Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context

Journal of Bacteriology

Volumn 195, Issue 17, 2013, Pages 3834-3844

  Iranzo, Jaime ^a   Lobkovsky, Alexander E ^b   Wolf, Yuri I ^b   Koonin, Eugene V ^b  

^a CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN;

ADAPTIVE IMMUNITY; ARTICLE; AUTOIMMUNITY; BACTERIAL IMMUNITY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HYPERTHERMOPHILE; MATHEMATICAL MODEL; MESOPHILE; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; PROKARYOTE; PROTEIN MOTIF; SHORT INTERSPERSED REPEAT; VIRUS GENOME;

ADAPTATION, BIOLOGICAL; ARCHAEA; BACTERIA; EVOLUTION, MOLECULAR; MODELS, THEORETICAL;

EID: 84883510431     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00412-13     Document Type: Article

References (88)

1. Stern A, Sorek R. 2011. The phage-host arms race: shaping the evolution of microbes. Bioessays 33:43-51.
2. Koonin EV, Wolf YI. 2012. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front. Cell Infect. Microbiol. 2:119.
3. Forterre P, Prangishvili D. 2009. The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann. N. Y. Acad. Sci. 1178:65-77.
4. Haaber J, Samson JE, Labrie SJ, Campanacci V, Cambillau C, Moineau S, Hammer K. 2010. Lactococcal abortive infection protein AbiV interacts directly with the phage protein SaV and prevents translation of phage proteins. Appl. Environ. Microbiol. 76:7085-7092.
5. Makarova KS, Wolf YI, Snir S, Koonin EV. 2011. Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J. Bacteriol. 193:6039-6056.
6. Makarova KS, Wolf YI, Koonin EV. 2013. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 41:4360-4377.
7. Blower TR, Salmond GP, Luisi BF. 2011. Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr. Opin. Struct. Biol. 21:109-118.
8. Blower TR, Evans TJ, Przybilski R, Fineran PC, Salmond GP. 2012. Viral evasion of a bacterial suicide system by RNA-based molecular mimicry enables infectious altruism. PLoS Genet. 8:e1003023. doi:10.1371/journal.pgen.1003023.
9. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, Van Melderen L. 2011. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res. 39:5513-5525.
10. Vasu K, Nagaraja V. 2013. Diverse functions of restrictionmodification systems in addition to cellular defense. Microbiol. Mol. Biol. Rev. 77:53-72.
11. Koonin EV, Makarova KS. 2013. CRISPR-Cas: evolution of an RNAbased adaptive immunity system in prokaryotes. RNA Biol. 10:679-686.
12. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273-297.
13. Deveau H, Garneau JE, Moineau S. 2010. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 64:475-493.
14. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181-190.
15. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331-338.
16. Haft DH, Selengut J, Mongodin EF, Nelson KE. 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:10.1371/journal.pcbi.0010060.
17. 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.
18. Koonin EV, Makarova KS. 2009. CRISPR-Cas: an adaptive immunity system in prokaryotes. F1000 Biol. Rep. 1:95.
19. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 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.
20. 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.
21. Goren M, Yosef I, Edgar R, Qimron U. 2012. The bacterial CRISPR/Cas system as analog of the mammalian adaptive immune system. RNA Biol. 9:549-554.
22. Koonin EV, Wolf YI. 2009. Is evolution Darwinian and/or Lamarckian? Biol. Direct 4:42.
23. 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.
24. Fabre L, Zhang J, Guigon G, Le Hello S, Guibert V, Accou-Demartin M, de Romans S, Lim C, Roux C, Passet V, Diancourt L, Guibourdenche M, Issenhuth-Jeanjean S, Achtman M, Brisse S, Sola C, Weill FX. 2012. CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PLoS One 7:e36995. doi:10.1371/journal.pone.0036995.
25. 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.
26. Carroll D. 2012. A CRISPR approach to gene targeting. Mol. Ther. 20:1658-1660.
27. Qi L, Haurwitz RE, Shao W, Doudna JA, Arkin AP. 2012. RNA processing enables predictable programming of gene expression. Nat. Biotechnol. 30:1002-1006.
28. Mali P, Yang L, Esvelt KM, Aach J, Guell M, Dicarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826.
29. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering Using CRISPR/Cas systems. Science 339:819-823.
