1932

Abstract

Bacteria and archaea use CRISPR-Cas adaptive immune systems to defend themselves from infection by bacteriophages (phages). These RNA-guided nucleases are powerful weapons in the fight against foreign DNA, such as phages and plasmids, as well as a revolutionary gene editing tool. Phages are not passive bystanders in their interactions with CRISPR-Cas systems, however; recent discoveries have described phage genes that inhibit CRISPR-Cas function. More than 20 protein families, previously of unknown function, have been ascribed anti-CRISPR function. Here, we discuss how these CRISPR-Cas inhibitors were discovered and their modes of action were elucidated. We also consider the potential impact of anti-CRISPRs on bacterial and phage evolution. Finally, we speculate about the future of this field.

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2017-09-29
2024-05-18
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Literature Cited

  1. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. 1.  1999. Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. PNAS 96:2192–97 [Google Scholar]
  2. Cobián Güemes AG, Youle M, Cantú VA, Felts B, Nulton J, Rohwer F. 2.  2016. Viruses as winners in the game of life. Annu. Rev. Virol. 3:197–214 [Google Scholar]
  3. Seed KD. 3.  2015. Battling phages: how bacteria defend against viral attack. PLOS Pathog 11:e1004847 [Google Scholar]
  4. Bebeacua C, Lorenzo Fajardo JC, Blangy S, Spinelli S, Bollmann S. 4.  et al. 2013. X-ray structure of a superinfection exclusion lipoprotein from phage TP-J34 and identification of the tape measure protein as its target. Mol. Microbiol. 89:152–65 [Google Scholar]
  5. Cumby N, Edwards AM, Davidson AR, Maxwell KL. 5.  2012. The bacteriophage HK97 gp15 moron element encodes a novel superinfection exclusion protein. J. Bacteriol. 194:5012–19 [Google Scholar]
  6. Cumby N, Reimer K, Mengin-Lecreulx D, Davidson AR, Maxwell KL. 6.  2014. The phage tail tape measure protein, an inner membrane protein, and a periplasmic chaperone play connected roles in the genome injection process of E.coli phage HK97. Mol. Microbiol. 96:437–47 [Google Scholar]
  7. Labrie SJ, Samson JE, Moineau S. 7.  2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27 [Google Scholar]
  8. Westra ER, Swarts DC, Staals RHJ, Jore MM, Brouns SJJ, van der Oost J. 8.  2012. The CRISPRs, they are a-changin’: how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311–39 [Google Scholar]
  9. Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S. 9.  et al. 2015. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J 34:169–83 [Google Scholar]
  10. Seed KD, Lazinski DW, Calderwood SB, Camilli A. 10.  2013. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489–91 [Google Scholar]
  11. Samson JE, Magadán AH, Sabri M, Moineau S. 11.  2013. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11:675–87 [Google Scholar]
  12. Yosef I, Goren MG, Qimron U. 12.  2012. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 40:5569–76 [Google Scholar]
  13. Levy A, Goren MG, Yosef I, Auster O, Manor M. 13.  et al. 2015. CRISPR adaptation biases explain preference for acquisition of foreign DNA. Nature 520:505–10 [Google Scholar]
  14. Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E. 14.  2012. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun. 3:945 [Google Scholar]
  15. Pourcel C, Salvignol G, Vergnaud G. 15.  2005. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:Pt. 3653–63 [Google Scholar]
  16. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. 16.  2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:Pt. 82551–61 [Google Scholar]
  17. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Soria E. 17.  2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174–82 [Google Scholar]
  18. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA. 18.  2010. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355–58 [Google Scholar]
  19. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y. 19.  et al. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–7 [Google Scholar]
  20. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA. 20.  et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13:722–36 [Google Scholar]
  21. Westra ER, van Erp PBG, Künne T, Wong SP, Staals RHJ. 21.  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]
  22. Mulepati S, Bailey S. 22.  2013. In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA target. J. Biol. Chem. 288:22184–92 [Google Scholar]
  23. Sternberg SH, LaFrance B, Kaplan M, Doudna JA. 23.  2015. Conformational control of DNA target cleavage by CRISPR-Cas9. Nature 527:110–13 [Google Scholar]
  24. Jiang W, Samai P, Marraffini LA. 24.  2016. Degradation of phage transcripts by CRISPR-associated RNases enables type III CRISPR-Cas immunity. Cell 164:710–21 [Google Scholar]
