The CRISPRs, they are A-Changin': How prokaryotes generate adaptive immunity

Annual Review of Genetics

Volumn 46, Issue , 2012, Pages 311-339

  Westra, Edze R ^a   Swarts, Daan C ^a   Staals, Raymond H J ^a   Jore, Matthijs M ^a   Brouns, Stan J J ^a   Van Der Oost, John ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEIC ACID;

ADAPTATION; ADAPTIVE IMMUNITY; ARCHEAN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA DEGRADATION; DNA MODIFICATION; DNA RESTRICTION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; INFECTION; MICROARRAY ANALYSIS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN PROCESSING; REVIEW; VIRUS ATTACHMENT;

AMINO ACID MOTIFS; BACTERIOPHAGES; DEOXYRIBONUCLEASES, TYPE I SITE-SPECIFIC; DNA HELICASES; DNA, VIRAL; ENDODEOXYRIBONUCLEASES; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LYSOGENY; PROPHAGES; SPECIES SPECIFICITY; VIRUS INTERNALIZATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 84870180587     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-110711-155447     Document Type: Review

References (185)

1. Abedon ST. 2011. Facilitation of CRISPR adaptation. Bacteriophage 1:179-81
2. Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, Shinkai A. 2010. Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol. 395:270-81
3. Agari Y, Yokoyama S, Kuramitsu S, Shinkai A. 2008. X-ray crystal structure of a CRISPR-associated protein, Cse2, from Thermus thermophilus HB8. Proteins 73:1063-67
4. Aklujkar M, Lovley DR. 2010. Interference with histidyl-tRNA synthetase by aCRISPRspacer sequence as a factor in the evolution of Pelobacter carbinolicus. BMC Evol. Biol. 10:230
5. Al-Attar S, Westra ER, van der Oost J, Brouns SJ. 2011. Clustered regularly interspaced short palindromic repeats (CRISPRs): the hallmark of an ingenious antiviral defense mechanism in prokaryotes. Biol. Chem. 392:277-89
6. Altfeld M, Fadda L, Frleta D, Bhardwaj N. 2011. DCs and NK cells: critical effectors in the immune response to HIV-1. Nat. Rev. Immunol. 11:176-86
7. Ando T, Xu Q, Torres M, Kusugami K, Israel DA, Blaser MJ. 2000. Restriction-modification system differences in Helicobacter pylori are a barrier to interstrain plasmid transfer. Mol. Microbiol. 37:1052-65
8. Aravind L, Koonin EV. 1998. The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci. 23:469-72
9. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. 2011. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474:604-8
10. Babu M, Beloglazova N, Flick R, Graham C, Skarina T, et al. 2011. A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol. Microbiol. 79:484-502
11. Bachi B, Reiser J, Pirrotta V. 1979. Methylation and cleavage sequences of the EcoP1 restrictionmodification enzyme. J. Mol. Biol. 128:143-63
12. Bair CL, Black LW. 2007. A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. J. Mol. Biol. 366:768-78
13. Baranova N, Nikaido H. 2002. The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J. Bacteriol. 184:4168-76
14. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-12
15. Beloglazova N, Brown G, Zimmerman MD, Proudfoot M, Makarova KS, 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
16. Beloglazova N, Petit P, Flick R, Brown G, Savchenko A, Yakunin AF. 2011. Structure and activity of the Cas3 HD nucleaseMJ0384, an effector enzyme of the CRISPR interference. EMBO J. 30:4616-27
17. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273-97
18. Bickle TA, Kruger DH. 1993. Biology of DNA restriction. Microbiol. Rev. 57:434-50
19. Blower TR, Pei XY, Short FL, Fineran PC, Humphreys DP, et al. 2011. A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nat. Struct. Mol. Biol. 18:185-90
20. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551-61
21. Bossi L, Fuentes JA, Mora G, Figueroa-Bossi N. 2003. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185:6467-71
22. Boyd EF, Brussow H. 2002. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10:521-29
23. Boyer HW. 1971. DNA restriction and modification mechanisms in bacteria. Annu. Rev. Microbiol. 25:153-76
24. Brinkman AB, Ettema TJ, de Vos WM, van der Oost J. 2003. The Lrp family of transcriptional regulators. Mol. Microbiol. 48:287-94
25. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960-64
26. Brown SP, Le Chat L, De Paepe M, Taddei F. 2006. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16:2048-52
27. Brussow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560-602
28. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA. 2012. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. doi: 10.1128/JB.01184-12.
