The Discovery, Mechanisms, and Evolutionary Impact of Anti-CRISPRs

Annual Review of Virology

Volumn 4, Issue , 2017, Pages 37-59

  Borges, Adair L ^a   Davidson, Alan R ^b   Bondy Denomy, Joseph ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anti CRISPR; Bacteriophage; Cas9; CRISPR Cas

Indexed keywords

NUCLEIC ACID; VIRAL PROTEIN;

ARTICLE; BACTERIOPHAGE; CRISPR CAS SYSTEM; GENE EDITING; GENETIC ORGANIZATION; GENETIC VARIABILITY; HORIZONTAL GENE TRANSFER; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; REGULATOR GENE; STOICHIOMETRY; ARCHAEON; BACTERIUM; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYSIOLOGY; VIROLOGY;

ARCHAEA; BACTERIA; BACTERIOPHAGES; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; EVOLUTION, MOLECULAR; GENE EDITING; VIRAL PROTEINS;

EID: 85030331090     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-101416-041616     Document Type: Article

References (110)

1. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. 1999. Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. PNAS 96:2192-97
2. Cobián Güemes AG, YouleM, Cantú VA, Felts B, Nulton J, Rohwer F. 2016. Viruses as winners in the game of life. Annu. Rev. Virol. 3:197-214
3. Seed KD. 2015. Battling phages: how bacteria defend against viral attack. PLOS Pathog. 11:e1004847
4. Bebeacua C, Lorenzo Fajardo JC, Blangy S, Spinelli S, Bollmann S, 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
5. Cumby N, Edwards AM, Davidson AR, Maxwell KL. 2012. The bacteriophage HK97 gp15 moron element encodes a novel superinfection exclusion protein. J. Bacteriol. 194:5012-19
6. Cumby N, Reimer K, Mengin-Lecreulx D, Davidson AR, Maxwell KL. 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
7. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317-27
8. Westra ER, Swarts DC, Staals RHJ, Jore MM, Brouns SJJ, van der Oost J. 2012. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311-39
9. Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S, et al. 2015. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J. 34:169-83
10. Seed KD,LazinskiDW,Calderwood SB, Camilli A. 2013.A bacteriophage encodes its ownCRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489-91
11. Samson JE, Magadán AH, Sabri M, Moineau S. 2013. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11:675-87
12. Yosef I, Goren MG, Qimron U. 2012. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40:5569-76
13. Levy A, Goren MG, Yosef I, Auster O, Manor M, et al. 2015. CRISPR adaptation biases explain preference for acquisition of foreign DNA. Nature 520:505-10
14. Datsenko KA,Pougach K, Tikhonov A, WannerBL, Severinov K, Semenova E. 2012. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun. 3:945
15. 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(Pt. 3):653-63
16. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(Pt. 8):2551-61
17. Mojica FJM, Dez-Villasenor C, Garca-Martnez J, Soria E. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174-82
18. 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
19. 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
20. Makarova KS,Wolf YI, Alkhnbashi OS, Costa F, Shah SA, et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13:722-36
21. 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
22. Mulepati S, Bailey S. 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
23. Sternberg SH, LaFrance B, Kaplan M, Doudna JA. 2015. Conformational control ofDNAtarget cleavage by CRISPR-Cas9. Nature 527:110-13
24. JiangW, Samai P, Marraffini LA. 2016. Degradation of phage transcripts by CRISPR-associated RNases enables type III CRISPR-Cas immunity. Cell 164:710-21
25. Marraffini LA. 2015. CRISPR-Cas immunity in prokaryotes. Nature 526:55-61
26. Mohanraju P,MakarovaKS, Zetsche B, Zhang F, Koonin EV, van derOost J. 2016. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353:aad5147
27. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960-64
28. Westra ER, Nilges B, van Erp PBG, van der Oost J, Dame RT, Brouns SJJ. 2012. Cascade-mediated binding and bending of negatively supercoiled DNA. RNA Biol. 9:1134-38
29. Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. PNAS 109:E2579-86
30. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Sciece 337:816-21
31. Heler R, Samai P, Modell JW, Weiner C, Goldberg GW, et al. 2015. Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519:199-202
32. Garneau JE, DupuisME, VillionM, Romero DA, Barrangou R, et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67-71
33. Barrangou R, Doudna JA. 2016. Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34:933-41
34. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Almendros C. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733-40
35. Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H, et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:1401-12
36. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, et al. 2008. Phage response to CRISPRencoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:1390-400
37. 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. PNAS 108:10098-103
38. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C, 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
39. Nakayama K, Kanaya S, Ohnishi M, Terawaki Y, Hayashi T. 1999. The complete nucleotide sequence ofCTX, a cytotoxin-converting phage of Pseudomonas aeruginosa: implications for phage evolution and horizontal gene transfer via bacteriophages. Mol. Microbiol. 31:399-419
40. Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, et al. 2016. Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 10:2854-66
41. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. 2013. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493:429-32
42. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR,O'Toole GA. 2012. TheCRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. 194:5728-38
43. van Belkum A, Soriaga LB, LaFave MC, Akella S, Veyrieras JB, et al. 2015. Phylogenetic distribution of CRISPR-Cas systems in antibiotic-resistant Pseudomonas aeruginosa. mBio 6:e01796-15
44. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA. 2009. Interaction between bacteriophageDMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J. Bacteriol. 191:210-19
45. Cady KC, O'Toole GA. 2011. Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J. Bacteriol. 193:3433-45
46. Cady KC, White AS, Hammond JH, Abendroth MD, Karthikeyan RSG, et al. 2011. Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 157:430-37
47. Heussler GE, Cady KC, KoeppenK, Bhuju S, Stanton BA, O'Toole GA. 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
48. Pawluk A, Bondy-Denomy J, Cheung VHW, Maxwell KL, Davidson AR. 2014. A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa. mBio 5:e00896-14
49. Pawluk A, Staals RHJ, Taylor C,Watson BNJ, Saha S, et al. 2016. Inactivation of CRISPR-Cas systems by anti-CRISPR proteins in diverse bacterial species. Nat. Microbiol. 1:1-6
50. Pawluk A, AmraniN, Zhang Y, Garcia B, Hidalgo-Reyes Y, et al. 2016. Naturally occurring off-switches for CRISPR-Cas9. Cell 167:1829-29
51. Rauch BJ, Silvis MR, Hultquist JF,Waters CS, McGregor MJ, et al. 2016. Inhibition of CRISPR-Cas9 with bacteriophage proteins. Cell 168:150-58
52. Bondy-Denomy J, Davidson AR. 2014. To acquire or resist: the complex biological effects of CRISPRCas systems. Trends Microbiol. 22:218-25
53. Bondy-Denomy J, Garcia B, Strum S,DuM, RollinsMF, et al. 2015. Multiple mechanisms for CRISPRCas inhibition by anti-CRISPR proteins. Nature 526:136-39
54. Wang X, YaoD, Xu JG, Li AR, Xu J, et al. 2016. Structural basis of Cas3 inhibition by the bacteriophage protein AcrF3. Nat. Struct. Mol. Biol. 23:868-70
55. Wang J, Ma J, Cheng Z, Meng X, You L, et al. 2016. A CRISPR evolutionary arms race: structural insights into viral anti-CRISPR/Cas responses. Cell Res. 26:1165-68
56. Maxwell KL, Garcia B, Bondy-Denomy J, Bona D, Hidalgo-Reyes Y, Davidson AR. 2016. The solution structure of an anti-CRISPR protein. Nat. Commun. 7:13134
57. Stern A, Sorek R. 2011. The phage-host arms race: shaping the evolution of microbes. Bioessays 33:43-51
58. Arber W, Dussoix D. 1962. Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage. J. Mol. Biol. 5:18-36
59. Krüger DH, Bickle TA. 1983. Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol. Rev. 47:345-60
60. Dryden DTF, Tock MR. 2006. DNA mimicry by proteins. Biochem. Soc. Trans. 34(Pt. 2):317-19
61. Walkinshaw MD, Taylor P, Sturrock SS, Atanasiu C, Berge T, et al. 2002. Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol. Cell 9:187-94
62. McMahon SA, Roberts GA, Johnson KA, Cooper LP, Liu H, 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
63. Wang HC,WangHC, Ko TP, Lee YM, Leu JH, et al. 2008. White spot syndrome virus protein ICP11: a histone-binding DNA mimic that disrupts nucleosome assembly. PNAS 105:20758-63
64. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, et al. 2016. C2c2 is a singlecomponent programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573
65. Soutourina OA, Monot M, Boudry P, Saujet L, Pichon C, et al. 2013. Genome-wide identification of regulatory RNAs in the human pathogen Clostridium difficile. PLOS Genet. 9:e1003493
66. Wiedenheft B, Zhou K, JinekM,Coyle SM,MaW,Doudna JA. 2009. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17:904-12
67. LuoML, Mullis AS, Leenay RT, BeiselCL. 2014. Repurposing endogenous type ICRISPR-Cas systems for programmable gene repression. Nucleic Acids Res. 43:674-81
68. Rath D, Amlinger L, Hoekzema M, Devulapally PR, Lundgren M. 2015. Efficient programmable gene silencing by Cascade. Nucleic Acids Res. 43:237-46
69. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173-83
70. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, et al. 2013. CRISPR-mediated modular RNAguided regulation of transcription in eukaryotes. Cell 154:442-51
71. Vorontsova D, Datsenko KA,Medvedeva S, Bondy-Denomy J, Savitskaya EE, et al. 2015. ForeignDNA acquisition by the I-F CRISPR-Cas system requires all components of the interferencemachinery. Nucleic Acids Res. 43:10848-60