  25. Marraffini LA. 25.  2015. CRISPR-Cas immunity in prokaryotes. Nature 526:55–61 [Google Scholar]
  26. Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV, van der Oost J. 26.  2016. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353:aad5147 [Google Scholar]
  27. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH. 27.  et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–64 [Google Scholar]
  28. Westra ER, Nilges B, van Erp PBG, van der Oost J, Dame RT, Brouns SJJ. 28.  2012. Cascade-mediated binding and bending of negatively supercoiled DNA. RNA Biol 9:1134–38 [Google Scholar]
  29. Gasiunas G, Barrangou R, Horvath P, Siksnys V. 29.  2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. PNAS 109:E2579–86 [Google Scholar]
  30. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 30.  2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–21 [Google Scholar]
  31. Heler R, Samai P, Modell JW, Weiner C, Goldberg GW. 31.  et al. 2015. Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519:199–202 [Google Scholar]
  32. Garneau JE, Dupuis , Villion M, Romero DA, Barrangou R. 32.  et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71 [Google Scholar]
  33. Barrangou R, Doudna JA. 33.  2016. Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34:933–41 [Google Scholar]
  34. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Almendros C. 34.  2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733–40 [Google Scholar]
  35. Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H. 35.  et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:1401–12 [Google Scholar]
  36. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C. 36.  et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:1390–400 [Google Scholar]
  37. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER. 37.  et al. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. PNAS 108:10098–103 [Google Scholar]
  38. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C. 38.  et al. 2009. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Res. 19:12–23 [Google Scholar]
  39. Nakayama K, Kanaya S, Ohnishi M, Terawaki Y, Hayashi T. 39.  1999. The complete nucleotide sequence of φCTX, a cytotoxin-converting phage of Pseudomonas aeruginosa: implications for phage evolution and horizontal gene transfer via bacteriophages. Mol. Microbiol. 31:399–419 [Google Scholar]
  40. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS. 40.  et al. 2016. Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10:2854–66 [Google Scholar]
  41. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. 41.  2013. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493:429–32 [Google Scholar]
  42. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA. 42.  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]
  43. van Belkum A, Soriaga LB, LaFave MC, Akella S, Veyrieras JB. 43.  et al. 2015. Phylogenetic distribution of CRISPR-Cas systems in antibiotic-resistant Pseudomonas aeruginosa. mBio 6:e01796–15 [Google Scholar]
  44. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA. 44.  2009. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191:210–19 [Google Scholar]
  45. Cady KC, O'Toole GA. 45.  2011. Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193:3433–45 [Google Scholar]
  46. Cady KC, White AS, Hammond JH, Abendroth MD, Karthikeyan RSG. 46.  et al. 2011. Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 157:430–37 [Google Scholar]
  47. Heussler GE, Cady KC, Koeppen K, Bhuju S, Stanton BA, O'Toole GA. 47.  2015. Clustered regularly interspaced short palindromic repeat-dependent, biofilm-specific death of Pseudomonas aeruginosa mediated by increased expression of phage-related genes. mBio 6:e00129–15 [Google Scholar]
  48. Pawluk A, Bondy-Denomy J, Cheung VHW, Maxwell KL, Davidson AR. 48.  2014. A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa. mBio 5:e00896–14 [Google Scholar]
  49. Pawluk A, Staals RHJ, Taylor C, Watson BNJ, Saha S. 49.  et al. 2016. Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol. 1:1–6 [Google Scholar]
  50. Pawluk A, Amrani N, Zhang Y, Garcia B, Hidalgo-Reyes Y. 50.  et al. 2016. Naturally occurring off-switches for CRISPR-Cas9. Cell 167:1829–29 [Google Scholar]
  51. Rauch BJ, Silvis MR, Hultquist JF, Waters CS, McGregor MJ. 51.  et al. 2016. Inhibition of CRISPR-Cas9 with bacteriophage proteins. Cell 168:150–58 [Google Scholar]
  52. Bondy-Denomy J, Davidson AR. 52.  2014. To acquire or resist: the complex biological effects of CRISPR-Cas systems. Trends Microbiol 22:218–25 [Google Scholar]
  53. Bondy-Denomy J, Garcia B, Strum S, Du M, Rollins MF. 53.  et al. 2015. Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature 526:136–39 [Google Scholar]
