Functional analysis of bacteriophage immunity through a Type I-E CRISPR-Cas system in Vibrio cholerae and its application in bacteriophage genome engineering

Journal of Bacteriology

Volumn 198, Issue 3, 2016, Pages 578-590

  Box, Allison M ^a   McGuffie, Matthew J ^a   O'Hara, Brendan J ^a   Seed, Kimberley D ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIOPHAGE; BIOTYPE; CHOLERA; CRISPR CAS SYSTEM; GENE TARGETING; GENETIC ENGINEERING; GENOMIC ISLAND; HOMOLOGOUS RECOMBINATION; MUTANT; NONHUMAN; PLASMID; PRIORITY JOURNAL; VIBRIO CHOLERAE; GENETICS; MUTATION; PHYSIOLOGY; PROCEDURES; VIROLOGY; VIRUS GENOME;

VIRUS DNA;

BACTERIOPHAGES; CRISPR-CAS SYSTEMS; DNA, VIRAL; GENETIC ENGINEERING; GENOME, VIRAL; MUTATION; VIBRIO CHOLERAE;

EID: 84957706239     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00747-15     Document Type: Article

References (53)

1. Kaper JB, Morris JG, Levine MM. 1995. Cholera. Clin Microbiol Rev 8:48-86.
2. Chin C-S, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK. 2011. The origin of the Haitian cholera outbreak strain. N Engl J Med 364:33-42. http://dx.doi.org/10.1056/NEJMoa1012928.
3. Siddique AK, Nair GB, Alam M, Sack DA, Huq A, Nizam A, Longini IM, Jr, Qadri F, Faruque SM, Colwell RR, Ahmed S, Iqbal A, Bhuiyan NA, Sack RB. 2010. El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect 138:347-352. http://dx.doi.org/10.1017/S0950268809990550.
4. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, Croucher NJ, Choi SY, Harris SR, Lebens M, Niyogi SK, Kim EJ, Ramamurthy T, Chun J, Wood JLN, Clemens JD, Czerkinsky C, Nair GB, Holmgren J, Parkhill J, Dougan G. 2011. Evidence for several wavesof global transmission in the seventh cholera pandemic. Nature 477:462-465 http://dx.doi.org/10.1038/nature10392.
5. Cho Y-J, Yi H, Lee JH, Kim DW, Chun J. 2010. Genomic evolution of Vibrio cholerae. Curr Opin Microbiol 13:646-651. http://dx.doi.org/10.1016/j.mib.2010.08.007.
6. Kim EJ, Lee CH, Nair GB, Kim DW. 2015. Whole-genome sequence comparisons reveal the evolution of Vibrio cholerae O1. Trends Microbiol 23:479-489. http://dx.doi.org/10.1016/j.tim.2015.03.010.
7. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY, Haley BJ, Taviani E, Jeon Y-S, Kim DW, Lee J-H, Brettin TS, Bruce DC, Challacombe JF, Detter JC, Han CS, Munk AC, Chertkov O, Meincke L, Saunders E, Walters RA, Huq A, Nair GB, Colwell RR. 2009. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 106:15442-15447. http://dx.doi.org/10.1073/pnas.0907787106.
8. Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor RK, Levine MM. 1988. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J Exp Med168:1487-1492. http://dx.doi.org/10.1084/jem.168.4.1487.
9. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ. 2002. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci U S A 99:1556-1561. http://dx.doi.org/10.1073/pnas.042667999.
10. 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. http://dx.doi.org/10.1126/science.1138140.
11. Barrangou R, Marraffini LA. 2014. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol Cell 54:234-244. http://dx.doi.org/10.1016/j.molcel.2014.03.011.
12. 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. http://dx.doi.org/10.1038/nrmicro3279.
13. Doudna JA, Charpentier E. 2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096. http://dx.doi.org/10.1126/science.1258096.
14. Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, Moineau S, Mojica FJM, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPRCas systems. Nat Rev Microbiol 9:467-477. http://dx.doi.org/10.1038/nrmicro2577.
15. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843-1845 http://dx.doi.org/10.1126/science.1165771.