29. Cady KC, O'Toole GA. 2011. Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193:3433-45
30. Carre-Mlouka A, Gaumer S, Gay P, Petitjean AM, Coulondre C, et al. 2007. Control of sigma virus multiplication by the ref(2)P gene of Drosophila melanogaster: an in vivo study of the PB1 domain of Ref(2)P. Genetics 176:409-19
31. Carte J, Pfister NT, Compton MM, Terns RM, Terns MP. 2010. Binding and cleavage of CRISPR RNA by Cas6. RNA 16:2181-88
32. 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. 22:3489-96
33. Carthew RW, Sontheimer EJ. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642-55
34. Chen CC, Wu HY. 2005. LeuO protein delimits the transcriptionally active and repressive domains on the bacterial chromosome. J. Biol. Chem. 280:15111-21
35. ChopinMC, Chopin A, Bidnenko E. 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473-79
36. Craigie R. 2001. HIV integrase, a brief overview from chemistry to therapeutics. J. Biol. Chem. 276:23213-16
37. Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E. 2012. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun. 3:945
38. De la Cruz MA, Fernández-Mora M, Guadarrama C, Flores-Valdez MA, Bustamante VH, et al. 2007. LeuO antagonizes H-NS and StpA-dependent repression in Salmonella enterica ompS1. Mol. Microbiol. 66:727-43
39. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, et al. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602-7
40. Deng L, Kenchappa CS, Peng X, She Q, Garrett RA. 2011. Modulation of CRISPR locus transcription by the repeat-binding protein Cbp1 in Sulfolobus. Nucleic Acids Res. 40:2470-80
41. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, et al. 2008. Phage response to CRISPRencoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:1390-400
42. Diez-Villasenor C, Almendros C, Garcia-Martinez J, Mojica FJ. 2010. Diversity of CRISPR loci in Escherichia coli. Microbiology 156:1351-61
43. Dillon SC, Cameron AD, Hokamp K, Lucchini S, Hinton JC, Dorman CJ. 2010. Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol. Microbiol. 76:1250-65
44. Donahue JP, Israel DA, Peek RM, Blaser MJ, Miller GG. 2000. Overcoming the restriction barrier to plasmid transformation of Helicobacter pylori. Mol. Microbiol. 37:1066-74
45. Doyle M, Fookes M, Ivens A, Mangan MW, Wain J, Dorman CJ. 2007. An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315:251-52
46. Dulbecco R. 1952. Mutual exclusion between related phages. J. Bacteriol. 63:209-17
47. Ebihara A, Yao M, Masui R, Tanaka I, Yokoyama S, Kuramitsu S. 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
48. Edgar R, Qimron U. 2010. The Escherichia coli CRISPR system protects from lambda lysogenization, lysogens, and prophage induction. J. Bacteriol. 192:6291-94
49. Edson KM, Vinson SB, Stoltz DB, Summers MD. 1981. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host. Science 211:582-83
50. Ellinger P, Arslan Z, Wurm R, Tschapek B, MacKenzie C, et al. 2012. The crystal structure of the CRISPR-associated protein Csn2 from Streptococcus agalactiae. J. Struct. Biol. 178:350-62
51. Erdmann S, Garrett RA. 2012. Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol. Microbiol. doi:10.1111/j.1365- 2958.2012.08171.x
52. Esposito D, Craigie R. 1999. HIV integrase structure and function. Adv. Virus Res. 52:319-33
53. Fineran PC, Blower TR, Foulds IJ, HumphreysDP, Lilley KS, SalmondGP. 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA 106:894-99
54. Fischer S, Maier LK, Stoll B, Brendel J, Fischer E, et al. 2012. An archaeal immune system can detect multiple protospacer adjacent motifs (PAMs) to target invader DNA. J. Biol. Chem. doi
55. Forde A, Fitzgerald GF. 1999. Bacteriophage defence systems in lactic acid bacteria. Antonie Van Leeuwenhoek 76:89-113
56. Tarlinton RE, Meers J, Young PR. 2006. Retroviral invasion of the koala genome. Nature 442:79-81
57. Fox KL, Srikhanta YN, Jennings MP. 2007. Phase variable type III restriction-modification systems of host-adapted bacterial pathogens. Mol. Microbiol. 65:1375-79
58. French RC, Lesley SM, Graham AF, van Rooyen CE. 1951. Studies on the relationship between virus and host cell. III. The breakdown of P32 labelled T2r+ bacteriophage adsorbed to E. coli previously infected by other coliphages of the T group. Can. J. Med. Sci. 29:144-48
59. Garneau JE, Dupuis ME, VillionM, Romero DA, Barrangou R, et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67-71
