Degenerate target sites mediate rapid primed CRISPR adaptation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages

  Fineran, Peter C ^a,b   Gerritzen, Matthias J H ^a   Suárez Diez, María ^a   Kun̈ne, Tim ^a   Boekhorst, Jos ^c   Van Hijum, Sacha A F T ^c,d   Staals, Raymond H J ^a   Brouns, Stan J J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c NIZO FOOD RESEARCH   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Adaptive immunity; crRNA; Horizontal gene transfer; Next generation sequencing; Phage resistance

Indexed keywords

NUCLEOTIDE;

ARTICLE; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA FLANKING REGION; DNA LIBRARY; ESCHERICHIA COLI K 12; GENE MAPPING; GENE TARGETING; HIGH THROUGHPUT SCREENING; MISMATCH REPAIR; MOLECULAR SYSTEMATICS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL;

ADAPTIVE IMMUNITY; CRRNA; HORIZONTAL GENE TRANSFER; NEXT-GENERATION SEQUENCING; PHAGE RESISTANCE;

BASE PAIR MISMATCH; BASE SEQUENCE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DATABASES, GENETIC; ESCHERICHIA COLI K12; HIGH-THROUGHPUT SCREENING ASSAYS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOTIDE MOTIFS; PLASMIDS; RNA, BACTERIAL;

EID: 84899087750     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400071111     Document Type: Article

References (55)

1. Samson JE, Magadán AH, Sabri M, Moineau S (2013) Revenge of the phages: Defeating bacterial defences. Nat Rev Microbiol 11(10):675-687.
2. Richter C, Chang JT, Fineran PC (2012) Function and regulation of clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR associated (Cas) systems. Viruses 4(10):2291-2311.
3. Westra ER, et al. (2012) The CRISPRs, they are a-changin': How prokaryotes generate adaptive immunity. Annu Rev Genet 46:311-339.
4. Barrangou R (2013) CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip Rev RNA 4(3):267-278.
5. Sorek R, Lawrence CM, Wiedenheft B (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu Rev Biochem 82:237-266.
6. Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11(3):181-190.
7. Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482(7385):331-338.
8. Terns MP, Terns RM (2011) CRISPR-based adaptive immune systems. Curr Opin Microbiol 14(3):321-327.
9. Fineran PC, Charpentier E (2012) Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 434(2):202-209.
10. Makarova KS, et al. (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9(6):467-477.
11. Datsenko KA, et al. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 3:945.
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(12):5569-5576.
13. Barrangou R, et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819):1709-1712. (Pubitemid 46515624)
14. Deveau H, et al. (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190(4):1390-1400. (Pubitemid 351215022)
15. Horvath P, et al. (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190(4):1401-1412. (Pubitemid 351215023)
16. Garneau JE, et al. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468(7320):67-71.
17. 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 194(21):5728-5738.
18. 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 85(6):1044-1056.
19. Li M, Wang R, Zhao D, Xiang H (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res 42(4):2483-2492.
20. Swarts DC, Mosterd C, van Passel MW, Brouns SJ (2012) CRISPR interference directs strand specific spacer acquisition. PLoS ONE 7(4):e35888.
21. Díez-Villaseñor C, Guzmán NM, Almendros C, García-Martínez J, Mojica FJ (2013) CRISPR-spacer integration reporter plasmids reveal distinct genuine acquisition specificities among CRISPR-Cas I-E variants of Escherichia coli. RNA Biol 10(5):792-802.
22. Savitskaya E, Semenova E, Dedkov V, Metlitskaya A, Severinov K (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol 10(5):716-725.
23. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Almendros C (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155(Pt 3):733-740.
24. Semenova E, 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(25):10098-10103.
25. Vercoe RB, et al. (2013) Cytotoxic chromosomal targeting by CRISPR/Cas systems can reshape bacterial genomes and expel or remodel pathogenicity islands. PLoS Genet 9(4):e1003454.
26. Brouns SJ, et al. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321(5891):960-964.
27. Jore MM, et al. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol 18(5):529-536.
28. Wiedenheft B, et al. (2011) Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477(7365):486-489.
29. Rose RE (1988) The nucleotide sequence of pACYC184. Nucleic Acids Res 16(1):355.
30. Westra ER, et al. (2013) Type I-E CRISPR-cas systems discriminate target from nontarget DNA through base pairing-independent PAM recognition. PLoS Genet 9(9):e1003742.
31. Sinkunas T, et al. (2013) In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J 32(3):385-394.
32. Hall KB, McLaughlin LW (1991) Thermodynamic and structural properties of pentamer DNA.DNA, RNA.RNA, and DNA.RNA duplexes of identical sequence. Biochemistry 30(44):10606-10613.
33. Roberts RW, Crothers DM (1992) Stability and properties of double and triple helices: Dramatic effects of RNA or DNA backbone composition. Science 258(5087):1463-1466. (Pubitemid 23011000)
34. Sugimoto N, Nakano M, Nakano S (2000) Thermodynamics-structure relationship of single mismatches in RNA/DNA duplexes. Biochemistry 39(37):11270-11281.
35. Sapranauskas R, et al. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39(21):9275-9282.
36. Sun CL, et al. (2013) Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol 15(2):463-470.
37. Magadán AH, Dupuis ME, Villion M, Moineau S (2012) Cleavage of phage DNA by the Streptococcus thermophilus CRISPR3-Cas system. PLoS ONE 7(7):e40913.
38. Paez-Espino D, et al. (2013) Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat Commun 4:1430.
39. Biswas A, Gagnon JN, Brouns SJ, Fineran PC, Brown CM (2013) CRISPRTarget: Bioinformatic prediction and analysis of crRNA targets. RNA Biol 10(5):817-827.
40. Perez-Rodriguez R, et al. (2011) Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol Microbiol 79(3):584-599.
41. Manica A, Zebec Z, Steinkellner J, Schleper C (2013) Unexpectedly broad target recognition of the CRISPR-mediated virus defence system in the archaeon Sulfolobus solfataricus. Nucleic Acids Res 41(22):10509-10517.
42. Touchon M, et al. (2011) CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J Bacteriol 193(10):2460-2467.
43. Touchon M, Rocha EP (2010) The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS ONE 5(6):e11126.
44. Díez-Villaseñor C, Almendros C, García- Martínez J, Mojica FJ (2010) Diversity of CRISPR loci in Escherichia coli. Microbiology 156(Pt 5):1351-1361.
45. Yosef I, et al. (2013) DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc Natl Acad Sci USA 110(35):14396-14401.
46. Künne T, Swarts DC, Brouns SJ (2014) Planting the seed: Target recognition of short guide RNAs. Trends Microbiol 22(2):74-83.
47. Shah SA, Erdmann S, Mojica FJ, Garrett RA (2013) Protospacer recognition motifs: Mixed identities and functional diversity. RNA Biol 10(5):891-899.
48. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233-239.
49. Jinek M, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816-821.
50. Esvelt KM, et al. (2013) Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods 10(11):1116-1121.
51. Fonfara I, et al. (2014) Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res 42(4):2577-2590.
52. Westra ER, et al. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol Cell 46(5):595-605.
53. Sashital DG, Wiedenheft B, Doudna JA (2012) Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol Cell 46(5):606-615.
54. Staals RH, et al. (2013) Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Mol Cell 52(1):135-145.
55. Hale CR, et al. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139(5):945-956.