30. Cain AK, Boinett CJ. 2013. A CRISPR view of genome sequences. Nat. Rev. Microbiol. 11:226.
31. Makarova KS, Aravind L, Wolf YI, Koonin EV. 2011. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6:38.
32. 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.
33. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ. 2009. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34:401-407.
34. 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.
35. Andersson AF, Banfield JF. 2008. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047-1050.
36. 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. U. S. A. 108:10098-10103.
37. Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D. 2009. Germ warfare in a microbial mat community: CRISPRs provide insights into the coevolution of host and viral genomes. PLoS One 4:e4169. doi:10.1371/journal.pone.0004169.
38. Horvath P, Romero DA, Coute-Monvoisin AC, Richards M, Deveau H, Moineau S, Boyaval P, Fremaux C, Barrangou R. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:1401-1412.
39. 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.
40. Weinberger AD, Wolf YI, Lobkovsky AE, Gilmore MS, Koonin EV. 2012. Viral diversity threshold for adaptive immunity in prokaryotes. mBio 3:e00456-12. doi:10.1128/mBio.00456-12.
41. Jorth P, Whiteley M. 2012. An evolutionary link between natural transformation and CRISPR adaptive immunity. mBio 3:e00309. doi:10.1128/mBio.00309-12.
42. Pleckaityte M, Zilnyte M, Zvirbliene A. 2012. Insights into the CRISPR/ Cas system of Gardnerella vaginalis. BMC Microbiol. 12:301. doi:10.1128/mBio.00309-12.
43. Horvath P, Coute-Monvoisin AC, Romero DA, Boyaval P, Fremaux C, Barrangou R. 2009. Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int. J. Food Microbiol. 131:62-70.
44. Chakraborty S, Snijders AP, Chakravorty R, Ahmed M, Tarek AM, Hossain MA. 2010. Comparative network clustering of direct repeats (DRs) and cas genes confirms the possibility of the horizontal transfer of CRISPR locus among bacteria. Mol. Phylogenet. Evol. 56:878-887.
45. Weinberger AD, Gilmore MS. 2012. CRISPR-Cas: to take up DNA or not-that is the question. Cell Host Microbe 12:125-126.
46. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-Cas. mBio 1:e00227. doi:10.1128/mBio.00227-10.
47. 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.
48. 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.
49. Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J. 2012. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311-339.
50. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. 2010. Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet. 26:335-340.
51. Paez-Espino D, Morovic W, Sun CL, Thomas BC, Ueda K, Stahl B, Barrangou R, Banfield JF. 2013. Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat. Commun. 4:14-30.
52. Han P, Niestemski LR, Barrick JE, Deem MW. 2013. Physical model of the immune response of bacteria against bacteriophage through the adaptive CRISPR-Cas immune system. Phys Biol. 10:025004.
53. Kupczok A, Bollback JP. 2013. Probabilistic models for CRISPR spacer content evolution. BMC Evol. Biol. 13:54. doi:10.1186/1471-2148-13-54.
54. He J, Deem MW. 2010. Heterogeneous diversity of spacers within CRISPR (clustered regularly interspaced short palindromic repeats). Phys. Rev. Lett. 105:128102.
55. Childs LM, Held NL, Young MJ, Whitaker RJ, Weitz JS. 2012. Multiscale model of CRISPR-induced coevolutionary dynamics: diversification at the interface of Lamarck and Darwin. Evolution 66:2015-2029.
56. Haerter JO, Sneppen K. 2012. Spatial structure and Lamarckian adaptation explain extreme genetic diversity at CRISPR locus. mBio 3:e00126-12. doi:10.1128/mBio.00126-12.
57. Haerter JO, Trusina A, Sneppen K. 2011. Targeted bacterial immunity buffers phage diversity. J. Virol. 85:10554-10560.
58. Levin BR. 2010. Nasty viruses, costly plasmids, population dynamics, and the conditions for establishing and maintaining CRISPR-mediated adaptive immunity in bacteria. PLoS Genet. 6:e1001171. doi:10.1371/journal.pgen.1001171.
59. Levin BR, Moineau S, Bushman M, Barrangou R. 2013. The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLoS Genet. 9:e1003312. doi:10.1371/journal.pgen.1003312.
60. Weinberger AD, Sun CL, Pluciński MM, Denef VJ, Thomas BC, Horvath P, Barrangou R, Gilmore MS, Getz WM, Banfield JF. 2012. Persisting low-abundance viral sequences shape microbial CRISPR-based immunity. PLoS Comput. Biol. 8:e1002475. doi:10.1371/journal.pcbi.1002475.
