The CRISPR-Cas immune system and genetic transfers: Reaching an equilibrium

Microbiology Spectrum

Volumn 3, Issue 1, 2015, Pages

  Samson, Julie E ^a   Magadan, Alfonso H ^a   Moineau, Sylvain ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

BACTERIUM; BACTERIUM CONJUGATION; CRISPR CAS SYSTEM; GENETIC TRANSFORMATION; GENETICS; HORIZONTAL GENE TRANSFER; INTERSPERSED REPEAT; METABOLISM; MOLECULAR EVOLUTION;

BACTERIA; CONJUGATION, GENETIC; CRISPR-CAS SYSTEMS; DNA; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; INTERSPERSED REPETITIVE SEQUENCES; TRANSFORMATION, GENETIC;

EID: 84959010234     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.PLAS-0034-2014     Document Type: Article

References (76)

1. 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 169:5429-5433.
2. Nakata A, Amemura M, Makino K. 1989. Unusual nucleotide arrangement with repeated sequences in the Escherichia coli K-12 chromosome. J Bacteriol 171:3553-3556.
3. Jansen R, Embden JD, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565-1575.
4. 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 36:244-246.
5. Deveau H, Garneau JE, Moineau S. 2010. CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475-493.
6. Terns MP, Terns RM. 2011. CRISPR-based adaptive immune systems. Curr Opin Microbiol 14:321-327.
7. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331-338.
8. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551-2561.
9. 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 60:174-182.
10. 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 151:653-663.
11. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709-1712.
12. Westra ER, Staals RH, Gort G, Hogh S, Neumann S, de la Cruz F, Fineran PC, Brouns SJ. 2013. CRISPR-Cas systems preferentially target the leading regions of MOBF conjugative plasmids. RNA Biol 10:749-761.
13. Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS, Schoen C, Vogel J, Sontheimer EJ. 2013. Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol Cell 50:488-503.
14. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843-1845.
15. Sampson TR, Weiss DS. 2014. CRISPR-Cas systems: new players in gene regulation and bacterial physiology. Front Cell Infect Microbiol 4:37.
16. Sampson TR, Saroj SD, Llewellyn AC, Tzeng YL, Weiss DS. 2013. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254-257.
17. Babu M, Beloglazova N, Flick R, Graham C, Skarina T, Nocek B, Gagarinova A, Pogoutse O, Brown G, Binkowski A, Phanse S, Joachimiak A, Koonin EV, Savchenko A, Emili A, Greenblatt J, Edwards AM, Yakunin AF. 2011. A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol Microbiol 79:484-502.
18. Louwen R, Horst-Kreft D, de Boer AG, van der Graaf L, de Knegt G, Hamersma M, Heikema AP, Timms AR, Jacobs BC, Wagenaar JA, Endtz HP, van der Oost J, Wells JM, Nieuwenhuis EE, van Vliet AH, Willemsen PT, van Baarlen P, van Belkum A. 2013. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barre syndrome. Eur J Clin Microbiol Infect Dis 32:207-226.
19. 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 191:210-219.
20. Cady KC, O'Toole GA. 2011. Non-identity-mediated CRISPRbacteriophage interaction mediated via the Csy and Cas3 proteins. J Bacteriol 193:3433-3445.
21. Viswanathan P, Murphy K, Julien B, Garza AG, Kroos L. 2007. Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats. J Bacteriol 189:3738-3750.
22. Makarova KS,Haft DH,Barrangou R,Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467-477.
23. Marraffini LA, Sontheimer EJ. 2010. CRISPRinterference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181-190.
24. Tyson GW, Banfield JF. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10:200-207.
25. Swarts DC, Mosterd C, van Passel MW, Brouns SJ. 2012. CRISPR interference directs strand specific spacer acquisition. PLoS One 7: e35888. doi:10.1371/journal.pone.0035888.
26. Hynes AP, Villion M, Moineau S. 2014. Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages. Nat Commun 5:4399.
27. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S. 2008. Phage response to CRISPRencoded resistance in Streptococcus thermophilus. J Bacteriol 190:1390- 1400.
28. Yosef I, Goren MG, Qimron U. 2012. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 40:5569-5576.
29. van der Oost J, Westra ER, Jackson RN, Wiedenheft B. 2014. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat Rev Microbiol 12:479-492.
30. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadan AH, Moineau S. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67-71.
31. Magadan AH, Dupuis ME, Villion M, Moineau S. 2012. Cleavage of phage DNA by the Streptococcus thermophilus CRISPR3-Cas system. PLoS One 7:e40913. doi:10.1371/journal.pone.0040913.
32. Shah SA, Erdmann S, Mojica FJ, Garrett RA. 2013. Protospacer recognition motifs: mixed identities and functional diversity. RNA Biol 10: 891-899.
33. Barrangou R, Marraffini LA. 2014. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol Cell 54:234-244.
34. Marraffini LA, Sontheimer EJ. 2010. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463:568-571.
35. Thomas CM, Nielsen KM. 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711-721.
36. Humphrey B, Thomson NR, Thomas CM, Brooks K, Sanders M, Delsol AA, Roe JM, Bennett PM, Enne VI. 2012. Fitness of Escherichia coli strains carrying expressed and partially silent IncN and IncP1 plasmids. BMC Microbiol 12:53.
37. Smith MA, Bidochka MJ. 1998. Bacterial fitness and plasmid loss: the importance of culture conditions and plasmid size. Can J Microbiol 44: 351-355.
38. De Gelder L, Ponciano JM, Joyce P, Top EM. 2007. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153:452-463.
39. Dahlberg C, Chao L. 2003. Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165:1641-1649.
40. Paulander W, Maisnier-Patin S, Andersson DI. 2009. The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (sigmaS). Genetics 183:539-546.
41. Johnston C, Martin B, Polard P, Claverys JP. 2013. Postreplication targeting of transformants by bacterial immune systems? Trends Microbiol 21:516-521.
42. Dupuis ME, Villion M, Magadan AH, Moineau S. 2013. CRISPR-Cas and restriction-modification systems are compatible and increase phage resistance. Nat Commun 4:2087.
43. Westra ER, Pul U, Heidrich N, Jore MM, Lundgren M, Stratmann T, Wurm R, Raine A, Mescher M, van Heereveld L, Mastop M, Wagner EG, Schnetz K, van der Oost J, Wagner R, Brouns SJ. 2010. H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol Microbiol 77:1380-1393.
44. Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M, Wanner BL, Severinov K. 2010. Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol Microbiol 77:1367-1379.
45. Fineran PC, Gerritzen MJ, Suarez-Diez M, Kunne T, Boekhorst J, van Hijum SA, Staals RH, Brouns SJ. 2014. Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci USA 111: E1629-1638.
46. 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.
47. 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 10:716-725.
48. 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 42:2483-2492.
49. Richter C, Dy RL, McKenzie RE, Watson BN, Taylor C, Chang JT, McNeil MB, Staals RH, Fineran PC. 2014. Priming in the type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bidirectionally from the primed protospacer. Nucleic Acids Res 42:8516-8526.
50. Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW, Duportet X, Fischetti VA, Marraffini LA. 2014. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat Biotechnol 32: 1146-1150.
51. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:e00227-10. doi:10.1128/mBio.00227-10.
52. Touchon M, Charpentier S, Pognard D, Picard B, Arlet G, Rocha EP, Denamur E, Branger C. 2012. Antibiotic resistance plasmids spread among natural isolates of Escherichia coli in spite of CRISPR elements. Microbiology 158:2997-3004.
53. Touchon M, Rocha EP. 2010. The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS One 5: e11126. doi:10.1371/journal.pone.0011126.
