Google Scholar]
  93. Babu M, Beloglazova N, Flick R, Graham C, Skarina T. 93.  et al. 2011. A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol. Microbiol. 79:484–502 [Google Scholar]
  94. Beloglazova N, Brown G, Zimmerman MD, Proudfoot M, Makarova KS. 94.  et al. 2008. A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J. Biol. Chem. 283:20361–71 [Google Scholar]
  95. Wiedenheft B, Zhou K, Jinek M, Coyle SM, Ma W, Doudna JA. 95.  2009. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated antiviral defense. Structure 17:904–12 [Google Scholar]
  96. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. 96.  2010. Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet. 26:335–40 [Google Scholar]
  97. Gudbergsdottir S, Deng L, Chen Z, Jensen JV, Jensen LR. 97.  et al. 2011. Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol. Microbiol. 79:35–49 [Google Scholar]
  98. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER. 98.  et al. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl. Acad. Sci. USA 108:10098–103 [Google Scholar]
  99. Carte J, Pfister NT, Compton MM, Terns RM, Terns MP. 99.  2010. Binding and cleavage of CRISPR RNA by Cas6. RNA 16:2181–88 [Google Scholar]
  100. Carte J, Wang R, Li H, Terns RM, Terns MP. 100.  2008. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 22:3489–96 [Google Scholar]
  101. Hatoum-Aslan A, Maniv I, Marraffini LA. 101.  2011. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc. Natl. Acad. Sci. USA 108:21218–22 [Google Scholar]
  102. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA. 102.  2010. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355–58 [Google Scholar]
  103. Haurwitz RE, Sternberg SH, Doudna JA. 103.  2012. Csy4 relies on an unusual catalytic dyad to position and cleave CRISPR RNA. EMBO J. 31:2824–32 [Google Scholar]
  104. Sternberg SH, Haurwitz RE, Doudna JA. 104.  2012. Mechanism of substrate selection by a highly specific CRISPR endoribonuclease. RNA 18:661–72 [Google Scholar]
  105. Wang RY, Li H. 105.  2012. The mysterious RAMP proteins and their roles in small RNA-based immunity. Protein Sci. 21:463–70 [Google Scholar]
  106. Maris C, Dominguez C, Allain FHT. 106.  2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272:2118–31 [Google Scholar]
  107. Ebihara A, Yao M, Masui R, Tanaka I, Yokoyama S, Kuramitsu S. 107.  2006. Crystal structure of hypothetical protein TTHB192 from Thermus thermophilus HB8 reveals a new protein family with an RNA recognition motif-like domain. Protein Sci. 15:1494–99 [Google Scholar]
  108. Wang R, Preamplume G, Terns MP, Terns RM, Li H. 108.  2011. Interaction of the Cas6 riboendonuclease with CRISPR RNAs: recognition and cleavage. Structure 19:257–64 [Google Scholar]
  109. Wang R, Zheng H, Preamplume G, Shao Y, Li H. 109.  2012. The impact of CRISPR repeat sequence on structures of a Cas6 protein-RNA complex. Protein Sci. 21:405–17 [Google Scholar]
  110. Hale C, Kleppe K, Terns RM, Terns MP. 110.  2008. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14:2572–79 [Google Scholar]
  111. Calnan BJ, Tidor B, Biancalana S, Hudson D, Frankel AD. 111.  1991. Arginine-mediated RNA recognition: the arginine fork. Science 252:1167–71 [Google Scholar]
  112. Yang W. 112.  2011. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44:1–93 [Google Scholar]
  113. Halford SE, Marko JF. 113.  2004. How do site-specific DNA-binding proteins find their targets?. Nucleic Acids Res. 32:3040–52 [Google Scholar]
  114. Westra ER, van Erp PBG, Künne T, Wong SP, Staals RHJ. 114.  et al. 2012. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell 46:595–605 [Google Scholar]
  115. Gowers DM, Halford SE. 115.  2003. Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J. 22:1410–18 [Google Scholar]
  116. Sashital DG, Wiedenheft B, Doudna JA. 116.  2012. Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell 48:606–15 [Google Scholar]
  117. Mulepati S, Orr A, Bailey S. 117.  2012. Crystal structure of the largest subunit of a bacterial RNA-guided immune complex and its role in DNA target binding. J. Biol. Chem. 287:22445–49 [Google Scholar]
  118. Banerjee A, Santos WL, Verdine GL. 118.  2006. Structure of a DNA glycosylase searching for lesions. Science 311:1153–57 [Google Scholar]
  119. Horton JR, Zhang X, Maunus R, Yang Z, Wilson GG. 119.  et al. 2006. DNA nicking by HinP1I endonuclease: bending, base flipping and minor groove expansion. Nucleic Acids Res. 34:939–48 [Google Scholar]
  120. Westra ER, Nilges B, van Erp PBG, van der Oost J, Dame RT, Brouns SJJ. 120.  2012. Cascade-mediated binding and bending of negatively supercoiled DNA. RNA Biol. 9:1134–1138 [Google Scholar]
  121. Beloglazova N, Petit P, Flick R, Brown G, Savchenko A, Yakunin AF. 121.  2011. Structure and activity of the Cas3 HD nuclease MJ0384, an effector enzyme of the CRISPR interference. EMBO J. 30:4616–27 [Google Scholar]
  122. Han D, Krauss G. 122.  2009. Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2. FEBS Lett. 583:771–76 [Google Scholar]
  123. Mulepati S, Bailey S. 123.  2011. Structural and biochemical analysis of the nuclease domain of the clustered regularly interspaced short palindromic repeat (CRISPR) associated protein 3 (CAS3). J. Biol. Chem. 286:31896–903 [Google Scholar]
  124. Sinkunas T, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 124.  2011. Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J. 30:1335–42 [Google Scholar]
  125. Marraffini LA, Sontheimer EJ. 125.  2010. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463:568–71 [Google Scholar]
