CRISPR-Cas systems preferentially target the leading regions of MOB F conjugative plasmids

RNA Biology

Volumn 10, Issue 5, 2013, Pages 749-761

  Westra, Edze R ^a   Staals, Raymond H J ^a   Gort, Gerrit ^a   Høgh, Søren ^a   Neumann, Sarah ^a,d   De La Cruz, Fernando ^b   Fineran, Peter C ^a,c   Brouns, Stan J J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b University of Cantabria   (Spain)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Adaptive immunity; Conjugation; CRISPR; Mobile genetic element; Plasmid mobilization; Protospacer distribution

Indexed keywords

PLASMID DNA; SINGLE STRANDED DNA; BACTERIAL PROTEIN; F FACTOR; MOB PROTEIN, BACTERIA;

ARTICLE; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; CAS GENE; CONJUGATION; CRISPR CAS SYSTEM; DNA SEQUENCE; DNA STRUCTURE; ESCHERICHIA COLI; GENE EXPRESSION; GENE LOCUS; GENE TRANSFER; NONHUMAN; PLASMID; SEQUENCE ALIGNMENT; TYPE I SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; BACTERIUM CONJUGATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ESCHERICHIA COLI K 12; GENETICS; IMMUNOLOGY; NUCLEOTIDE SEQUENCE;

ESCHERICHIA COLI; PROKARYOTA;

BACTERIAL PROTEINS; BASE SEQUENCE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CONJUGATION, GENETIC; CRISPR-CAS SYSTEMS; DNA, SINGLE-STRANDED; ESCHERICHIA COLI K12; F FACTOR;

EID: 84878831136     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.24202     Document Type: Article

References (102)