54. 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 12:177-186.
55. Jiang W, Maniv I, Arain F, Wang Y, Levin BR, Marraffini LA. 2013. Dealing with the evolutionary downside of CRISPR immunity: bacteria and beneficial plasmids. PLoS Genet 9:e1003844. doi:10.1371/journal .pgen.1003844.
56. Maier LK, Stoll B, Brendel J, Fischer S, Pfeiffer F, Dyall-Smith M, Marchfelder A. 2013. The ring of confidence: a haloarchaeal CRISPR/Cas system. Biochem Soc Trans 41:374-378.
57. Fischer S, Maier LK, Stoll B, Brendel J, Fischer E, Pfeiffer F, Dyall-Smith M, Marchfelder A. 2012. An archaeal immune system can detect multiple protospacer adjacent motifs (PAMs) to target invader DNA. J Biol Chem 287:33351-33363.
58. Gudbergsdottir S, Deng L, Chen Z, Jensen JV, Jensen LR, She Q, Garrett RA. 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.
59. Jorth P, Whiteley M. 2012. An evolutionary link between natural transformation and CRISPR adaptive immunity. mBio 3:e00309-12. doi:10.1128/mBio.00309-12.
60. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 2011. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39:9275- 9282.
61. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, Wanner B, van der Oost J, Brouns SJ, Severinov K. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci USA 108:10098- 10103.
62. Almendros C, Guzman NM, Diez-Villasenor C, Garcia-Martinez J, Mojica FJ. 2012. Target motifs affecting natural immunity by a constitutive CRISPR-Cas system in Escherichia coli. PLoS One 7:e50797. doi:10.1371/journal.pone.0050797.
63. Shmakov S, Savitskaya E, Semenova E, Logacheva MD, Datsenko KA, Severinov K. 2014. Pervasive generation of oppositely oriented spacers during CRISPR adaptation. Nucleic Acids Res 42:5907-5916.
64. Maier LK, Lange SJ, Stoll B, Haas KA, Fischer S, Fischer E, Duchardt-Ferner E, Wohnert J, Backofen R, Marchfelder A. 2013. Essential requirements for the detection and degradation of invaders by the Haloferax volcanii CRISPR/Cas system I-B. RNA Biol 10:865-874.
65. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, Poyart C, Rosinski-Chupin I, Glaser P. 2012. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 85:1057-1071.
66. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, Poyart C, Rosinski-Chupin I, Glaser P. 2012. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 85:1057-1071.
67. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602-607.
68. Elmore JR, Yokooji Y, Sato T, Olson S, Glover CV, Graveley BR, Atomi H, Terns RM, Terns MP. 2013. Programmable plasmid interference by the CRISPR-Cas system in Thermococcus kodakarensis. RNA Biol 10:828-840.
69. Garcillan-Barcia MP, Francia MV, de la Cruz F. 2009. The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33:657-687.
70. 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 85:1044-1056.
71. Erdmann S, Shah SA, Garrett RA. 2013. SMV1 virus-induced CRISPR spacer acquisition from the conjugative plasmid pMGB1 in Sulfolobus solfataricus P2. Biochem Soc Trans 41:1449-1458.
72. Sesto N, Touchon M, Andrade JM, Kondo J, Rocha EP, Arraiano CM, Archambaud C, Westhof E, Romby P, Cossart P. 2014. A PNPase dependent CRISPR system in Listeria. PLoS Genet 10:e1004065. doi:10.1371/journal.pgen.1004065.
73. Hatoum-Aslan A, Maniv I, Samai P, Marraffini LA. 2014. Genetic characterization of antiplasmid immunity through a type III-A CRISPRCas system. J Bacteriol 196:310-317.
74. Ivancic-Bace I, Radovcic M, Bockor L, Howard JL, Bolt EL. 2013. Cas3 stimulates runaway replication of a ColE1 plasmid in Escherichia coli and antagonises RNaseHI. RNA Biol 10:770-778.
75. Perez-Rodriguez R, Haitjema C, Huang Q, Nam KH, Bernardis S, Ke A, Delisa MP. 2011. Envelope stress is a trigger of CRISPR RNAmediated DNA silencing in Escherichia coli. Mol Microbiol 79:584-599.
76. Hatoum-Aslan A, Marraffini LA. 2014. Impact of CRISPR immunity on the emergence and virulence of bacterial pathogens. Curr Opin Microbiol 17:82-90