60. Garvey P, Hill C, Fitzgerald GF. 1996. The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Appl. Environ. Microbiol. 62:676-79
61. Gesner EM, Schellenberg MJ, Garside EL, George MM, Macmillan AM. 2011. Recognition and maturation of effector RNAs in a CRISPR interference pathway. Nat. Struct. Mol. Biol. 18:688-92
62. Gomez P, Buckling A. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106-9
63. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform. 8:172
64. Groenen PM, Bunschoten AE, van SoolingenD, van Embden JD. 1993. Nature ofDNApolymorphism in the direct repeat cluster of Mycobacterium tuberculosis: application for strain differentiation by a novel typing method. Mol. Microbiol. 10:1057-65
65. Gudbergsdottir S, Deng L, Chen Z, Jensen JV, Jensen LR, et al. 2011. Dynamic properties of the Sulfolobus CRISPR/Cas andCRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol. Microbiol. 79:35-49
66. 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
67. Hale C, Kleppe K, Terns RM, Terns MP. 2008. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14:2572-79
68. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, 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
69. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, et al. 2009. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:945-56
70. Hall AR, Scanlan PD, Morgan AD, Buckling A. 2011. Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett. 14:635-42
71. Han D, Krauss G. 2009. Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2. FEBS Lett. 583:771-76
72. Harris JR. 1991. The evolution of placental mammals. FEBS Lett. 295:3-4
73. Hatoum-Aslan A, Maniv I, Marraffini LA. 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
74. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA. 2010. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355-58
75. Haurwitz RE, Sternberg SH, Doudna JA. 2012. Csy4 relies on an unusual catalytic dyad to position and cleave CRISPR RNA. EMBO J. 31:2824-32
76. Heller KJ. 1992. Molecular interaction between bacteriophage and the gram-negative cell envelope. Arch. Microbiol. 158:235-48
77. Hernandez-Lucas I, Gallego-Hernandez AL, Encarnacion S, Fernandez-Mora M, Martinez-Batallar AG, et al. 2008. The LysR-type transcriptional regulator LeuO controls expression of several genes in Salmonella enterica serovar Typhi. J. Bacteriol. 190:1658-70
78. Hoe N, Nakashima K, Grigsby D, Pan X, Dou SJ, et al. 1999. Rapid molecular genetic subtyping of serotype M1 group A Streptococcus strains. Emerg. Infect. Dis. 5:254-63
79. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167-70
80. Horvath P, Romero DA, Coute-Monvoisin AC, Richards M, Deveau H, et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:1401-12
81. Hoskisson PA, Smith MC. 2007. Hypervariation and phase variation in the bacteriophage "resistome." Curr. Opin. Microbiol. 10:396-400
82. Hyman P, Abedon ST. 2010. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 70:217-48
83. Iida S, Meyer J, Bachi B, Stalhammar-Carlemalm M, Schrickel S, et al. 1983. DNA restrictionmodification genes of phage P1 and plasmid p15B. Structure and in vitro transcription. J. Mol. Biol. 165:1-18
84. Ishiguro EE, Kay WW, Ainsworth T, Chamberlain JB, Austen RA, et al. 1981. Loss of virulence during culture of Aeromonas salmonicida at high temperature. J. Bacteriol. 148:333-40
85. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. 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
86. Jansen R, van Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565-75
87. Jansen R, van Embden JD, Gaastra W, Schouls LM. 2002. Identification of a novel family of sequence repeats among prokaryotes. OMICS J. Integr. Biol. 6:23-33
88. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual- RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816-21
89. Jore MM, Brouns SJ, van der Oost J. 2012. RNA in defense: CRISPRs protect prokaryotes against mobile genetic elements. Cold Spring Harb. Perspect. Biol. 4:a003657
90. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER, et al. 2011. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18:529-36
91. Karginov FV, Hannon GJ. 2010. The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol. Cell 37:7-19
92. Klauck E, Böhringer J, Hengge-Aronis R. 1997. The LysR-like regulator LeuO in Escherichia coli is involved in the translational regulation of rpoS by affecting the expression of the small regulatory DsrARNA. Mol. Microbiol. 25:559-69
