CRISPR-mediated phage resistance and the ghost of coevolution past

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1691, 2010, Pages 2097-2103

  Vale, Pedro F ^a,b   Little, Tom J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Bacteria; Coevolution; Epidemiology; Evolution; Phage; Resistance

Indexed keywords

BACTERIOPHAGE; BACTERIUM; COEVOLUTION; DISEASE RESISTANCE; EPIDEMIOLOGY; EXPERIMENTAL STUDY; GENETIC MARKER; HERITABILITY; HOST-PATHOGEN INTERACTION; IMMUNITY; MICROBIAL COMMUNITY;

EID: 77955342938     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0055     Document Type: Review

References (79)

1. Abedon, S. T. 2008 Bacteriophage ecology: population growth, evolution, and impact of bacterial viruses. Cambridge, UK: Cambridge University Press.
2. Agrawal, A. & Lively, C. M. 2002 Infection genetics: genefor-gene versus matching-alleles models and all points in between. Evol. Ecol Res. 4, 79-90. (Pubitemid 135693221)
3. Andersson, A. F. & Banfield, J. F. 2008 Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047-1050. (doi:10.1126/science.1157358)
4. Anderson, R. M. & May, R. M. 1982 Coevolution of hosts and parasites. Parasitology 85, 411-426. (doi:10.1017/ S0031182000055360)
5. Antonovics, J. & Thrall, P. H. 1994 The cost of resistance and maintenance of genetic polymorphism in host-pathogen systems. Proc. R. Soc. Lond. B 257, 105-110. (doi:10. 1098/rspb.1994.0101)
6. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A. & Horvath, P. 2007 CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712. (doi:10. 1126/science.1138140) (Pubitemid 46515624)
7. Barrett, R. & Schluter, D. 2008 Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44. (doi:10. 1016/j.tree.2007.09.008)
8. Best, A., White, A. & Boots, M. 2009 The implications of coevolutionary dynamics to host-parasite interactions. Am. Nat. 173, 779-791. (doi:10.1086/598494)
9. Bland, C., Ramsey, T. L., Sabree, F., Lowe, M., Brown, K., Kyrpides, N. C. & Hugenholtz, P. 2007 CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8, 209. (doi:10.1186/1471-2105-8-209) (Pubitemid 47090614)
10. Brockhurst, M., Morgan, A., Rainey, P. & Buckling, A. 2003 Population mixing accelerates coevolution. Ecol. Lett. 6, 975-979. (doi:10.1046/j.1461- 0248.2003.00531.x)
11. Brouns, S. J. et al 2008 Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960-964. (doi:10. 1126/science. 1159689)
12. Buckling, A. & Rainey, P. B. 2002a The role of parasites in sympatric and allopatric host diversification. Nature 420, 496-499. (doi:10.1038/ nature01164) (Pubitemid 35477039)
13. Buckling, A. & Rainey, P. B. 20026 Antagonistic coevolution between a bacterium and a bacteriophage. Proc. Biol. Sci. 269, 931-936. (doi:10.1098/rspb.2001.1945)
14. Buckling, A., Craig Maclean, R., Brockhurst, M. A. & Colegrave, N. 2009 The Beagle in a bottle. Nature 457, 824-829. (doi:10.1038/nature07892)
15. Bustamante, C. D. et al. 2005 Natural selection on proteincoding genes in the human genome. Nature 437, 11531157. (doi:10.1038/nature04240)
16. Bzymek, M. & Lovett, S. T. 2001 Instability of repetitive DNA sequences: The role of replication in multiple mechanisms. Proc. Nad Acad. Sci. USA 98, 8319-8325. (doi:10.1073/pnas.111008398) (Pubitemid 32678030)
17. Colegrave, N. 2002 Sex releases the speed limit on evolution. Nature 420, 664-666. (doi:10.1038/nature01191) (Pubitemid 36764496)
18. Cooper, T. F. 2007 Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biol. 5, e225. (doi:10.1371/journal.pbio.0050225)