72. Bryson AL, Hwang Y, Sherrill-Mix S, Wu GD, Lewis JD, et al. 2015. Covalent modification of bacteriophage T4 DNA inhibits CRISPR-Cas9. mBio 6:e00648-15
73. Strotskaya A, Savitskaya E, Metlitskaya A, Morozova N, Datsenko KA, 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
74. Yaung SJ, Esvelt KM, Church GM. 2014. CRISPR/Cas9-mediated phage resistance is not impeded by the DNA modifications of phage T4. PLOS ONE 9:e98811
75. Hatfull GF, Hendrix RW. 2011. Bacteriophages and their genomes. Curr. Opin. Virol. 1:298-303
76. Botstein D. 1980. A theory of modular evolution for bacteriophages. Ann. N. Y. Acad. Sci. 354:484-90
77. Comeau AM, Bertrand C, Letarov A, Tétart F, KrischHM. 2007. Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 362:384-96
78. Hatfull GF. 2008. Bacteriophage genomics. Curr. Opin. Microbiol. 11:447-53
79. Hatfull GF. 2015. Dark matter of the biosphere: the amazing world of bacteriophage diversity. J. Virol. 89:8107-10
80. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. 2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299:27-51
81. Cumby N, Davidson AR, Maxwell KL. 2012. The moron comes of age. Bacteriophage 2:225-28
82. Bondy-Denomy J, Davidson AR. 2014. When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness. J. Microbiol. 52:235-42
83. Brüssow 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
84. Dedrick RM, Jacobs-Sera D, Bustamante CAG, Garlena RA, Mavrich TN, et al. 2017. Prophagemediated defence against viral attack and viral counter-defence. Nat. Microbiol. 2:16251
85. Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc. R. Soc. B 205:489-511
86. Betts A, KaltzO,HochbergME. 2014. Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. PNAS 111:11109-14
87. Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS, et al. 2012. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150:831-41
88. Cazares A, Mendoza-Hernández G, Guarneros G. 2014. Core and accessory genome architecture in a group of Pseudomonas aeruginosa Mu-like phages. BMC Genom. 15:1146
89. Westra ER, van Houte S, Oyesiku-Blakemore S,Makin B, Broniewski JM, et al. 2015. Parasite exposure drives selective evolution of constitutive versus inducible defense. Curr. Biol. 25:1043-49
90. Childs LM, England WE, Young MJ, Weitz JS, Whitaker RJ. 2014. CRISPR-induced distributed immunity in microbial populations. PLOS ONE 9:e101710
91. van Houte S, Ekroth AKE, Broniewski JM, Chabas H, Ashby B, et al. 2016. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532:385-88
92. Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N, et al. 2017. Diversity and evolution of class 2 CRISPR-Cas systems. Nat. Rev. Microbiol. 15:169-82
93. Carte J, Christopher RT, Smith JT, Olson S, Barrangou R, 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
94. 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
95. Patterson AG, Jackson SA, Taylor C, Evans GB, Salmond GPC, et al. 2016. Quorum sensing controls adaptive immunity through the regulation of multiple CRISPR-Cas systems. Mol. Cell 64:1102-8
96. Høyland-Kroghsbo NM, Paczkowski J, Mukherjee S, Broniewski J, Westra E, et al. 2016. Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system. PNAS 114:131-35
97. Medina-Aparicio L, Rebollar-Flores JE, Gallego-Hernández AL, Vázquez 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
98. Patterson AG, Chang JT, Taylor C, Fineran PC. 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
99. Agari Y, Sakamoto K, TamakoshiM, Oshima T, Kuramitsu S, Shinkai A. 2010. Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J. Mol. Biol. 395:270-81
100. Young JC, Dill BD, Pan C, Hettich RL, Banfield JF, et al. 2012. Phage-induced expression of CRISPRassociated proteins is revealed by shotgun proteomics in Streptococcus thermophilus. PLOS ONE 7:e38077
101. Goldberg GW, JiangW, Bikard D,Marraffini LA. 2014. Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514:633-37
102. Westra ER, Buckling A, Fineran PC. 2014. CRISPR-Cas systems: beyond adaptive immunity. Nat. Rev. Microbiol. 12:317-26
103. Sampson TR, Saroj SD, Llewellyn AC, Tzeng YL, Weiss DS. 2013. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254-57
104. Li R, Fang L, Tan S, Yu M, Li X, et al. 2016. Type I CRISPR-Cas targets endogenous genes and regulates virulence to evade mammalian host immunity. Cell Res. 26:1273-87
105. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843-45
106. Bikard D, Hatoum-Aslan A, Mucida D, Marraffini LA. 2012. CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12:177-86
107. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:e00227-10
108. Edgar R,QimronU. 2010. The Escherichia coli CRISPR system protects from lysogenization, lysogens, and prophage induction. J. Bacteriol. 192:6291-94
109. Gophna U, Kristensen DM,Wolf YI, Popa O, Drevet C, Koonin EV. 2015. No evidence of inhibition of horizontal gene transfer by CRISPR-Cas on evolutionary timescales. ISME J. 9:2021-27
110. Chung IY, Jang HJ, BaeHW,Cho YH. 2014. A phage protein that inhibits the bacterial ATPase required for type IV pilus assembly. PNAS 111:11503-8