16. Samai P, Pyenson N, Jiang W, Goldberg GW, Hatoum-Aslan A, Marraffini LA. 2015. Co-transcriptional DNA and RNA cleavage during type III CRISPR-Cas immunity. Cell 161:1164-1174. http://dx.doi.org/10.1016/j.cell.2015.04.027.
17. Deveau H, Barrangou R, Garneau JE, Labonté 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 http://dx.doi.org/10.1128/JB.01412-07.
18. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Almendros C. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733-740. http://dx.doi.org/10.1099/mic.0.023960-0.
19. 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 46:311-339. http://dx.doi.org/10.1146/annurev-genet-110711-155447.
20. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8:172. http://dx.doi.org/10.1186/1471-2105-8-172.
21. Seed KD, Lazinski DW, Calderwood SB, Camilli A. 2013. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489-491. http://dx.doi.org/10.1038/nature11927.
22. Bondy-Denomy J, Davidson AR. 2014. To acquire or resist: the complex biological effects of CRISPR-Cas systems. Trends Microbiol 22:218-225. http://dx.doi.org/10.1016/j.tim.2014.01.007.
23. Pul U, Wurm R, Arslan Z, Geißen R, Hofmann N, Wagner R. 2010. Identification and characterization of E. coli CRISPR-Cas promoters andtheir silencing by H-NS. Mol Microbiol 75:1495-1512. http://dx.doi.org/10.1111/j.1365-2958.2010.07073.x.
24. Ratner HK, Sampson TR, Weiss DS. 2015. I can see CRISPR now, even when phage are gone. Curr Opin Infect Dis 28:267-274. http://dx.doi.org/10.1097/QCO.0000000000000154.
25. Chakraborty S, Waise TMZ, Hassan F, Kabir Y, Smith MA, Arif M. 2009 Assessment of the evolutionary origin and possibility of CRISPRCas (CASS) mediated RNA interference pathway in Vibrio cholerae O395. In Silico Biol 9:245-254.
26. Nelson EJ, Harris JB, Morris JG, Calderwood SB, Camilli A. 2009. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7:693-702. http://dx.doi.org/10.1038/nrmicro2204.
27. Seed KD, Yen M, Shapiro BJ, Hilaire IJ, Charles RC, Teng JE, Ivers LC, Boncy J, Harris JB, Camilli A. 2014. Evolutionary consequences of intra-patient phage predation on microbial populations. eLife 3:e03497. http://dx.doi.org/10.7554/eLife.03497.
28. Kiro R, Shitrit D, Qimron U. 2014. Efficient engineering of a bacteriophage genome using the type I-E CRISPR-Cas system. RNA Biol 11:42-44. http://dx.doi.org/10.4161/rna.27766.
29. Martel B, Moineau S. 2014. CRISPR-Cas: an efficient tool for genome engineering of virulent bacteriophages. Nucleic Acids Res 42:9504-9513. http://dx.doi.org/10.1093/nar/gku628.
30. Lazinski DW, Camilli A. 2013. Homopolymer tail-mediated ligation PCR: a streamlined and highly efficient method for DNA cloning and library construction. Biotechniques 54:25-34. http://dx.doi.org/10.2144/000113981.
31. Crooks GE, Hon G, Chandonia J-M, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14:1188-1190. http://dx.doi.org/10.1101/gr.849004.
32. Donnenberg MS, Kaper JB. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59:4310-4317.
33. Dalia AB, Lazinski DW, Camilli A. 2014. Identification of a membranebound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 5:e01028-13. http://dx.doi.org/10.1128/mBio.01028-13.
34. Dalia AB, McDonough E, Camilli A. 2014. Multiplex genome editing by natural transformation. Proc Natl Acad Sci U S A 111:8937-8942. http://dx.doi.org/10.1073/pnas.1406478111.
35. Furste JP, Pansegrau W, Frank R, Blocker H, Scholz P, Bagdasarian M, Lanka E. 1986. Molecular-cloning of the plasmid Rp4 primase region in a multi-host-range tacP expression vector. Gene 48:119-131. http://dx.doi.org/10.1016/0378-1119(86)90358-6.
36. Jiang W, Cox D, Zhang F, Bikard D, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233-239. http://dx.doi.org/10.1038/nbt.2508.