93. Kruger DH, Bickle TA. 1983. Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol. Rev. 47:345-60
94. KuninV, Sorek R, Hugenholtz P. 2007. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol. 8:R61
95. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317-27
96. Lehnherr H, Maguin E, Jafri S, Yarmolinsky MB. 1993. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 233:414-28
97. Lillestol RK, Redder P, Garrett RA, Brugger K. 2006. A putative viral defence mechanism in archaeal cells. Archaea 2:59-72
98. Lillestol RK, Shah SA, Brugger K, Redder P, Phan H, et al. 2009. CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties. Mol. Microbiol. 72:259-72
99. Lintner NG, KerouM, Brumfield SK, Graham S, Liu H, 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
100. Llave C. 2010. Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci. 15:701-7
101. Lu MJ, Henning U. 1994. Superinfection exclusion by T-even-type coliphages. Trends Microbiol. 2:137- 39
102. Majumder A, Fang M, Tsai KJ, Ueguchi C, Mizuno T, Wu HY. 2001. LeuO expression in response to starvation for branched-chain amino acids. J. Biol. Chem. 276:19046-51
103. Makarova KS, Aravind L, Grishin NV, Rogozin IB, Koonin EV. 2002. ADNArepair system specific for thermophilic archaea and bacteria predicted by genomic context analysis. Nucleic Acids Res. 30:482-96
104. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 2006. A putative RNA-interferencebased 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
105. Makarova KS, Haft DH, Barrangou R, Brouns SJ, CharpentierE, et al. 2011. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9:467-77
106. Manica A, ZebecZ, Teichmann D, Schleper C. 2011. In vivo activity ofCRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol. Microbiol. 80:481-91
107. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843-45
108. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181-90
109. Marraffini LA, Sontheimer EJ. 2010. Self versus non-self discrimination duringCRISPR RNA-directed immunity. Nature 463:568-71
110. Masepohl B, Gorlitz K, Bohme H. 1996. Long tandemly repeated repetitive (LTRR) sequences in the filamentous cyanobacterium Anabaena sp. PCC 7120. Biochim. Biophys. Acta 1307:26-30
111. McGrath S, Fitzgerald GF, van Sinderen D. 2002. Identification and characterization of phageresistance genes in temperate lactococcal bacteriophages. Mol. Microbiol. 43:509-20
112. Medina-Aparicio L, Rebollar-Flores JE, Gallego-Hernandez AL, Vazquez A, Olvera L, 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
113. Meisel A, Bickle TA, Kruger DH, Schroeder C. 1992. Type III restriction enzymes need two inversely oriented recognition sites for DNA cleavage. Nature 355:467-69
114. Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, LenskiRE. 2012. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335:428-32
115. Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, AlmendrosC. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733-40
116. 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. 60:174-82
117. Mojica FJ, Diez-Villasenor C, Soria E, Juez G. 2000. Biological significance of a family of regularly spaced repeats in the genomes of archaea, bacteria and mitochondria. Mol. Microbiol. 36:244-46
118. Mojica FJ, Ferrer C, Juez G, Rodriguez-Valera F. 1995. Long stretches of short tandem repeats are present in the largest replicons of the archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol. Microbiol. 17:85-93
119. Molineux IJ. 1991. Host-parasite interactions: recent developments in the genetics of abortive phage infections. New Biol. 3:230-36
120. Mulepati S, Bailey S. 2011. Structural and biochemical analysis of nuclease domain of clustered regularly interspaced short palindromic repeat (CRISPR)-associated protein 3 (Cas3). J. Biol. Chem. 286:31896- 903
121. Murray NE. 2000. Type I restriction systems: sophisticated molecular machines (a legacy of Bertani andWeigle). Microbiol. Mol. Biol. Rev. 64:412-34
122. Naito T, Kusano K, Kobayashi I. 1995. Selfish behavior of restriction-modification systems. Science 267:897-99
123. Nam KH, Ding F, Haitjema C, Huang Q, Delisa MP, Ke A. 2012. Double-stranded endonuclease activity in B. halodurans clustered regularly interspaced short palindromic repeats (CRISPR)-associated Cas2 protein. J. Biol. Chem. doi:10.1074/jbc.M112.382598
124. Nam KH, Haitjema C, Liu X, Ding F, Wang H, et al. 2012. Cas5d protein processes pre-crRNA and assembles Cascade-like interference complex in subtype I-C/Dvulg CRISPR-Cas system. Structure 20:1574-84