  54. Wang X, Yao D, Xu JG, Li AR, Xu J. 54.  et al. 2016. Structural basis of Cas3 inhibition by the bacteriophage protein AcrF3. Nat. Struct. Mol. Biol. 23:868–70 [Google Scholar]
  55. Wang J, Ma J, Cheng Z, Meng X, You L. 55.  et al. 2016. A CRISPR evolutionary arms race: structural insights into viral anti-CRISPR/Cas responses. Cell Res 26:1165–68 [Google Scholar]
  56. Maxwell KL, Garcia B, Bondy-Denomy J, Bona D, Hidalgo-Reyes Y, Davidson AR. 56.  2016. The solution structure of an anti-CRISPR protein. Nat. Commun. 7:13134 [Google Scholar]
  57. Stern A, Sorek R. 57.  2011. The phage-host arms race: shaping the evolution of microbes. Bioessays 33:43–51 [Google Scholar]
  58. Arber W, Dussoix D. 58.  1962. Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage λ.. J. Mol. Biol. 5:18–36 [Google Scholar]
  59. Krüger DH, Bickle TA. 59.  1983. Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol. Rev. 47:345–60 [Google Scholar]
  60. Dryden DTF, Tock MR. 60.  2006. DNA mimicry by proteins. Biochem. Soc. Trans. 34:Pt. 2317–19 [Google Scholar]
  61. Walkinshaw MD, Taylor P, Sturrock SS, Atanasiu C, Berge T. 61.  et al. 2002. Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol. Cell 9:187–94 [Google Scholar]
  62. McMahon SA, Roberts GA, Johnson KA, Cooper LP, Liu H. 62.  et al. 2009. Extensive DNA mimicry by the ArdA anti-restriction protein and its role in the spread of antibiotic resistance. Nucleic Acids Res 37:4887–97 [Google Scholar]
  63. Wang HC, Wang HC, Ko TP, Lee YM, Leu JH. 63.  et al. 2008. White spot syndrome virus protein ICP11: a histone-binding DNA mimic that disrupts nucleosome assembly. PNAS 105:20758–63 [Google Scholar]
  64. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM. 64.  et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573 [Google Scholar]
  65. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C. 65.  et al. 2013. Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLOS Genet. 9:e1003493 [Google Scholar]
  66. Wiedenheft B, Zhou K, Jinek M, Coyle SM, Ma W, Doudna JA. 66.  2009. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17:904–12 [Google Scholar]
  67. Luo ML, Mullis AS, Leenay RT, Beisel CL. 67.  2014. Repurposing endogenous type I CRISPR-Cas systems for programmable gene repression. Nucleic Acids Res 43:674–81 [Google Scholar]
  68. Rath D, Amlinger L, Hoekzema M, Devulapally PR, Lundgren M. 68.  2015. Efficient programmable gene silencing by Cascade. Nucleic Acids Res 43:237–46 [Google Scholar]
  69. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS. 69.  et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–83 [Google Scholar]
  70. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA. 70.  et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–51 [Google Scholar]
  71. Vorontsova D, Datsenko KA, Medvedeva S, Bondy-Denomy J, Savitskaya EE. 71.  et al. 2015. Foreign DNA acquisition by the I-F CRISPR-Cas system requires all components of the interference machinery. Nucleic Acids Res 43:10848–60 [Google Scholar]
  72. Bryson AL, Hwang Y, Sherrill-Mix S, Wu GD, Lewis JD. 72.  et al. 2015. Covalent modification of bacteriophage T4 DNA inhibits CRISPR-Cas9. mBio 6:e00648–15 [Google Scholar]
  73. Strotskaya A, Savitskaya E, Metlitskaya A, Morozova N, Datsenko KA. 73.  et al. 2017. The action of Escherichia coli CRISPR-Cas system on lytic bacteriophages with different lifestyles and development strategies. Nucleic Acids Res 45:1946–57 [Google Scholar]
  74. Yaung SJ, Esvelt KM, Church GM. 74.  2014. CRISPR/Cas9-mediated phage resistance is not impeded by the DNA modifications of phage T4. PLOS ONE 9:e98811 [Google Scholar]
  75. Hatfull GF, Hendrix RW. 75.  2011. Bacteriophages and their genomes. Curr. Opin. Virol. 1:298–303 [Google Scholar]
  76. Botstein D. 76.  1980. A theory of modular evolution for bacteriophages. Ann. N. Y. Acad. Sci. 354:484–90 [Google Scholar]
  77. Comeau AM, Bertrand C, Letarov A, Tétart F, Krisch HM. 77.  2007. Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 362:384–96 [Google Scholar]
  78. Hatfull GF. 78.  2008. Bacteriophage genomics. Curr. Opin. Microbiol. 11:447–53 [Google Scholar]
  79. Hatfull GF. 79.  2015. Dark matter of the biosphere: the amazing world of bacteriophage diversity. J. Virol. 89:8107–10 [Google Scholar]
  80. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. 80.  2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299:27–51 [Google Scholar]
  81. Cumby N, Davidson AR, Maxwell KL. 81.  2012. The moron comes of age. Bacteriophage 2:225–28 [Google Scholar]
  82. Bondy-Denomy J, Davidson AR. 82.  2014. When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness. J. Microbiol. 52:235–42 [Google Scholar]