61. Hofbauer J, Sigmund K. 1998. Evolutionary games and population dynamics. Cambridge University Press, Cambridge, United Kingdom.
62. Grimm V, Railsback SF. 2005. Individual-based modeling and ecology. Princeton University Press, Princeton, NJ.
63. May RM. 2001. Stability and complexity in model ecosystems. Princeton University Press, Princeton, NJ.
64. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81:2340-2361.
65. Breitbart M, Rohwer F. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13:278-284.
66. Suttle CA. 2007. Marine viruses: major players in the global ecosystem. Nat. Rev. Microbiol. 5:801-812.
67. Rohwer F, Truber RV. 2009. Viruses manipulate the marine environment. Nature 459:207-212.
68. Donalson DD, Nisbet RM. 1999. Population dynamics and spatial scale: effects of system size on population persistence. Ecology 80:2492-2507.
69. Zeldovich KB, Berezovsky IN, Shakhnovich EI. 2007. Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput. Biol. 3:e5. doi:10.1371/journal.pcbi.0030005.
70. Drake JW. 2009. Avoiding dangerous missense: thermophiles display especially low mutation rates. PLoS Genet. 5:e1000520. doi:10.1371/journal.pgen.1000520.
71. Fuhrman JA. 2002. Community structure and function in prokaryotic marine plankton. Antonie Van Leeuwenhoek 81:521-527.
72. Schrenk MO, Kelley DS, Delaney JR, Baross JA. 2003. Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl. Environ. Microbiol. 69:3580-3592.
73. Whitaker RJ, Banfield JF. 2006. Population genomics in natural microbial communities. Trends Ecol. Evol. 21:508-516.
74. Wilmes P, Simmons SL, Denef VJ, Banfield JF. 2009. The dynamic genetic repertoire of microbial communities. FEMS Microbiol. Rev. 33:109-132.
75. Hoaki T, Nishijima M, Miyashita H, Maruyama T. 1995. Dense community of hyperthermophilic sulfur-dependent heterotrophs in a geothermally heated shallow submarine biotope near Kodakara-Jima Island, Kagoshima, Japan. Appl. Environ. Microbiol. 61:1931-1937.
76. Takai K, Komatsu T, Inagaki F, Horikoshi K. 2001. Distribution of archaea in a black smoker chimney structure. Appl. Environ. Microbiol. 67:3618-3629.
77. Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J, Kataoka S, Hirayama H, Nunoura T, Horikoshi K, Sako Y. 2005. Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol. Ecol. 54:141-155.
78. Zhou H, Li J, Peng X, Meng J, Wang F, Ai Y. 2009. Microbial diversity of a sulfide black smoker in main endeavour hydrothermal vent field, Juan de Fuca Ridge. J. Microbiol. 47:235-247.
79. Flores GE, Wagner ID, Liu Y, Reysenbach AL. 2012. Distribution, abundance, and diversity patterns of the thermoacidophilic "deep-sea hydrothermal vent euryarchaeota 2". Front. Microbiol. 3:47.
80. Llobet-Brossa E, Rossello-Mora R, Amann R. 1998. Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl. Environ. Microbiol. 64:2691-2696.
81. Sahm K, MacGregor BJ, Jorgensen BB, Stahl DA. 1999. Sulphate reduction and vertical distribution of sulphate-reducing bacteria quantified by rRNA slot blot hybridization in a coastal marine sediment. Environ. Microbiol. 1:65-74.
82. Wieringa EB, Overmann J, Cypionka H. 2000. Detection of abundant sulfate-reducing bacteria in marine oxic sediment layers by a combined cultivation and molecular approach. Environ. Microbiol. 2:417-427.
83. Rusch A, Huettel M, Reimers CE, Taghon GL, Fuller CM. 2003. Activity and distribution of bacterial populations in Middle Atlantic Bight shelf sands. FEMS Microbiol. Ecol. 44:89-100.
84. Mussmann M, Ishii K, Rabus R, Amann R. 2005. Diversity and vertical distribution of cultured and uncultured deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ. Microbiol. 7:405-418.
85. Musat N, Werner U, Knittel K, Kolb S, Dodenhof T, van Beusekom JE, de Beer D, Dubilier N, Amann R. 2006. Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Romo Basin, Wadden Sea. Syst. Appl. Microbiol. 29:333-348.
86. Carr SA, Vogel SW, Dunbar RB, Brandes J, Spear JR, Levy R, Naish TR, Powell RD, Wakeham SG, Mandernack KW. 2013. Bacterial abundance and composition in marine sediments beneath the Ross Ice Shelf, Antarctica. Geobiology 11:377-395.
87. Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Almendros C. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defense system. Microbiology 155:733-740.
88. 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.