19. Decaestecker, E., Gaba, S., Raeymaekers, J. A., Stoks, R, Van Kerckhoven, L., Ebert, D. & De Meester, L. 2007 Hostparasite 'Red Queen' dynamics archived in pond sediment. Nature 450, 870-873. (doi:10.1038/nature06291)
20. Deveau, H., Barrangou, R., Garneau, J. E., Labonte, J., Fremaux, C., Boyaval, P., Romero, D. A., Horvath, P. & Moineau, S. 2008 Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190, 1390-1400. (doi:10.1128/JB.01412-07)
21. Ding, S. W., Li, H., Lu, R., Li, F. & Li, W. X. 2004 RNA silencing: a conserved antiviral immunity of plants and animals. Virus Res. 102, 109-115. (doi:10.1016/j. virusres.2004.01.021) (Pubitemid 38450743)
22. Dlugosch, K. M. & Parker, I. M. 2008 Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431-449. (doi:10.1111/j.1365-294X.2007.03538.x)
23. Drake, J. W., Charlesworth, B., Charlesworth, D. & Crow, J. F. 1998 Rates of spontaneous mutation. Genetics 148, 1667-1686.
24. Edgar, R. C. 2007 PILER-CR: fast and accurate identification of CRISPR repeats. BMC Bioinformatics 8, 18. (doi:10.1186/1471-2105-8-18)
25. Faulkner, W. 1951 Requiem for a nun. New York, NY: Random House.
26. Ferenci, T., Brass, J. & Boos, W. 1980 The role of the periplasms maltose-binding protein and the outer-membrane phage lambda receptor in maltodextrin transport of Escherichia coli. Biochem. Soc. Trans. 8, 680-681.
27. Fisher, R. A. 1930 The genetical theory of natural selection. Oxford, UK: Clarendon Press.
28. Gaba, S. & Ebert, D. 2009 Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol. 24, 226-232. (doi:10.1016/j.tree. 2008.11.005)
29. Gandon, S. & Day, T. 2009 Evolutionary epidemiology and the dynamics of adaptation. Evolution 63, 826-838. (doi: 10.1111/j. 1558-5646.2009.00609.x)
30. Gandon, S., Buckling, A., Decaestecker, E. & Day, T. 2008 Host-parasite coevolution and patterns of adaptation across time and space. J. Evol. Biol. 21, 1861-1866. (doi:10.1111/j.1420-9101.2008.01598.x)
31. Greischar, M. A. & Koskella, B. 2007 A synthesis of experimental work on parasite local adaptation. Ecol. Lett. 10, 418-434. (doi:10.1111/j.1461- 0248.2007.01028.x) (Pubitemid 46718944)
32. Grissa, I., Vergnaud, G. & Pourcel, C. 2007 CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35, W52-W57. (doi:10.1093/nar/gkm360)
33. Grissa, I., Vergnaud, G. & Pourcel, C. 2008a CRISPRcompar: a website to compare clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 36, WHSWHS. (doi:10.1093/nar/gkn228)
34. Grissa, I., Bouchon, P., Pourcel, C. & Vergnaud, G. 2008b On-line resources for bacterial micro-evolution studies using MLVA or CRISPR typing. Biochimie 90, 660-668. (doi:10.1016/j.biochi.2007.07.014)
35. Haft, D. H., Selengut, J., Mongodin, E. F. & Nelson, K. E. 2005 A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 1, e60. (doi: 10. 137 1/joumal.pcbi.0010060)
36. Hamilton, W. D. 1993 Haploid dynamic polymorphism in a host with matching parasites: effects of mutation subdivision, linkage, and patterns of selection. Heredity 84, 328-338.
37. Heidelberg, J. F., Nelson, W. C., Schoenfeld, T. & Bhaya, D. 2009 Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4, e4169. (doi:10.1371/ journal.pone.0004169)
38. Held, N. L. & Whitaker, R. J. 2009 Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ. Microbiol. 11, 457-466. (doi:10.1111/j.l4622920.2008.01784.x)
39. Hermisson, J. & Pennings, P. S. 2005 Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335-2352. (doi:10.1534/genetics. 104.036947) (Pubitemid 40695640)
40. Horvath, P. & Barrangou, R. 2010 CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167-170. (doi:10.1126/science.1179555)