  83. Brüssow H, Canchaya C, Hardt WD. 83.  2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560–602 [Google Scholar]
  84. Dedrick RM, Jacobs-Sera D, Bustamante CAG, Garlena RA, Mavrich TN. 84.  et al. 2017. Prophage-mediated defence against viral attack and viral counter-defence. Nat. Microbiol. 2:16251 [Google Scholar]
  85. Dawkins R, Krebs JR. 85.  1979. Arms races between and within species. Proc. R. Soc. B 205:489–511 [Google Scholar]
  86. Betts A, Kaltz O, Hochberg ME. 86.  2014. Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. PNAS 111:11109–14 [Google Scholar]
  87. Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS. 87.  et al. 2012. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150:831–41 [Google Scholar]
  88. Cazares A, Mendoza-Hernández G, Guarneros G. 88.  2014. Core and accessory genome architecture in a group of Pseudomonas aeruginosa Mu-like phages. BMC Genom 15:1146 [Google Scholar]
  89. Westra ER, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM. 89.  et al. 2015. Parasite exposure drives selective evolution of constitutive versus inducible defense. Curr. Biol. 25:1043–49 [Google Scholar]
  90. Childs LM, England WE, Young MJ, Weitz JS, Whitaker RJ. 90.  2014. CRISPR-induced distributed immunity in microbial populations. PLOS ONE 9:e101710 [Google Scholar]
  91. van Houte S, Ekroth AKE, Broniewski JM, Chabas H, Ashby B. 91.  et al. 2016. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532:385–88 [Google Scholar]
  92. Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N. 92.  et al. 2017. Diversity and evolution of class 2 CRISPR-Cas systems. Nat. Rev. Microbiol. 15:169–82 [Google Scholar]
  93. Carte J, Christopher RT, Smith JT, Olson S, Barrangou R. 93.  et al. 2014. The three major types of CRISPR-Cas systems function independently in CRISPR RNA biogenesis in Streptococcus thermophilus. Mol. Microbiol. 93:98–112 [Google Scholar]
  94. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P. 94.  et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–12 [Google Scholar]
  95. Patterson AG, Jackson SA, Taylor C, Evans GB, Salmond GPC. 95.  et al. 2016. Quorum sensing controls adaptive immunity through the regulation of multiple CRISPR-Cas systems. Mol. Cell 64:1102–8 [Google Scholar]
  96. Høyland-Kroghsbo NM, Paczkowski J, Mukherjee S, Broniewski J, Westra E. 96.  et al. 2016. Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system. PNAS 114:131–35 [Google Scholar]
  97. Medina-Aparicio L, Rebollar-Flores JE, Gallego-Hernández AL, Vázquez A, Olvera L. 97.  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]
  98. Patterson AG, Chang JT, Taylor C, Fineran PC. 98.  2015. Regulation of the type I-F CRISPR-Cas system by CRP-cAMP and GalM controls spacer acquisition and interference. Nucleic Acids Res 43:6038–48 [Google Scholar]
  99. Agari Y, Sakamoto K, Tamakoshi M, Oshima T, Kuramitsu S, Shinkai A. 99.  2010. Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol. 395:270–81 [Google Scholar]
  100. Young JC, Dill BD, Pan C, Hettich RL, Banfield JF. 100.  et al. 2012. Phage-induced expression of CRISPR-associated proteins is revealed by shotgun proteomics in Streptococcus thermophilus. PLOS ONE 7:e38077 [Google Scholar]
  101. Goldberg GW, Jiang W, Bikard D, Marraffini LA. 101.  2014. Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514:633–37 [Google Scholar]
  102. Westra ER, Buckling A, Fineran PC. 102.  2014. CRISPR-Cas systems: beyond adaptive immunity. Nat. Rev. Microbiol. 12:317–26 [Google Scholar]
  103. Sampson TR, Saroj SD, Llewellyn AC, Tzeng YL, Weiss DS. 103.  2013. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254–57 [Google Scholar]
  104. Li R, Fang L, Tan S, Yu M, Li X. 104.  et al. 2016. Type I CRISPR-Cas targets endogenous genes and regulates virulence to evade mammalian host immunity. Cell Res 26:1273–87 [Google Scholar]
  105. Marraffini LA, Sontheimer EJ. 105.  2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–45 [Google Scholar]
  106. Bikard D, Hatoum-Aslan A, Mucida D, Marraffini LA. 106.  2012. CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12:177–86 [Google Scholar]
  107. Palmer KL, Gilmore MS. 107.  2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:e00227–10 [Google Scholar]
  108. Edgar R, Qimron U. 108.  2010. The Escherichia coli CRISPR system protects from λ lysogenization, lysogens, and prophage induction. J. Bacteriol. 192:6291–94 [Google Scholar]
  109. Gophna U, Kristensen DM, Wolf YI, Popa O, Drevet C, Koonin EV. 109.  2015. No evidence of inhibition of horizontal gene transfer by CRISPR-Cas on evolutionary timescales. ISME J 9:2021–27 [Google Scholar]
  110. Chung IY, Jang HJ, Bae HW, Cho YH. 110.  2014. A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. PNAS 111:11503–8 [Google Scholar]
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