37. Dalia AB, Seed KD, Calderwood SB, Camilli A. 2015. A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. Proc Natl Acad Sci U S A 112:10485-10490. http://dx.doi.org/10.1073/pnas.1509097112.
38. Lange SJ, Alkhnbashi OS, Rose D, Will S, Backofen R. 2013. CRISPRmap: an automated classification of repeat conservation in prokaryotic adaptive immune systems. Nucleic Acids Res 41:8034-8044. http://dx.doi.org/10.1093/nar/gkt606.
39. Comeau AM, Tremblay D, Moineau S, Rattei T, Kushkina AI, Tovkach FI, Krisch HM, Ackermann H-W. 2012. Phage morphology recapitulates phylogeny: the comparative genomics of a new group of myoviruses. PLoS One 7:e40102. http://dx.doi.org/10.1371/journal.pone.0040102.
40. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJJ, van der Oost J, Doudna JA, Nogales E. 2011. Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477:486-489. http://dx.doi.org/10.1038/nature10402.
41. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER, Waghmare SP, Wiedenheft B, Pul Ü, Wurm R, Wagner R, Beijer MR, Barendregt A, Zhou K, Snijders APL, Dickman MJ, Doudna JA, Boekema EJ, Heck AJR, van der Oost J, Brouns SJJ. 2011. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol 18:529-536. http://dx.doi.org/10.1038/nsmb.2019.
42. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH, Snijders APL, Dickman MJ, Makarova KS, Koonin EV, van der Oost J. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321: 960-964. http://dx.doi.org/10.1126/science.1159689.
43. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, WannerB, van der Oost J, Brouns SJJ, Severinov K. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci U S A 108:10098-10103 http://dx.doi.org/10.1073/pnas.1104144108.
44. Seed KD, Bodi KL, Kropinski AM, Ackermann H-W, Calderwood SB, Qadri F, Camilli A. 2011. Evidence of a dominant lineage of Vibrio cholerae-specific lytic bacteriophages shed by cholera patients over a 10-year period in Dhaka, Bangladesh. mBio 2:e00334-10. http://dx.doi.org/10.1128/mBio.00334-10.
45. Fineran PC, Gerritzen MJH, Suárez-Diez M, Künne T, Boekhorst J, van Hijum SAFT, Staals RHJ, Brouns SJJ. 2014. Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci U S A 111: E1629-E1638. http://dx.doi.org/10.1073/pnas.1400071111.
46. Blokesch M, Schoolnik GK. 2007. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog 3:e81. http://dx.doi.org/10.1371/journal.ppat.0030081.
47. Devault AM, Golding GB, Waglechner N, Enk JM, Kuch M, Tien JH, Shi M, Fisman DN, Dhody AN, Forrest S, Bos KI, Earn DJD, Holmes EC, Poinar HN. 2014. Second-pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. N Engl J Med 370:334-340. http://dx.doi.org/10.1056/NEJMoa1308663.
48. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-Cas. mBio 1:e00227-10. http://dx.doi.org/10.1128/mBio.00227-10.
49. Marraffini LA. 2013. CRISPR-Cas immunity against phages: its effects on the evolution and survival of bacterial pathogens. PLoS Pathog 9:e1003765. http://dx.doi.org/10.1371/journal.ppat.1003765.
50. Waldor MK, Mekalanos JJ. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910-1914. http://dx.doi.org/10.1126/science.272.5270.1910.
51. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci U S A 84:2833-2837. http://dx.doi.org/10.1073/pnas.84.9.2833.
52. Levine MM, Black RE, Clements ML, Cisneros L, Saah A, Nalin DR, Gill DM, Craig JP, Young CR, Ristaino P. 1982. The pathogenicity of nonenterotoxigenic Vibrio cholerae serogroup O1 biotype El Tor isolated from sewage water in Brazil. J Infect Dis 145:296-299. http://dx.doi.org/10.1093/infdis/145.3.296.
53. Ogg JE, Timme TL, Alemohammad MM. 1981. General transduction in Vibrio cholerae. Infect Immun 31:737-741.