  126. Sakamoto K, Agari Y, Agari K, Yokoyama S, Kuramitsu S, Shinkai A. 126.  2009. X-ray crystal structure of a CRISPR-associated RAMP module Cmr5 protein from Thermus thermophilus HB8. Proteins 75:528–32 [Google Scholar]
  127. Bolduc B, Shaughnessy DP, Wolf YI, Koonin EV, Roberto FF, Young M. 127.  2012. Identification of novel positive-strand RNA viruses by metagenomic analysis of archaea-dominated Yellowstone hot springs. J. Virol. 86:5562–73 [Google Scholar]
  128. Dennehy JJ. 128.  2009. Bacteriophages as model organisms for virus emergence research. Trends Microbiol. 17:450–57 [Google Scholar]
  129. Gómez P, Buckling A. 129.  2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106–9 [Google Scholar]
  130. Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A. 130.  2009. Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325:833 [Google Scholar]
  131. Andersson AF, Banfield JF. 131.  2008. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047–50 [Google Scholar]
  132. Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D. 132.  2009. Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4:e4169 [Google Scholar]
  133. Held NL, Whitaker RJ. 133.  2009. Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ. Microbiol. 11:457–66 [Google Scholar]
  134. Pride DT, Sun CL, Salzman J, Rao N, Loomer P. 134.  et al. 2012. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res. 21:126–36 [Google Scholar]
  135. Stern A, Mick E, Tirosh I, Sagy O, Sorek R. 135.  2012. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res. 10:1985–94 [Google Scholar]
  136. Rho M, Wu YW, Tang H, Doak TG, Ye Y. 136.  2012. Diverse CRISPRs evolving in human microbiomes. PLoS Genet. 8:e1002441 [Google Scholar]
  137. Sorokin VA, Gelfand MS, Artamonova II. 137.  2010. Evolutionary dynamics of clustered irregularly interspaced short palindromic repeat systems in the ocean metagenome. Appl. Environ. Microbiol. 76:2136–44 [Google Scholar]
  138. Levin BR. 138.  2010. Nasty viruses, costly plasmids, population dynamics, and the conditions for establishing and maintaining CRISPR-mediated adaptive immunity in bacteria. PLoS Genet. 6:e1001171 [Google Scholar]
  139. He J, Deem MW. 139.  2010. Heterogeneous diversity of spacers within CRISPR (clustered regularly interspaced short palindromic repeats). Phys. Rev. Lett. 105:128102 [Google Scholar]
  140. Haerter JO, Trusina A, Sneppen K. 140.  2011. Targeted bacterial immunity buffers phage diversity. J. Virol. 85:10554–60 [Google Scholar]
  141. Weinberger AD, Sun CL, Plucinski MM, Denef VJ, Thomas BC. 141.  et al. 2012. Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput. Biol. 8:e1002475 [Google Scholar]
  142. Childs LM, Held NL, Young MJ, Whitaker RJ, Weitz JS. 142.  2012. Multiscale model of CRISPR-induced coevolutionary dynamics: diversification at the interface of Lamarck and Darwin. Evolution 66:2015–29 [Google Scholar]
  143. Tyson GW, Banfield JF. 143.  2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10:200–7 [Google Scholar]
  144. Tringe SG, Rubin EM. 144.  2005. Metagenomics: DNA sequencing of environmental samples. Nat. Rev. Genet. 6:805–14 [Google Scholar]
  145. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS. 145.  et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65 [Google Scholar]
  146. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. 146.  2011. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474:604–8 [Google Scholar]
  147. Díez-Villaseñor C, Almendros C, García-Martínez J, Mojica FJ. 147.  2010. Diversity of CRISPR loci in Escherichia coli. Microbiology 156:1351–61 [Google Scholar]
  148. Held NL, Herrera A, Cadillo-Quiroz H, Whitaker RJ. 148.  2010. CRISPR associated diversity within a population of Sulfolobus islandicus. PLoS ONE 5:e12988 [Google Scholar]
  149. Hambly E, Suttle CA. 149.  2005. The viriosphere, diversity, and genetic exchange within phage communities. Curr. Opin. Microbiol. 8:444–50 [Google Scholar]
  150. Medhekar B, Miller JF. 150.  2007. Diversity-generating retroelements. Curr. Opin. Microbiol. 10:388–95 [Google Scholar]
  151. Dyall-Smith M. 151.  2011. Dangerous weapons: a cautionary tale of CRISPR defence. Mol. Microbiol. 79:3–6 [Google Scholar]
  152. Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ. 152.  et al. 2010. Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc. Natl. Acad. Sci. USA 107:2383–90 [Google Scholar]
  153. Naor A, Lapierre P, Mevarech M, Papke RT, Gophna U. 153.  2012. Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr. Biol. 22:1444–48 [Google Scholar]
  154. Guo P, Cheng Q, Xie P, Fan Y, Jiang W, Qin Z. 154.  2011. Characterization of the multiple CRISPR loci on Streptomyces linear plasmid pSHK1. Acta Biochim. Biophys. Sin. 43:630–39 [Google Scholar]
  155. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N. 155.  et al. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38:779–86 [Google Scholar]
  156. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA. 156.  et al. 2011. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21:1616–25 [Google Scholar]
  157. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brussow H. 157.  2003. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6:417–24 [Google Scholar]
  158. Samai P, Smith P, Shuman S. 158.  2010. Structure of a CRISPR-associated protein Cas2 from Desulfovibrio vulgaris. Acta Crystallogr. Sect. F 66:1552–56 [Google Scholar]
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