1. Nakamura Y, Itoh T, Matsuda H, Gojobori T. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 2004; 36:760-6; PMID:15208628; http://dx.doi.org/10.1038/ng1381.
2. de la Cruz F, Davies J. Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 2000; 8:128-33; PMID:10707066; http://dx.doi.org/10.1016/S0966-842X(00)01703-0.
3. Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 2005; 3:711-21; PMID:16138099; http://dx.doi.org/10.1038/nrmicro1234.
4. Smith MA, Bidochka MJ. Bacterial fitness and plasmid loss: the importance of culture conditions and plasmid size. Can J Microbiol 1998; 44:351-5; PMID:9674107; http://dx.doi.org/10.1139/w98-020.
5. Meyer R. Replication and conjugative mobilization of broad host-range IncQ plasmids. Plasmid 2009; 62:57-70; PMID:19465049; http://dx.doi.org/10.1016/ j.plasmid.2009.05.001.
6. Dahlberg C, Chao L. Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 2003; 165:1641-9; PMID:14704155.
7. De Gelder L, Ponciano JM, Joyce P, Top EM. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 2007; 153:452-63; PMID:17259616; http://dx.doi.org/10.1099/mic.0. 2006/001784-0.
8. Heuer H, Fox RE, Top EM. Frequent conjugative transfer accelerates adaptation of a broad-host-range plasmid to an unfavorable Pseudomonas putida host. FEMS Microbiol Ecol 2007; 59:738-48; PMID:17059480; http://dx.doi.org/10. 1111/j.1574-6941.2006.00223.x.
9. Humphrey B, Thomson NR, Thomas CM, Brooks K, Sanders M, Delsol AA, et al. Fitness of Escherichia coli strains carrying expressed and partially silent IncN and IncP1 plasmids. BMC Microbiol 2012; 12:53; PMID:22475035; http://dx.doi.org/10.1186/1471-2180-12-53.
10. Godwin D, Slater JH. The influence of the growth environment on the stability of a drug resistance plasmid in Escherichia coli K12. J Gen Microbiol 1979; 111:201-10; PMID:379278; http://dx.doi.org/10.1099/00221287-111-1-201.
11. Paulander W, Maisnier-Patin S, Andersson DI. The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (sigmaS). Genetics 2009; 183:539-46; PMID:19652179; http://dx.doi.org/10.1534/ genetics.109.106104.
12. Petersen A, Aarestrup FM, Olsen JE. The in vitro fitness cost of antimicrobial resistance in Escherichia coli varies with the growth conditions. FEMS Microbiol Lett 2009; 299:53-9; PMID:19694815; http://dx.doi.org/10.1111/j. 1574-6968.2009.01734.x.
13. Bahl MI, Hansen LH, Sørensen SJ. Persistence mechanisms of conjugative plasmids. Methods Mol Biol 2009; 532:73-102; PMID:19271180; http://dx.doi.org/10.1007/978-1-60327-853-9-5.
14. Grissa I, Vergnaud G, Pourcel C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 2007; 8:172; PMID:17521438; http://dx.doi.org/10.1186/1471-2105- 8-172.
15. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011; 9:467-77; PMID:21552286; http://dx.doi.org/10.1038/nrmicro2577.
16. Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu Rev Genet 2012; 46:311-39; PMID:23145983; http://dx.doi.org/10.1146/annurev- genet-110711-155447.
17. Wiedenheft B, Sternberg SH, Doudna JA. RNA-guided genetic silencing systems in bacteria and archaea. Nature 2012; 482:331-8; PMID:22337052; http://dx.doi.org/10.1038/nature10886.
18. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315:1709-12; PMID:17379808; http://dx.doi.org/10.1126/science.1138140.
19. Swarts DC, Mosterd C, van Passel MW, Brouns SJ. CRISPR interference directs strand specific spacer acquisition. PLoS One 2012; 7:e35888; PMID:22558257; http://dx.doi.org/10.1371/journal.pone.0035888.
20. Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 2012; 3:945; PMID:22781758; http://dx.doi.org/10. 1038/ncomms1937.
21. Yosef I, Goren MG, Qimron U. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 2012; 40:5569-76; PMID:22402487; http://dx.doi.org/10.1093/nar/gks216.
22. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, Snijders APL, et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008; 321:960-4; PMID:18703739; http://dx.doi.org/10.1126/science.1159689.
23. Carte J, Wang RY, Li H, Terns RM, Terns MP. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 2008; 22:3489-96; PMID:19141480; http://dx.doi.org/10.1101/gad.1742908.
24. Przybilski R, Richter C, Gristwood T, Clulow JS, Vercoe RB, Fineran PC. Csy4 is responsible for CRISPR RNA processing in Pectobacterium atrosepticum. RNA Biol 2011; 8:517-28; PMID:21519197; http://dx.doi.org/10.4161/rna.8.3.15190.
25. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 2011; 471:602-7; PMID:21455174; http://dx.doi.org/10.1038/nature09886.
26. Hatoum-Aslan A, Maniv I, Marraffini LA. 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 2011; 108:21218-22; PMID:22160698; http://dx.doi.org/10.1073/pnas.1112832108.
27. Hale C, Kleppe K, Terns RM, Terns MP. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 2008; 14:2572-9; PMID:18971321; http://dx.doi.org/10. 1261/rna.1246808.
28. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012; 337:816-21; PMID:22745249; http://dx.doi.org/10.1126/science. 1225829.
29. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER, Waghmare SP, et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol 2011; 18:529-36; PMID:21460843; http://dx.doi.org/10.1038/nsmb. 2019.
30. Westra ER, van Erp PB, Künne T, Wong SP, Staals RH, Seegers CL, et al. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol Cell 2012; 46:595-605; PMID:22521689; http://dx.doi.org/10.1016/j.molcel.2012.03.018.
31. Lintner NG, Kerou M, Brumfield SK, Graham S, Liu H, Naismith JH, et al. Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). J Biol Chem 2011; 286:21643-56; PMID:21507944; http://dx.doi.org/10.1074/jbc.M111.238485.
32. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, Barendregt A, et al. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc Natl Acad Sci USA 2011; 108:10092-7; PMID:21536913; http://dx.doi.org/10.1073/pnas.1102716108.
33. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, et al. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell 2012; 45:292-302; PMID:22227116; http://dx.doi.org/10.1016/j.molcel.2011.10.023.
34. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, et al. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 2009; 139:945-56; PMID:19945378; http://dx.doi.org/10.1016/j.cell.2009.07.040.
35. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, et al. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol Cell 2012; 45:303-13; PMID:22227115; http://dx.doi.org/10.1016/j. molcel.2011.12.013.
36. Horvath P, Romero DA, CoÛté-Monvoisin AC, Richards M, Deveau H, Moineau S, et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 2008; 190:1401-12; PMID:18065539; http://dx.doi.org/10.1128/JB.01415-07.
37. Edgar R, Qimron U. The Escherichia coli CRISPR system protects from ë lysogenization, lysogens, and prophage induction. J Bacteriol 2010; 192:6291-4; PMID:20889749; http://dx.doi.org/10.1128/JB.00644-10.
38. Westra ER, Pul U, Heidrich N, Jore MM, Lundgren M, Stratmann T, et al. H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol Microbiol 2010; 77:1380-93; PMID:20659289; http://dx.doi.org/10.1111/j.1365-2958.2010.07315.x.
39. Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M, Wanner BL, et al. Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol Microbiol 2010; 77:1367-79; PMID:20624226; http://dx.doi.org/10.1111/j.1365-2958.2010.07265.x.
40. Manica A, Zebec Z, Teichmann D, Schleper C. In vivo activity of CRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol Microbiol 2011; 80:481-91; PMID:21385233; http://dx.doi.org/10.1111/j.1365-2958.2011. 07586.x.
41. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 2008; 190:1390-400; PMID:18065545; http://dx.doi.org/10.1128/JB.01412-07.
42. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 2010; 468:67-71; PMID:21048762; http://dx.doi.org/10.1038/ nature09523.
43. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, Wanner B, et al. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci USA 2011; 108:10098-103; PMID:21646539; http://dx.doi.org/10.1073/pnas.1104144108.
44. Perez-Rodriguez R, Haitjema C, Huang Q, Nam KH, Bernardis S, Ke A, et al. Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli. Mol Microbiol 2011; 79:584-99; PMID:21255106; http://dx.doi.org/10.1111/j.1365-2958.2010.07482.x.
45. Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 2008; 322:1843-5; PMID:19095942; http://dx.doi.org/10.1126/science.1165771.
46. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, et al. The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 2012; 85:1057-71; PMID:22834929; http://dx.doi.org/10.1111/j.1365-2958.2012.08172.x.
47. Erdmann S, Garrett RA. Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol Microbiol 2012; 85:1044-56; PMID:22834906; http://dx.doi.org/10.1111/j.1365- 2958.2012.08171.x.
48. Andersson AF, Banfield JF. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 2008; 320:1047-50; PMID:18497291; http://dx.doi.org/10.1126/science.1157358.
49. Tyson GW, Banfield JF. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 2008; 10:200-7; PMID:17894817.
50. Weinberger AD, Sun CL, Pluciñski MM, Denef VJ, Thomas BC, Horvath P, et al. Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput Biol 2012; 8:e1002475; PMID:22532794; http://dx.doi.org/10.1371/journal. pcbi.1002475.
51. Díez-Villaseñor C, Almendros C, García- Martínez J, Mojica FJ. Diversity of CRISPR loci in Escherichia coli. Microbiology 2010; 156:1351-61; PMID:20133361; http://dx.doi.org/10.1099/mic.0. 036046-0.
52. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 2005; 60:174-82; PMID:15791728; http://dx.doi.org/10.1007/s00239-004-0046-3.
53. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 2005; 151:2551-61; PMID:16079334; http://dx.doi.org/10. 1099/mic.0.28048-0.
54. Pourcel C, Salvignol G, Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 2005; 151:653-63; PMID:15758212; http://dx.doi.org/10.1099/mic.0.27437-0.
55. Snyder JC, Bateson MM, Lavin M, Young MJ. Use of cellular CRISPR (clusters of regularly interspaced short palindromic repeats) spacer-based microarrays for detection of viruses in environmental samples. Appl Environ Microbiol 2010; 76:7251-8; PMID:20851987; http://dx.doi.org/10.1128/AEM.01109- 10.
56. Bouma JE, Lenski RE. Evolution of a bacteria/plasmid association. Nature 1988; 335:351-2; PMID:3047585; http://dx.doi.org/10.1038/335351a0.
57. McDermott PJ, Gowland P, Gowland PC. Adaptation of Escherichia coli growth rates to the presence of pBR322. Lett Appl Microbiol 1993; 17:139-43; PMID:7764088; http://dx.doi.org/10.1111/j.1472-765X.1993.tb01443.x.
58. Helling RB, Kinney T, Adams J. The maintenance of Plasmid-containing organisms in populations of Escherichia coli. J Gen Microbiol 1981; 123:129-41; PMID:7033453.
59. De Gelder L, Ponciano JM, Abdo Z, Joyce P, Forney LJ, Top EM. Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution. Genetics 2004; 168:1131-44; PMID:15579675; http://dx.doi.org/10.1534/genetics.104.033431.
60. Enne VI, Bennett PM, Livermore DM, Hall LM. Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother 2004; 53:958-63; PMID:15102746; http://dx.doi.org/10.1093/ jac/dkh217.
61. Yates CM, Shaw DJ, Roe AJ, Woolhouse ME, Amyes SG. Enhancement of bacterial competitive fitness by apramycin resistance plasmids from non-pathogenic Escherichia coli. Biol Lett 2006; 2:463-5; PMID:17148431; http://dx.doi.org/10.1098/rsbl.2006.0478.
62. Kim S, Rahman M, Seol SY, Yoon SS, Kim J. Pseudomonas aeruginosa bacteriophage PA1Ø requires type IV pili for infection and shows broad bactericidal and biofilm removal activities. Appl Environ Microbiol 2012; 78:6380-5; PMID:22752161; http://dx.doi.org/10.1128/AEM.00648-12.
63. Jacobson A. Role of F pili in the penetration of bacteriophage fl. J Virol 1972; 10:835-43; PMID:4563597.
64. Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GP. The phage abortive infection system, ToxIN, functions as a protein-RNA toxinantitoxin pair. Proc Natl Acad Sci USA 2009; 106:894-9; PMID:19124776; http://dx.doi.org/10.1073/pnas.0808832106.
65. Turner SL, Bailey MJ, Lilley AK, Thomas CM. Ecological and molecular maintenance strategies of mobile genetic elements. FEMS Microbiol Ecol 2002; 42:177-85; PMID:19709277; http://dx.doi.org/10.1111/j.1574-6941.2002.tb01007.x.
66. Gerdes K, Møller-Jensen J, Ebersbach G, Kruse T, Nordström K. Bacterial mitotic machineries. Cell 2004; 116:359-66; PMID:15016371; http://dx.doi.org/10.1016/S0092-8674(04)00116-3.
67. Easter CL, Schwab H, Helinski DR. Role of the parCBA operon of the broad-host-range plasmid RK2 in stable plasmid maintenance. J Bacteriol 1998; 180:6023-30; PMID:9811663.
68. Van Melderen L. Molecular interactions of the CcdB poison with its bacterial target, the DNA gyrase. Int J Med Microbiol 2002; 291:537-44; PMID:11890555; http://dx.doi.org/10.1078/1438-4221-00164.
69. Gerdes K, Bech FW, Jørgensen ST, Løbner-Olesen A, Rasmussen PB, Atlung T, et al. Mechanism of postsegregational killing by the hok gene product of the parB system of plasmid R1 and its homology with the relF gene product of the E. coli relB operon. EMBO J 1986; 5:2023-9; PMID:3019679.
70. Yamaguchi Y, Park JH, Inouye M. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 2011; 45:61-79; PMID:22060041; http://dx.doi.org/10. 1146/annurev-genet-110410-132412.
71. Frost LS, Ippen-Ihler K, Skurray RA. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev 1994; 58:162-210; PMID:7915817.
72. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 2003; 224:1-15; PMID:12855161; http://dx.doi.org/10.1016/S0378-1097(03)00430-0.
73. Dürrenberger MB, Villiger W, Bächi T. Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J Struct Biol 1991; 107:146-56; PMID:1807350; http://dx.doi.org/10.1016/1047- 8477(91)90018-R.
74. Llosa M, Zunzunegui S, de la Cruz F. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc Natl Acad Sci USA 2003; 100:10465-70; PMID:12925737; http://dx.doi.org/10.1073/pnas.1830264100.
75. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EP, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev 2010; 74:434-52; PMID:20805406; http://dx.doi.org/10.1128/MMBR.00020-10.
76. de la Cruz F, Frost LS, Meyer RJ, Zechner EL. Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev 2010; 34:18-40; PMID:19919603; http://dx.doi.org/10.1111/j.1574-6976.2009.00195.x.