41. Hugenholtz, P. & Tyson, G. W. 2008 Microbiology: metagenomics. Nature 455, 481-483. (doi:10.1038/ 455481a)
42. 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. Bacteri0l. 169, 5429-5433. (Pubitemid 18017837)
43. Jansen, R., van Embden, J. D., Gaastra, W. & Schouls, L. M. 2002 Identification of a novel family of sequence repeats among prokaryotes. Omics 6, 23-33. (doi: 10.1089/ 15362310252780816) (Pubitemid 34595547)
44. Jessup, C. M., Kassen, R., Forde, S. E., Kerr, B., Buckling, A., Rainey, P. B. & Bohannan, B. J. 2004 Big questions, small worlds: microbial model systems in ecology. Trends Ecol. Evol. 19, 189-197. (doi:10.1016/j.tree.2004.01. 008) (Pubitemid 38355798)
45. Kraaijeveld, A. R. & Godfray, H. C. 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278-280. (doi:10. 1038/38483)
46. Kunin, V. et al. 2008 A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res. 18, 293-297. (doi:10.1101/gr.6835308) (Pubitemid 351240739)
47. Laine, A. L. 2007 Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach. J. Evol. Biol. 20, 1665-1673. (doi:10.1111/j.1420-9101.2007.01359.x)
48. Laine, A. L. & Tellier, A. 2008 Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117, 1281-1288. (doi:10.1111j.00301299.2008.16563.x)
49. Lennon, J. T., Khatana, S. A., Marston, M. F. & Martiny, J. B. 2007 Is there a cost of virus resistance in marine cyanobacteria? Isme J. 1, 300-312.
50. Lillestol, R. K., Shah, S. A., Brugger, K., Redder, P., Phan, H., Christiansen, J. & Garrett, R. A. 2009 CRISPR families of the crenarchaeal genus Sulfolobus: bidirectional transcription and dynamic properties. Mol. Microbiol. 72, 259-272. (doi:10.1111/j.1365-2958.2009.06641.x)
51. Lopez-Pascua, L. C. & Buckling, A. 2008 Increasing productivity accelerates host-parasite coevolution. J. Evol. Biol. 21, 853-860. (doi:10.1111/j.1420-9101.2008. 01501.x) (Pubitemid 351521529)
52. Makarova, K. S., Grishin, N. V, Shabalina, S. A., Wolf, Y I. & Koonin, E. V. 2006 A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1, 7. (doi: 10.1186/ 1745-6150-1-7)
53. Mardis, E. R. 2008 Next-generation DNA sequencing methods. Annu. Rev. Genomics Hum. Genet. 9, 387402. (doi:10.1146/annurev.genom.9.081307.164359)
54. Marrafnni, L. A. & Sontheimer, E. J. 2008 CRISPR interference limits horizontal gene transfer in Staphylococci by targeting DNA. Science 322, 1843-1845. (doi:10.1126/ science. 1165771)
55. Marrafnni, L. A. & Sontheimer, E. J. 2010a CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11, 181-190. (doi: 10.1038/ nrg2749)
56. Marraffini, L. A. & Sontheimer, E. J. 2010b Self versus non-self discrimination during CRISPR RNAdirected immunity. Nature 463, 568-571. (doi:10.1038/ nature08703)
57. May, R. M., Gupta, S. & McLean, A. R. 2001 Infectious disease dynamics: what characterizes a successful invader? Phil. Trans. R. Soc. Lond. B 356, 901-910. (doi:10. 1098/rstb.2001.0866) (Pubitemid 32614665)
58. Mealor, M. A. & Boots, M. 2006 An indirect approach to imply trade-off shapes: population level patterns in resistance suggest a decreasingly costly resistance mechanism in a model insect system. J. Evol. Biol. 19, 326-330. (doi:10.1111/j.1420-9101.2005.01031.x)
59. Miralles, R., Gerrish, P. J., Moya, A. & Elena, S. F. 1999 Clonal interference and the evolution of RNA viruses. Science 285, 1745-1747. (doi:10.1126/science.285.5434. 1745) (Pubitemid 29428876)
60. Mojica, F. J., 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. (doi:10.1099/mic.0. 023960-0)
