Spacer Acquisition Rates Determine the Immunological Diversity of the Type II CRISPR-Cas Immune Response

Cell Host and Microbe

Volumn 25, Issue 2, 2019, Pages 242-249.e3

  Heler, Robert ^a   Wright, Addison V ^b   Vucelja, Marija ^c   Doudna, Jennifer A ^b,d   Marraffini, Luciano A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Virginia   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

bacteriophage; Cas9; CRISPR; immunity; spacer acquisition; staphylococcus

Indexed keywords

RIBOSOMAL SPACER DNA; SPACER DNA; VIRUS DNA;

ARTICLE; BACTERIAL GENOME; BACTERIOPHAGE; CRISPR CAS SYSTEM; IMMUNE RESPONSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR EVOLUTION; STAPHYLOCOCCUS PHAGE;

CRISPR-CAS SYSTEMS; DNA, INTERGENIC; DNA, VIRAL; EVOLUTION, MOLECULAR; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES; STREPTOCOCCUS PYOGENES;

EID: 85060844813     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2018.12.016     Document Type: Article

References (25)

1. Anders, C., Niewoehner, O., Duerst, A., Jinek, M., Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513 (2014), 569–573.
2. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., Horvath, P., CRISPR provides acquired resistance against viruses in prokaryotes. Science 315 (2007), 1709–1712.
3. Bradde, S., Vucelja, M., Teşileanu, T., Balasubramanian, V., Dynamics of adaptive immunity against phage in bacterial populations. PLoS Comput. Biol., 13, 2017, e1005486.
4. Brouns, S.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhuis, R.J., Snijders, A.P., Dickman, M.J., Makarova, K.S., Koonin, E.V., van der Oost, J., Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321 (2008), 960–964.
5. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E., CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471 (2011), 602–607.
6. Deveau, H., Barrangou, R., Garneau, J.E., Labonté J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P., Moineau, S., Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190 (2008), 1390–1400.
7. Garneau, J.E., Dupuis, M.È., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A.H., Moineau, S., The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468 (2010), 67–71.
8. Goldberg, G.W., Jiang, W., Bikard, D., Marraffini, L.A., Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514 (2014), 633–637.
9. Heler, R., Samai, P., Modell, J.W., Weiner, C., Goldberg, G.W., Bikard, D., Marraffini, L.A., Cas9 specifies functinal viral targets during CRISPR-Cas adaptation. Nature 519 (2015), 199–202.
10. Heler, R., Wright, A.V., Vucelja, M., Bikard, D., Doudna, J.A., Marraffini, L.A., Mutations in Cas9 enhance the rate of acquisition of viral spacer sequences during the CRISPR-Cas immune response. Mol. Cell 65 (2017), 168–175.
11. Jiang, W., Bikard, D., Cox, D., Zhang, F., Marraffini, L.A., RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31 (2013), 233–239.
12. Jiang, F., Taylor, D.W., Chen, J.S., Kornfeld, J.E., Zhou, K., Thompson, A.J., Nogales, E., Doudna, J.A., Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science 351 (2016), 867–871.
13. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
14. Kreiswirth, B.N., Löfdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., Novick, R.P., The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305 (1983), 709–712.
15. Kwan, T., Liu, J., DuBow, M., Gros, P., Pelletier, J., The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl. Acad. Sci. U S A 102 (2005), 5174–5179.
16. Levy, A., Goren, M.G., Yosef, I., Auster, O., Manor, M., Amitai, G., Edgar, R., Qimron, U., Sorek, R., CRISPR adaptation biases explain preference for acquisition of foreign DNA. Nature 520 (2015), 505–510.
17. Marraffini, L.A., Sontheimer, E.J., CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322 (2008), 1843–1845.
18. McGinn, J., Marraffini, L.A., CRISPR-Cas systems optimize their immune response by specifying the site of spacer integration. Mol. Cell 64 (2016), 616–623.
19. Modell, J.W., Jiang, W., Marraffini, L.A., CRISPR-Cas systems exploit viral DNA injection to establish and maintain adaptive immunity. Nature 544 (2017), 101–104.
20. Paez-Espino, D., Morovic, W., Sun, C.L., Thomas, B.C., Ueda, K., Stahl, B., Barrangou, R., Banfield, J.F., Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat. Commun., 4, 2013, 1430.
21. Paez-Espino, D., Sharon, I., Morovic, W., Stahl, B., Thomas, B.C., Barrangou, R., Banfield, J.F., CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. MBio, 6, 2015 e00262–15.
22. Shipman, S.L., Nivala, J., Macklis, J.D., Church, G.M., CRISPR-Cas encoding of a digital movie into the genomes of a population of living bacteria. Nature 547 (2017), 345–349.
23. Wright, A.V., Doudna, J.A., Protecting genome integrity during CRISPR immune adaptation. Nat. Struct. Mol. Biol. 23 (2016), 876–883.
24. Wu, X., Bartel, D.P., kpLogo: positional k-mer analysis reveals hidden specificity in biological sequences. Nucleic Acids Res. 45 (2017), W534–W538.
25. Yosef, I., Shitrit, D., Goren, M.G., Burstein, D., Pupko, T., Qimron, U., DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc. Natl. Acad. Sci. U S A 110 (2013), 14396–14401.