77. Garcillán-Barcia MP, Francia MV, de la Cruz F. The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 2009; 33:657-87; PMID:19396961; http://dx.doi.org/10.1111/j.1574- 6976.2009.00168.x.
78. Francia MV, Varsaki A, Garcillán-Barcia MP, Latorre A, Drainas C, de la Cruz F. A classification scheme for mobilization regions of bacterial plasmids. FEMS Microbiol Rev 2004; 28:79-100; PMID:14975531; http://dx.doi.org/10.1016/j.femsre.2003.09.001.
79. Lederberg J, Cavalli LL, Lederberg EM. Sex Compatibility in Escherichia Coli. Genetics 1952; 37:720-30; PMID:17247418.
80. Couturier M, Bahassi el-M, Van Melderen L. Bacterial death by DNA gyrase poisoning. Trends Microbiol 1998; 6:269-75; PMID:9717215; http://dx.doi.org/10. 1016/S0966-842X(98)01311-0.
81. Zhong Z, Helinski D, Toukdarian A. Plasmid hostrange: restrictions to F replication in Pseudomonas. Plasmid 2005; 54:48-56; PMID:15907538; http://dx.doi.org/10.1016/j.plasmid.2004.11.001.
82. Mulec J, Starcic M, Zgur-Bertok D. F-like plasmid sequences in enteric bacteria of diverse origin, with implication of horizontal transfer and plasmid host range. Curr Microbiol 2002; 44:231-5; PMID:11910490; http://dx.doi.org/10. 1007/s00284-001-0039-7.
83. Baharoglu Z, Bikard D, Mazel D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet 2010; 6:e1001165; PMID:20975940; http://dx.doi.org/10.1371/journal.pgen.1001165.
84. de Lorenzo V, Herrero M, Jakubzik U, Timmis KN. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 1990; 172:6568-72; PMID:2172217.
85. Kunin V, Sorek R, Hugenholtz P. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 2007; 8:R61; PMID:17442114; http://dx.doi.org/10.1186/gb-2007-8-4-r61.
86. Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, Wagner R. Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol Microbiol 2010; 75:1495-512; PMID:20132443; http://dx.doi.org/10.1111/ j.1365-2958.2010.07073.x.
87. Baranova N, Nikaido H. 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 2002; 184:4168-76; PMID:12107134; http://dx.doi.org/10.1128/JB.184.15. 4168-4176.2002.
88. Barth M, Marschall C, Muffler A, Fischer D, Hengge-Aronis R. Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sigma S and many sigma S-dependent genes in Escherichia coli. J Bacteriol 1995; 177:3455-64; PMID:7768855.
89. Grohmann E, Muth G, Espinosa M. Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 2003; 67:277-301; PMID:12794193; http://dx.doi.org/10.1128/MMBR.67.2.277-301.2003.
90. Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, et al. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 2011; 21:126-36; PMID:21149389; http://dx.doi.org/10.1101/gr.111732.110.
91. Wilmes P, Simmons SL, Denef VJ, Banfield JF. The dynamic genetic repertoire of microbial communities. FEMS Microbiol Rev 2009; 33:109-32; PMID:19054116; http://dx.doi.org/10.1111/j.1574-6976.2008.00144.x.
92. Gudbergsdottir S, Deng L, Chen Z, Jensen JV, Jensen LR, She Q, et al. Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol Microbiol 2011; 79:35-49; PMID:21166892; http://dx.doi.org/10.1111/j.1365-2958. 2010.07452.x.
93. Westra ER, Brouns SJ. The rise and fall of CRISPRs - dynamics of spacer acquisition and loss. Mol Microbiol 2012; 85:1021-5; PMID:22804962; http://dx.doi.org/10.1111/j.1365-2958.2012.08170.x.
94. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 2009; 155:733-40; PMID:19246744; http://dx.doi.org/10.1099/mic.0.023960-0.
95. Fineran PC, Charpentier E. Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 2012; 434:202-9; PMID:23123013; http://dx.doi.org/10.1016/j.virol.2012.10.003.
96. Sinkunas T, Gasiunas G, Waghmare SP, Dickman MJ, Barrangou R, Horvath P, et al. In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J 2013; 32:385-94. PMID:23334296; http://dx.doi.org/10.1038/emboj.2012.352.
97. Westra ER, Nilges B, van Erp PB, van der Oost J, Dame RT, Brouns SJ. Cascade-mediated binding and bending of negatively supercoiled DNA. RNA Biol 2012; 9:1134-8; PMID:22954644; http://dx.doi.org/10.4161/rna.21410.
98. Dame RT, Luijsterburg MS, Krin E, Bertin PN, Wagner R, Wuite GJ. DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 2005; 187:1845-8; PMID:15716456; http://dx.doi.org/10.1128/JB.187.5.1845-1848.2005.
99. Dame RT, Wyman C, Goosen N. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res 2000; 28:3504-10; PMID:10982869; http://dx.doi.org/10.1093/nar/28.18.3504.
100. Owen-Hughes TA, Pavitt GD, Santos DS, Sidebotham JM, Hulton CS, Hinton JC, et al. The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression. Cell 1992; 71:255-65; PMID:1423593; http://dx.doi.org/10.1016/0092-8674(92)90354-F.
101. Tupper AE, Owen-Hughes TA, Ussery DW, Santos DS, Ferguson DJ, Sidebotham JM, et al. The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J 1994; 13:258-68; PMID:8306968.
102. Lund U, Agostinelli C, Agostinelli MC. Package 'circular'. 2011. Gezondheid