61. Morgan, A., Gandon, S. & Budding, A. 2005 The effect of migration on local adaptation in a coevolving hostparasite system. Nature 437, 253-256. (doi:10.1038/ nature03913) (Pubitemid 41294487)
62. Morgan, A. D., Brockhurst, M. A., Lopez-Pascua, L. D., Pal, C. & Buckling, A. 2007 Differential impact of simultaneous migration on coevolving hosts and parasites. BMC Evol. Biol. 7, 1. (doi:10.1186/1471-2148-7-1) Nielsen, R. 2005 Molecular signatures of natural selection. Annu. Rev. Genet. 39, 197-218. (doi:10.1146/annurev. genet.39.073003.112420) (Pubitemid 46169607)
63. Nuismer, S. L. & Gandon, S. 2008 Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am. Nat. 171, 658-668. (doi: 10.1086/587077) (Pubitemid 351589848)
64. Nuismer, S. L. & Otto, S. P. 2005 Host-parasite interactions and the evolution of gene expression. PLoS Biol. 3, e203. (doi:10.1371/joumal.pbio. 0030203)
65. Obbard, D. J., Gordon, K. H., Buck, A. H. & Jiggins, F. M. 2009 The evolution of RNAi as a defence against viruses and transposable elements. Phil. Trans. R. Soc. B 364, 99-115. (doi:10.1098/rstb.2008.0168)
66. Pease, C. M. & Bull, J. J. 1988 A critique of methods for measuring life-history trade-offs. J. Evol. Biol. 1, 293-303. (doi:10.1046/j.l420-9101. 1988.1040293.x)
67. Pepin, K. M. & Wichman, H. A. 2008 Experimental evolution and genome sequencing reveal variation in levels of clonal interference in large populations of bacteriophage phiX174. BMC Evol. Biol. 8, 85. (doi:10.1186/ 1471-2148-8-85)
68. Price, G. R. 1972 Fisher's 'fundamental theorem' made clear. Ann. Hum. Genet. 36, 129-140. (doi:10.1111/j. 1469-1809.1972.tb00764.x)
69. Schreiber, S. J. & Lloyd-Smith, J. O. 2009 Invasion dynamics in spatially heterogeneous environments. Am. Nat. 174, 490-505. (doi:10.1086/605405)
70. Sheldon, B. C. & Verhulst, S. 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi:10.1016/ 0169-5347(96)10039-2) (Pubitemid 27003142)
71. Sorek, R, Kunin, V & Hugenholtz, P. 2008 CRISPR- a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat. Rev. Microbiol. 6, 181-186. (doi:10.1038/nrmicrol793) (Pubitemid 351256313)
72. Sturino, J. M. & Klaenhammer, T. R. 2006 Engineered bacteriophage-defence systems in bioprocessing. Nat. Rev. Microbiol. 4, 395-404. (doi:10.1038/nrmicrol393)
73. Suttle, C. A. 2005 Viruses in the sea. Nature 437, 356-361. (doi: 10.1038/nature04160)
74. Tyson, G. W. & Banfield, J. F. 2008 Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10, 200-207.
75. van der Oost, J., Jore, M. M., Westra, E. R., Lundgren, M. & Brouns, S. J. 2009 CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34, 401-407. (doi:10.1016/j.tibs.2009.05.002)
76. Vos, M., Birkett, P. J., Birch, E., Griffiths, R. I. & Buckling, A. 2009 Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325, 833. (doi: 10.1126/ science. 1174173)
77. Wiedenheft, B., Zhou, K., Jinek, M., Coyle, S. M., Ma, W. & Doudna, J. A. 2009 Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17, 904-912. (doi:10.1016/j. str.2009.03.019)
78. Woolhouse, M. E., Webster, J. P., Domingo, E., Charlesworth, B. & Levin, B. R. 2002 Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32, 569-577. (doi:10.1038/ ngl202-569) (Pubitemid 35435167)
79. Yoshida, M., Yoshida, T., Kashima, A., Takashima, Y., Hosoda, N., Nagasaki, K. & Hiroishi, S. 2008 Ecological dynamics of the toxic bloom-forming cyanobacterium Microcystis aeruginosa and its cyanophages in freshwater. Appl. Environ. Microbiol. 74, 3269-3273. (doi:10.1128/ AEM.02240-07) (Pubitemid 351747034)