125. Nam KH, Kurinov I, Ke A. 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
126. NavarreWW, Porwollik S, Wang Y, McClellandM, Rosen H, et al. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236-38
127. Nordström K, Forsgren A. 1974. Effect of protein A on adsorption of bacteriophages to Staphylococcus aureus. J. Virol. 14:198-202
128. Nordström K, Forsgren A, Cox P. 1974. Prevention of bacteriophage adsorption to Staphylococcus aureus by immunoglobulin G. J. Virol. 14:203-6
129. Oliver KM, Degnan PH, Hunter MS, Moran NA. 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992-94
130. Peng X, Brugger K, Shen B, Chen L, She Q, Garrett RA. 2003. Genus-specific protein binding to the large clusters ofDNA repeats (short regularly spaced repeats) present in Sulfolobus genomes. J. Bacteriol. 185:2410-17
131. Perez-Rodriguez R, Haitjema C, Huang Q, Nam KH, Bernardis S, et al. 2011. Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol. Microbiol. 79:584-99
132. Pingoud A, FuxreiterM, Pingoud V, Wende W. 2005. Type II restriction endonucleases: structure and mechanism. Cell. Mol. Life Sci. 62:685-707
133. Plagens A, Tjaden B, Hagemann A, Randau L, Hensel R. 2012. Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J. Bacteriol. 194:2491- 500
134. Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M, et al. 2010. Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol. Microbiol. 77:1367-79
135. 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 151:653-63
136. Przybilski R, Richter C, Gristwood T, Clulow JS, Vercoe RB, Fineran PC. 2011. Csy4 is responsible for CRISPR RNA processing in Pectobacterium atrosepticum. RNA Biol. 8:517-28
137. PulU, Wurm R, Arslan Z, Geissen R, Hofmann N, Wagner R. 2010. Identification and characterization of E. coli CRISPR-Cas promoters and their silencing by H-NS. Mol. Microbiol. 75:1495-512
138. Riede I, Eschbach ML. 1986. Evidence that TraT interacts with OmpA of Escherichia coli. FEBS Lett. 205:241-45
139. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, et al. 2003. A nomenclature for restriction enzymes, DNAmethyltransferases, homing endonucleases and their genes. Nucleic Acids Res. 31:1805-12
140. Roossinck MJ. 2011. The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol. 9:99-108
141. Sashital DG, Jinek M, Doudna JA. 2011. An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol. 18:680-87
142. Sashital DG, Wiedenheft B, Doudna JA. 2012. Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell 46:606-15
143. Schnettler E, de VriesW, Hemmes H, Haasnoot J, Kormelink R, et al. 2009. The NS3 protein of rice hoja blanca virus complements the RNAi suppressor function of HIV-1 Tat. EMBO Rep. 10:258-63
144. Scholl D, Merril C. 2005. The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli. J. Bacteriol. 187:8499-503
145. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, 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
146. Semenova E, Nagornykh M, Pyatnitskiy M, Artamonova II, Severinov K. 2009. Analysis of CRISPR system function in plant pathogen Xanthomonas oryzae. FEMS Microbiol. Lett. 296:110-16
147. Shah SA, Hansen NR, Garrett RA. 2009. Distribution ofCRISPR spacermatches in viruses and plasmids of crenarchaeal acidothermophiles and implications for their inhibitory mechanism. Biochem. Soc. Trans. 37:23-28
148. Shimada T, Bridier A, Briandet R, Ishihama A. 2011. Novel roles of LeuO in transcription regulation of E. coli genome: antagonistic interplay with the universal silencer H-NS. Mol. Microbiol. 82:378-97
149. Shimada T, Yamamoto K, Ishihama A. 2009. Involvement of the leucine response transcription factor LeuO in regulation of the genes for sulfa drug efflux. J. Bacteriol. 191:4562-71
150. Shinkai A, Kira S, Nakagawa N, Kashihara A, Kuramitsu S, Yokoyama S. 2007. Transcription activation mediated by a cyclic AMP receptor protein from Thermus thermophilus HB8. J. Bacteriol. 189:3891-901
151. Sinkunas T, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 2011. Cas3 is a singlestranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J. 30:1335-42
152. Skennerton CT, Angly FE, Breitbart M, Bragg L, He S, et al. 2011. Phage encoded H-NS: a potential achilles heel in the bacterial defence system. PLoS ONE 6:e20095
153. Spector MP. 1998. The starvation-stress response (SSR) of Salmonella. Adv. Microb. Physiol. 40:233-79
154. Srikhanta YN, Fox KL, Jennings MP. 2010. The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol. 8:196-206
155. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. 2010. Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet. 26:335-40
156. Sternberg SH, Haurwitz RE, Doudna JA. 2012. Mechanism of substrate selection by a highly specific CRISPR endoribonuclease. RNA 18:661-72
157. Stoebel DM, Free A, Dorman CJ. 2008. Anti-silencing: overcoming H-NS-mediated repression of transcription in gram-negative enteric bacteria. Microbiology 154:2533-45
158. Studier FW, Bandyopadhyay PK. 1988. Model for how type I restriction enzymes select cleavage sites in DNA. Proc. Natl. Acad. Sci. USA 85:4677-81
159. Sumby P, Smith MCM. 2002. Genetics of the phage growth limitation (Pgl) system of Streptomyces coelicolor A3(2). Mol. Microbiol. 44:489-500
160. Sutherland IW, Hughes KA, Skillman LC, Tait K. 2004. The interaction of phage and biofilms. FEMS Microbiol. Lett. 232:1-6
161. Swarts DC, Mosterd C, van Passel MW, Brouns SJ. 2012. CRISPR interference directs strand specific spacer acquisition. PLoS ONE 7:e35888
162. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, 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
163. Tang TH, Polacek N, ZywickiM, HuberH, Brugger K, et al. 2005. Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol. Microbiol. 55:469-81
164. Terns MP, Terns RM. 2011. CRISPR-based adaptive immune systems. Curr. Opin.Microbiol. 14:321-27
165. Touchon M, Rocha EP. 2010. The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS ONE 5:e11126
166. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ. 2009. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34:401-7
167. van Embden JD, van Gorkom T, Kremer K, Jansen R, van Der Zeijst BA, Schouls LM. 2000. Genetic variation and evolutionary origin of the direct repeat locus of Mycobacterium tuberculosis complex bacteria. J. Bacteriol. 182:2393-401
168. van Rij RP, Berezikov E. 2009. Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol. 17:163-71
169. Voinnet O. 2005. Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6:206-20
170. Vovis GF, Horiuchi K, Zinder ND. 1974. Kinetics of methylation ofDNAby a restriction endonuclease from Escherichia coli B. Proc. Natl. Acad. Sci. USA 71:3810-13
171. Wang R, Preamplume G, Terns MP, Terns RM, Li H. 2011. Interaction of the Cas6 riboendonuclease with CRISPR RNAs: recognition and cleavage. Structure 19:257-64
172. Warren RA. 1980. Modified bases in bacteriophage DNAs. Annu. Rev. Microbiol. 34:137-58
173. Watanabe K, Ishibashi K, Nakashima Y, Sakurai T. 1984. A phage-resistant mutant of Lactobacillus casei which permits phage adsorption but not genome injection. J. Gen. Virol. 65:981-86
174. Westra ER, Pul U, Heidrich N, Jore MM, Lundgren M, 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
175. Westra ER, van Erp PBG, Künne T, Wong SP, Staals RHJ, 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
176. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJ, et al. 2011. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477:486-89
177. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, 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
178. Wiedenheft B, Zhou K, Jinek M, Coyle SM, Ma W, Doudna JA. 2009. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17:904-12
179. Williams E, Lowe TM, Savas J, DiRuggiero J. 2007. Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation. Extremophiles 11:19-29
180. Wyers F, Petitjean AM, Dru P, Gay P, Contamine D. 1995. Localization of domains within the Drosophila Ref(2)P protein involved in the intracellular control of sigma rhabdovirus multiplication. J. Virol. 69:4463-70
181. Yosef I, Goren MG, Kiro R, Edgar R, Qimron U. 2011. High-temperature protein G is essential for activity of the Escherichia coli clustered regularly interspaced short palindromic repeats (CRISPR)/Cas system. Proc. Natl. Acad. Sci. USA 108:20136-41
182. Yosef I, Goren MG, QimronU. 2012. Proteins andDNAelements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40:5569-76
183. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA. 2009. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191:210-19
184. Zhang H, Zheng X, Zhang Z. 2010. The role of vacuolar processing enzymes in plant immunity. Plant Signal. Behav. 5:1565-67
185. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, et al. 2012. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. Cell 3:303-13